Accepted Manuscript Regulation of photosynthesis during abiotic stress-induced photoinhibition Mayank Anand Gururani, Jelli Venkatesh, Lam-Son Phan Tran PII:
S1674-2052(15)00238-5
DOI:
10.1016/j.molp.2015.05.005
Reference:
MOLP 136
To appear in:
MOLECULAR PLANT
Received Date: 22 January 2015 Revised Date:
12 May 2015
Accepted Date: 12 May 2015
Please cite this article as: Gururani M.A., Venkatesh J., and Tran L.-S.P. (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol. Plant. doi: 10.1016/ j.molp.2015.05.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Regulation of photosynthesis during abiotic stress-induced photoinhibition
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Mayank Anand Gururani1, Jelli Venkatesh2, Lam-Son Phan Tran3
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School of Biotechnology, Yeungnam University, Gyeongsan, Gyeongbook 712-749, Korea
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Department of Bioresource and Food Science, Konkuk University, Seoul, 143-701, Korea
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Suehiro-cho, Tsurumi, Yokohama 230-0045, Japan
Running title: Photosynthesis under abiotic stress
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Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22,
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Corresponding author: Lam-Son Phan Tran
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Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama,
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Kanagawa, Japan Tel. +81-45-503-9593
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Fax. +81-45-503-9591
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Email: [email protected]
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Short Summary
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The current understanding of abiotic stress-induced photoinhibition in higher plants is reviewed.
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Furthermore, the mechanism of PSII damage-repair cycle and the involvement of various factors,
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such as phytohormones and transcription factors in regulation of photosynthetic machinery are
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discussed.
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ABSTRACT
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Plants as sessile organisms are continuously exposed to abiotic stress conditions that impose
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numerous detrimental effects on them, causing tremendous yield loss. Abiotic stresses, including
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high sunlight, confer serious damage to the photosynthetic machinery of the plants. Photosystem
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II (PSII) is one of the most susceptible components of the photosynthetic machinery that bears
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the brunt of abiotic stress. In addition to the generation of reactive oxygen species (ROS) by
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abiotic stress, ROS can also result from the absorption of excessive sunlight by the light-
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harvesting complex (LHC). ROS can damage the photosynthetic apparatus, particularly PSII,
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resulting in photoinhibition due to an imbalance in the photosynthetic redox signaling pathways
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and the inhibition of PSII repair. Designing plants with improved abiotic stress tolerance will
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require a comprehensive understanding of ROS signaling and regulatory functions of various
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components, including protein kinases, transcription factors and phytohormones, in responses of
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photosynthetic machinery to abiotic stress. Bioenergetics approaches, such as chlorophyll a
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transient kinetics analysis, have facilitated our understanding of plant vitality and the assessment
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of PSII efficiency under adverse environmental conditions. This review discusses the current
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understanding and indicates potential areas of further studies on the regulation of the
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photosynthetic machinery under abiotic stress.
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Key words: abiotic stress; chlorophyll a; fluorescence; hormones; light harvesting complex;
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photosynthesis; photosystem; redox signaling; transcription factors
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1. INTRODUCTION
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Photosynthesis is a multistep process of successive redox reactions that occur when the light-
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harvesting complexes (LHCs) absorb photonic energy and transfer it to photosystem (PS)
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reaction centers via excitons (Baker, 2008) (Figure 1). Abiotic stress caused by adverse
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environmental conditions, such as drought, heat, heavy metal toxicity and high light (HL),
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resulted in an over-reduction of the electron transport chain (ETC) which in turn leads to
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photooxidation (Foyer et al., 2012; Foyer and Noctor, 2005; Kangasjarvi et al., 2012; Nishiyama
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et al., 2006; Nishiyama and Murata, 2014; Rochaix, 2011; Takahashi and Murata, 2008). Plants
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have several mechanisms to overcome this problem, e.g. reducing the rate of electron transport
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by converting the excessively absorbed light into thermal energy. The dissipation of excess
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excitation energy as heat is known as non-photochemical quenching (NPQ) of chlorophyll
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fluorescence (Nath et al., 2013a; Rochaix, 2011; Spetea et al., 2014; Tikkanen et al., 2011). NPQ
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is a major photoprotective response as it reduces the concentration of chlorophyll excited states
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(Chl*) in PSII by activating a heat dissipation channel (Cazzaniga et al., 2013). Changes in the
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distribution and molecular orientation of chlorophyll proteins in the thylakoid membrane lead to
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the NPQ during HL stress (Herbstova et al., 2012; Johnson et al., 2011). Earlier studies have
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indicated that during abiotic stress, energized electrons are allocated to dioxygen (O2) (Baker,
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2008; Toth et al., 2011). This O2 is used in two vital photosynthetic reactions, photorespiration
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and the Mehler peroxidase (MP) reaction. In the MP reaction, O2 is reduced to superoxide (O2-)
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and the O2- to hydrogen peroxide (H2O2), both of which are potent reactive oxygen species
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(ROS) molecules. Consequently, less nicotinamide adenine dinucleotide phosphate (NADP+) is
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reduced which slows down the rate of CO2 fixation.
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2O2 + 2Fdred −→ 2O2•− + 2Fdox, where Fd is ferredoxin.
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Plants perceive stress signals through receptors that trigger molecular cascades to
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transmit the signals to regulatory systems via ion channels, signaling proteins, and secondary
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messengers (Choudhary et al., 2012; Le et al., 2012; Schmutz et al., 2010). The regulatory
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system is comprised of various components, including phytohormones, transcription factors
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(TFs), mitogen-activated protein kinases, and photosynthetic protein kinases and phosphatases,
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that regulate the expression of various stress-responsive genes (Foyer and Shigeoka, 2011;
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Osakabe et al., 2014; Puranik et al., 2012). Although the generation of ROS by abiotic stress and 3
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their detoxification have been extensively studied, the precise mechanisms underlying the
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distribution of ROS in specific cellular compartments are still unclear. Intracellular generation of
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H2O2, the most stable ROS, has always been associated with chloroplasts but recent studies
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suggest that peroxisomes may produce more H2O2 than other organelles (Noctor et al., 2014).
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The production of ROS in leaf tissues is regulated by the harvesting and distribution of light
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energy to the photosynthetic machinery (Tikkanen et al., 2014a). ROS are generated in
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chloroplasts within the ETCs of PSII and PSI during the light reactions, and their production is
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further increased during stress when carbon dioxide (CO2) is limited and ATP synthesis is
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impaired (Nishiyama and Murata, 2014; Noctor et al., 2014; Takahashi and Murata, 2008;
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Yamamoto et al., 2008). The damage to DNA, lipids and proteins by elevated levels of
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intracellular ROS is known as a result of oxidative stress (Foyer and Shigeoka, 2011; Schmutz et
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al., 2010). The detrimental effects of ROS accumulation in chloroplasts include the inhibition of
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de novo synthesis of D1 protein (also known as photosystem b A or PsbA) which is needed for
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PSII repair (Miyao, 1994; Nishiyama et al., 2011b; Tikkanen et al., 2011) (Figure 2),
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suppression of ROS-responsive chloroplastic enzymes (Kato and Sakamoto, 2014; Yoshioka et
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al., 2006), and the disarrangement of thylakoid architecture (Gratao et al., 2009). Recent studies
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in various organisms suggest that ROS also play pivotal roles as signaling molecules in normal
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biochemical and physiological responses (Foyer and Shigeoka, 2011; Schmutz et al., 2010;
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Tikkanen et al., 2014a). The level of intracellular ROS can be regulated by modulating the
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expression of genes that encode antioxidants, such as ascorbate or glutathione (Upadhyaya et al.,
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2011), or ROS-scavenging enzymes, such as peroxidases or dismutases (Schmutz et al., 2010;
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Takahashi and Murata, 2008). Even ROS-scavenging systems, however, do not completely
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remove intracellular ROS. Numerous reports have documented an increase in abiotic stress
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tolerance by the genetic manipulation of antioxidants and ROS-scavenging enzymes (Schmutz et
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al., 2010; Toth et al., 2011; Upadhyaya et al., 2011). Associating such modifications with
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cellular redox homeostasis and redox signaling, however, may be a more appropriate approach.
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2. IMPACT OF CELLULAR ROS PRODUCTION AND PHOTOINHIBITION ON THE
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PHOTOSYNTHETIC APPARATUS
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The PSII complex accomplishes the unique task of splitting water molecules and liberating
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molecular oxygen through an oxygen-evolving complex (OEC) (Gururani et al., 2012; Tikkanen
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and Aro, 2014; Yamamoto et al., 2008; Yi et al., 2005). The released electrons are then
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transferred to the PSI complex via ETC from plastocyanin to ferredoxin (Nellaepalli et al., 2014)
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(Figure 1). These reactions generate a high level of reactive oxygen radicals in PSII, which
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cause photodamage to the photosynthetic machinery (Henmi et al., 2004; Murata et al., 2007;
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Takahashi and Badger, 2011; Takahashi and Murata, 2008). One of the primary sources of PSII
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photodamage is the light-dependent disruption of OEC, which results in the release of
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manganese ions (Hakala et al., 2005; Henmi et al., 2004; Murata et al., 2007; Takahashi and
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Badger, 2011). The inhibition of PSII activity under continuous exposure to HL is commonly
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known as photoinhibition (Murata et al., 2007).
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Environmental stresses do not directly affect photoinhibition but rather facilitate the inhibition of PSII damage repair (Murata et al., 2007; Nishiyama et al., 2011b; Nishiyama and
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Murata, 2014). Several studies in plants and cyanobacteria have suggested that extent of
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photodamage to PSII is directly proportional to the intensity of incident light and that this
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proportionality remains unaffected by various environmental stresses (Allakhverdiev and Murata,
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2004; Gombos et al., 1994; Nishiyama et al., 2004; Takahashi and Murata, 2008). When light
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energy absorbed by the LHCII pigments is higher than the energy consumed, photoinhibition
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increases exponentially, thus causing severe damage to PSII (Nishiyama and Murata, 2014;
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Tikkanen and Aro, 2014). Superoxide anion radical or singlet oxygen (·O2-) is produced when
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more electrons are released in the ETC than the electron-consuming capacity of the Calvin cycle.
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The singlet oxygen is then converted to H2O2 by the action of superoxide dismutase (SOD)
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(Figure 1) (Nishiyama and Murata, 2014). According to the currently accepted scheme of PSII
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photoinhibition, ROS, such as superoxide radicals and singlet oxygen produced as a result of HL,
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high salinity (Allakhverdiev and Murata, 2004; Allakhverdiev et al., 2002; Ohnishi and Murata,
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2006), high or low temperature (Allakhverdiev et al., 2007; Allakhverdiev and Murata, 2004;
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Mohanty et al., 2007; Takahashi et al., 2009; Yang et al., 2007) and limited CO2 fixation
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(Takahashi and Murata, 2005; Takahashi and Murata, 2006; Wang et al., 2014), can inhibit the
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translation of PsbA mRNA, thus inactivating the PSII repair process (Figure 2H) (Nishiyama et
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al., 2006; Nishiyama et al., 2011b; Nishiyama and Murata, 2014; Takahashi and Murata, 2008).
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Accumulation of intracellular ROS depends on a balance between the generation and
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detoxification of ROS via various ROS-scavenging enzymes (Figure 1). This postulation makes
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the ROS-scavenging enzymes an obvious target to reduce the levels of ROS. Several studies
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suggest that decreased levels of intracellular ROS and reduced rate of photoinhibition can be
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achieved by engineering the production of ROS-scavenging enzymes, such as catalase (Al-
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Taweel et al., 2007; Miyagawa et al., 2000; Shikanai et al., 1998) and APX (Kornyeyev et al.,
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2003; Maruta et al., 2010; Murgia et al., 2004; Yabuta et al., 2002), in higher plants. Similarly,
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increased levels of low molecular weight antioxidants, such as α-tocopherol (vitamin E)
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(Demmig-Adams et al., 2013; Havaux et al., 2005) and carotenoids (Ramel et al., 2012; Stahl
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and Sies, 2003; Triantaphylides and Havaux, 2009), have also been proposed to reduce the level
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of singlet oxygen. On the basis of previous findings, it is reasonable to predict that increased
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activity of ROS-scavenging enzymes and increased accumulation of antioxidants might reduce
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the levels of intracellular ROS, thereby allowing the synthesis of D1 protein. PSI and PSII are
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associated with their respective light-absorbing antenna systems, LHCI and LHCII (Klimmek et
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al., 2006; Rochaix, 2014; Shapiguzov et al., 2010). In Arabidopsis thaliana, six and fifteen genes
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encoding the components of LHCI and LHCII, respectively, have been identified (Klimmek et al.,
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2006; Rochaix, 2014). The PSI complex is mainly comprised of 15 photosystem a (Psa) subunits,
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(PsaA - L and PsaN-P) (Nellaepalli et al., 2014; Rochaix, 2014). Chlorophyll molecules bound to
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PSI reaction centers act as light absorbing pigments, and the entire PSI complex is bound to its
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corresponding LHCI proteins (Amunts et al., 2010). The compositions of PSII and PSI antenna
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complexes are quite distinct, as LHCII mainly contains chlorophyll b while LHCI is enriched
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with chlorophyll a (Rochaix, 2014; Xu et al., 2012). Additionally, PSII-LHCII supercomplex
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contains a D1-D2 (or PsbA-PsbD) dimer coupled with two antennal proteins, the chlorophyll
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proteins (CPs) CP43 and CP47, and three minor proteins CP24, CP26 and CP29 (Che et al.,
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2013; de Bianchi et al., 2008). The entire PSII-LHCII supercomplex is embedded in the granum,
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while PSI is localized in the stromal lamellae of the chloroplasts (Rochaix, 2014).
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Recent studies on the acclimation of PSII-LHCII supercomplex during photoinhibition
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suggest that moderate phosphorylation of PSII under normal light results in efficient LHCII
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activity and slower PSII damage (Grieco et al., 2012; Nath et al., 2013a; Tikkanen and Aro,
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2014; Tikkanen et al., 2010). Under these conditions, the PSII-LHCII supercomplex remains
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intact and moderates the transfer of energy from LHCII to PSI. Moderate phosphorylation of
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LHCII allows the PSI complexes to move towards the grana margins, which ensures the transfer 6
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of adequate amounts of excitation energy to PSI. However, PSII proteins under HL conditions
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are phosphorylated at a much higher rate in order to negate the effect of photodamaged PSII
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complexes. The PSII-LHCII supercomplex loses its structural integrity, and the transfer of excess
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excitation energy from PSII-LHCII to PSI becomes unlimited (Grieco et al., 2012; Tikkanen and
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Aro, 2014; Tikkanen et al., 2010). Under conditions of continuous HL, dephosphorylation of
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LHCII inhibits any further transfer of energy to PSI (Tikkanen and Aro, 2014).
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Unlike PSII, PSI is not frequently damaged due to a very efficient mechanism that
protects it from photoinhibition. Photodamage to PSI is primarily caused when the supply of
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electrons from PSII exceeds the electron-accepting capacity of PSI, and once the PSI is damaged,
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the consequent recovery of PSI centers becomes very slow (Sonoike, 2011; Tikkanen et al.,
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2014b). Slow recovery of PSI centers in chilling stress-treated plant leaves has been reported in
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Arabidopsis (Zhang and Scheller, 2004), cucumber (Terashima et al., 1994; Kudoh and Sonoike,
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2002; Zhou et al., 2004, Zhang et al., 2014) and sweet pepper (Li et al., 2004). Apparently,
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photoinhibition in isolated thylakoids has been reported to be promptly induced under non-
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stressed conditions, whereas specific environmental conditions and specific plant species are
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required to induce photoinhibition under in vivo conditions (Sonoike, 2011). This is one of the
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most important factors that have limited our understanding of the putative protective mechanism
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of PSI photoinhibition. Nevertheless, several studies have indicated that the proton gradient-
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dependent or Cytb6f-mediated slowdown of ETC and LHCII-mediated excitation of PSII and
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PSI via NPQ and LHCII phosphorylation regulate the photoprotection of PSI in higher plants
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(Sonoike et al., 1995; Joliot and Johnson, 2011; Suorsa et al., 2012; Grieco et al., 2012).
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Recently, Tikkannen et al. (2014b) demonstrated that in addition to the above mentioned
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mechanisms, controlled photoinhibition of PSII regulates the ETC and prevents the formation of
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ROS and photodamage to PSI. Increased PSI-mediated cyclic electron flow was reported in
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Secale cereale plants subjected to chilling and high light stress, indicating the role of
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temperature/light-dependent acclimation in the induction of selective tolerance to PSI
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photoinhibition (Ivanov et al. 1998). Similarly, it has been reported that cyclic electron flow
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around PSI is required to produce a proton gradient that in turn leads to an efficient NPQ under
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heat stress in Ficus concinna trees (Jin et al., 2009).
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3. ROLE OF PSII PROTEIN PHOSPHORYLATION IN REGULATION OF D1
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DEGRADATION
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PSII, which is often referred to as the engine of life on earth, is the component of the
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photosynthetic machinery that is most susceptible to abiotic stresses (Nath et al., 2013a). Plants
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have evolved a mechanism for repairing PSII damage in order to attenuate photodamage and for
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the efficient functioning of PSII (Yamamoto et al., 2008). Photodamage caused by HL in plants
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can be determined by inhibiting the PSII repair process using chemicals like chloramphenicol or
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lincomycin that can inhibit the protein synthesis in the exposed plant cells (Murata et al., 2007).
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The PSII damage-repair cycle includes (i) phosphorylation and dephosphorylation of PSII
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proteins, (ii) disassembling of the PSII complex, (iii) proteolysis and de novo synthesis of D1
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protein, and (iv) reconstitution of the PSII complex (Bonardi et al., 2005; Nath et al., 2013a;
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Nixon et al., 2010; Samol et al., 2012; Tikkanen et al., 2014b) (Figure 2).
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Synchronizing the photosynthetic apparatus requires a balance between the excitation energies of PSII and PSI. This balance has been attributed to the ability to regulate the level of
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phosphorylation and dephosphorylation of LHCII and PSII proteins (Grieco et al., 2012;
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Tikkanen et al., 2010; Tikkanen et al., 2014b). Phosphorylation of LHCII and PSII proteins in
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Arabidopsis is facilitated by the state transition kinases, STN7 and STN8, respectively (Bonardi
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et al., 2005), while their dephosphorylation is triggered by thylakoid associated phosphatase 38
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(TAP38 or PPH1) (Pribil et al., 2010; Shapiguzov et al., 2010) and Psb core phosphatase (PBCP)
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(Samol et al., 2012), respectively (Figure 2). A recent study has demonstrated that TAP38/PPH1
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phosphatase was required to prevent the canonical state transition upon increase in light intensity
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(Nageswara et al., 2015).
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4. PROTEASES INVOLVED IN THE DEGRADATION AND SYNTHESIS OF D1
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PROTEIN
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PSII phosphorylation regulates the functional folding and macroscopic structure of plant
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thylakoid membranes (Fristedt et al., 2009; Nath et al., 2013a; Pribil et al., 2014). STN7-
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dependent phosphorylation appears to provide adequate levels of excitation energy to PSI to
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accomplish an efficient electron transfer from PSII to PSI (Grieco et al., 2012). Additionally, as a 8
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retrograde signaling kinase, STN7 is known to trigger the phosphorylation cascade, and thus
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regulating the expression of photosynthesis-related genes and assembly of the photosynthetic
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machinery (Tikkanen et al., 2012). The functional characterization of Arabidopsis stn8 single
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and stn7 × stn8 double mutants indicated that STN7 can phosphorylate LHCII, as well as PSII
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proteins to some extent, because complete inhibition of PSII phosphorylation was only observed
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in the stn7 x stn8 double mutant (Bonardi et al., 2005; Fristedt et al., 2009). In contrast, studies
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of a rice stn8 mutant revealed that Osstn8 alone can produce all of the phenotypes observed in
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Arabidopsis stn7 x stn8 mutants, indicating that distinctly specific regulatory mechanisms
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involving STN7 and STN8 exist in monocots vs. dicots (Nath et al., 2013b). Studies on
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TAP38/PPH1 have indicated that PPH1 may have other unknown function(s) besides STN7-
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mediated dephosphorylation of LHCII, as co-expression of PPH1 and STN7 was not detected
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(Nath et al., 2013a; Obayashi et al., 2009). Recent studies using Arabidopsis mutants with
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inactivated protein phosphatase 2C (PP2C)-type PBCP revealed that dephosphorylation of PSII
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subunits is crucial for efficient degradation of D1 (Puthiyaveetil et al., 2014). Additionally,
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PBCP has been found to regulate thylakoid stacking (Bonardi et al., 2005). Although the role of
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LHCII phosphorylation in PSII repair is still not clear, the phosphorylation of CP29, a minor
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subunit of LHCII, appears to be essential for the disassembly of the LHCII-PSII supercomplex
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(Fristedt and Vener, 2011).
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Reaction-center D1 protein is a key player in the PSII repair cycle (Nath et al., 2013a; Nishiyama and Murata, 2014; Rochaix, 2014; Tikkanen and Aro, 2014). The proteolysis and de
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novo synthesis of D1 protein during the PSII repair cycle are facilitated by chloroplastic
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proteases in the lumen, stroma and the thylakoid envelope (Che et al., 2013; Kapri-Pardes et al.,
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2007; Kato et al., 2009; Pribil et al., 2014; Schuhmann and Adamska, 2012; Sun et al., 2007).
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Serine-, metallo- and putative cysteine- and aspartic acid-proteases, have been identified, some
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of which require ATP (Pribil et al., 2014; Sakamoto, 2006; van der Hoorn, 2008). Presumably,
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many other proteases remain to be discovered. Known protease functions include chloroplastic
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biogenesis, degradation of signaling components, maintenance of chloroplastic homeostasis, and
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degradation of damaged proteins (Che et al., 2013; Sun et al., 2010a; Sun et al., 2010b; Yin et al.,
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2008). The current understanding of chloroplastic proteases that play pivotal roles in D1 protein
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processing and degradation are summarized in the next section and in Supplementary Table 1.
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4.1. Degradation (Deg) proteases
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Chloroplastic Deg proteases have received significant attention primarily due to their role in the
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degradation of photodamaged PSII proteins. The function of many of these proteases, however,
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remains to be determined. In plants, periplasmic degradation (Deg) proteases are ATP-
264
independent serine endopeptidases which are involved in the degradation of photodamaged
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proteins (Haussuhl et al., 2001; Sakamoto, 2006; Schuhmann and Adamska, 2012; Sun et al.,
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2010a; van der Hoorn, 2008) (Figure 2). Although these proteases were first discovered in
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Escherichia coli, they are present in most organisms (Schuhmann and Adamska, 2012).
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Arabidopsis contains 16 Deg proteases (Deg1-16) that, with the exception of Deg5, possess a C-
269
terminal protease domain and an N-terminal PDZ domain (Haussuhl et al., 2001). Deg proteases
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are present in chloroplasts, mitochondria, peroxisomes and nuclei (Schuhmann and Adamska,
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2012). Of the five known chloroplastic Deg proteases, Deg1, Deg5 and Deg8 are attached to the
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luminal side of thylakoid membranes, and Deg2 and Deg7 are in the stroma (Chi et al., 2012).
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Arabidopsis mutants with reduced levels of Deg1 exhibit enhanced sensitivity to photoinhibition
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and an increased accumulation of D1 protein; indicating that Deg1 plays a role in the degradation
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of D1 protein (Kapri-Pardes et al., 2007). In addition, recent studies in Arabidopsis have
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indicated the involvement of Deg1in the degradation of CP29 and CP26 proteins under
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photoinhibition (Zienkiewicz et al., 2012), and of Deg2 in degradation of CP24 under various
278
abiotic stress conditions (Lucinski et al., 2011). The Deg2 protease has been associated with
279
abiotic stress responses in plants. Arabidopsis deg2 mutants showed impaired activity to degrade
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CP24 in response to various abiotic stresses, such as high salinity, HL and wounding, indicating
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that Deg2 protease is required for plant growth and development under optimal as well as
282
stressed conditions (Lucinski et al., 2011). Interestingly, the effect of different abiotic stresses on
283
the accumulation of proteases is distinctive. For instance, 2- to 4-fold increase in the amount of
284
Deg2 was observed in Arabidopsis leaves treated with high salinity, desiccation or high
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irradiance for 2 h, while heat-treated leaves exhibited only trace amounts of Deg2 in the
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thylakoid membranes (Haussuhl et al., 2001).
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4.2. Filamentation temperature-sensitive H (FtsH) proteases
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FtsH proteases are ATP-dependent metalloproteases found in the thylakoids of higher-plant
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chloroplasts. Twelve genes encoding FtsH proteins have been identified in the Arabidopsis
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nuclear genome; nine of which (FtsH1, 2, 5-9, 11-12) are found in chloroplasts, three (FtsH3,4
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and 10) in mitochondria and one (FtsH11) in both chloroplasts and mitochondria (Yoshioka-
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Nishimura and Yamamoto, 2014). The exact location of the FtsH proteases in the thylakoid
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membrane still remains to be elucidated. Given their large hexameric form (Kirchhoff et al.,
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2011), however, it is most likely that they reside in the unstacked region of the thylakoid
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membrane rather than in the stacked grana. Early studies of Arabidopsis proteases suggested that
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Deg proteases initiated D1 degradation while further degradation was accomplished by FtsH
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proteases (Kapri-Pardes et al., 2007; Sun et al., 2010a; Sun et al., 2007). In contrast, recent
300
studies, using Arabidopsis deg and ftsH mutants, have suggested that FtsH proteins act as the
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initiating proteases and Deg as the assisting proteases in D1 protein degradation (Adam et al.,
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2011; Kato et al., 2012) (Figure 2). A recent study using transmission electron microscopy and
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immunogold labeling of FtsH in spinach leaves under HL stress revealed unstacking of
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thylakoids on the marginal regions of grana stacks, indicating a prominent role of thylakoid for
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efficient repair of photodamaged D1 proteins (Yoshioka-Nishimura et al., 2014). Interestingly,
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several reports have corroborated D1 phosphorylation and protease activity with abiotic stress
307
tolerance. It has been proposed that protein phosphorylation of D1 plays an important role in
308
protection of plants against the oxidative damage (Chen et al., 2012). Superoxide anions, H2O2
309
and hydroxyl radical are reportedly involved in the D1degradation under HL as one of the
310
initiating factors (Miyao, 1994; Miyao et al., 1995). Increased levels of H2O2 were found in
311
Arabidopsis mutants with limited FtsH activity. Apparently, the protein instability caused by
312
partial cleavage of D1 proteins led to cytotoxicity that resulted in increased levels of ROS (Kato
313
and Sakamoto, 2014). Earlier, FtsH was reported to be involved in D1 turnover in response to
314
heat stress in spinach (Yoshioka et al., 2006). One of the 12 known FtsHs, FtsH11 was proposed
315
to have a direct role in thermo-tolerance in Arabidopsis plants (Chen et al., 2006) and that
316
FtsH11 protects the photosynthesis apparatus from heat stress at all stages of plant development
317
(Chen et al., 2006).
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4.3. C-terminus-processing (Ctp) proteases
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Further processing of D1 protein by Ctp proteases is essential for the formation of fully
322
functional PSII complexes that are capable of splitting water (Chi et al., 2012; Yin et al., 2008)
323
(Figure 2). Unlike bacteria, in which many types of Ctp proteases exist, in plants, such as
324
Arabidopsis, only CtpA-type proteases have been identified (Che et al., 2013). Three genes
325
encoding CtpA-type proteases have been identified in Arabidopsis (Chi et al., 2012; Yin et al.,
326
2008). Characterization of CtpA1(CtpA/At3g57680) indicated that D1degradation significantly
327
increased in the Arabidopsis AtctpA1loss-of-function mutant. CtpA1 thus appears to be essential
328
for the efficient repair of PSII under HL (Yin et al., 2008). Additionally, functional analysis of
329
another CtpA/At4g17740 in Arabidopsis revealed that the loss of its activity led to a recovery of
330
D1 protein in its precursor form, indicating that CtpA/At4g17740 is essential for D1 C-terminal
331
processing, and thus PSII damage repair (Che et al., 2013). In order to determine the role of
332
cytokinin (CK) in HL-induced stress, expression of several Deg (Deg5 and Deg8) and FtsH
333
(FtsH1, FtsH2, FtsH5 and FtsH8) genes, as well as that of all three identified CtpA genes, were
334
analyzed in CK-deficient and wild-type (WT) Arabidopsis plants (Cortleven et al., 2014). No
335
significant difference in the expression of the examined FtsH and Deg genes were observed
336
between the WT and CK-deficient plants exposed to HL. While differences in the level of
337
expression of CtpA/At4g17740 and CtpA/At5g46390 in response to HL were non-significant in
338
the WT and CK-deficient plants, expression of AtCtpA1 was more strongly up-regulated by HL
339
in WT than in CK-deficient plants. These data suggest that HL-responsive expression of AtCtpA1
340
is CK-dependent. Additionally, AtCtpA1 mutants exhibited a WT-like response to HL (Cortleven
341
et al., 2014), indicating that AtCtpA1might act in concert with other proteins to regulate plant
342
response to HL.
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5. ASSESSMENT OF PHOTOSYSTEM II EFFICIENCY: MEASUREMENT OF
345
CHLOROPHYLL A FLUORESCENCE
346 347
The chlorophyll a fluorescence induction reflects the variations in chlorophyll a fluorescence
348
intensity, which occur when a photosynthetic specimen is moved from darkness to light
349
(Papageorgiou et al., 2007). The fluorescence induction is divided into two phases: (i) the fast
350
induction phase or the OJIP phase, in which O is origin, P is peak and J-I are the intermediate
351
phases, and (ii) the slow induction phase or PSMT phase in which P is peak, S is steady, M is 12
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maximum and T is the terminal state (Figure 3). The fast induction kinetics expresses the
353
primary photochemistry of PSII, while the slow kinetics is a complex phase primarily related to
354
the interactions between processes in the thylakoids and in the reductive carbon cycle of the
355
stroma (Krause and Weis 1984). In other words, slow induction phase is the light that is emitted
356
from photosynthetic specimen in the red-infra-red region of the spectrum for a short time after
357
the fast fluorescence has decayed. The fast phase of the transient provides relevant information
358
of the events that take place during the reduction of electron acceptors during ETC. On the other
359
hand, the slow transient phase is very difficult to be interpreted, primarily because several
360
different processes like non-photochemical quenching, ATP synthesis and Calvin–Benson cycle
361
begin to be involved during this phase (Stirbet and Govindjee, 2011). Nevertheless, the slow
362
fluorescence emission of PSII is considered as a useful approach to quantitatively study the light-
363
induced electron transfer and related events, such as proton movement, which are not detectable
364
by conventional spectroscopic methods (Goltsev et al., 2009). Over the years, researchers have
365
analyzed the slow fluorescence method to assess the plant’s performance under low temperature
366
(Itoh, 1980), high salinity (Zhang and Xing 2008), heavy metal stress (Plekhanov and Chemeris
367
2003), heat stress (Goltsev et al., 1987; Bilger and Schreiber 1990), drought (Mladenova et al.
368
1998), light stress (Valikhanov et al., 2002) and UV irradiation (Zhang et al., 2007a). Zhang et
369
al. (2007b) described a technique for detecting plant senescence based on quantitative
370
measurements of slow fluorescence and proposed that the changes in slow fluorescence intensity
371
reflect the changes in photosynthetic capacity and chlorophyll content during age-dependent and
372
hormone-modulated senescence (Zhang et al., 2007b). PSII efficiency under normal and stress
373
conditions can also be determined by fast chlorophyll a transient kinetics (Baker, 2008; Gururani
374
et al., 2012; Gururani et al., 2013; Gururani et al., 2015) (Figure 4). Analysis of fast chlorophyll
375
a transients has the potential to reveal interesting details pertaining to the alteration and
376
adjustment of the photosynthetic machinery during stress conditions. The reactivity of the
377
photosynthetic apparatus is important to the physiological status and vitality of plants subjected
378
to environmental stress. Measuring alterations of fast chlorophyll a fluorescence transients has
379
become a widely applied technique for assessing reactivity. Fluorescence (F) increases sharply
380
from F0 (minimum) to Fm (maximum) in dark-adapted plants exposed to a strong saturating light
381
pulse [3000-12000 µmol photons m-2 s-1, 200-1000 milliseconds (ms)]. At high temporal
382
resolution (0 to 200 ms), this increase can be seen as a polyphasic OJIP transient in three phases:
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OJ (0-3 ms), JI (3-30 ms) and IP (30-200 ms). Recent findings indicate that the increase from F0
384
to Fm may indicate the reduction of quinone (QA), the primary electron acceptor of PSII
385
(Schansker et al., 2014). The OJIP (or JIP) test elaborated by Strasser et al. (Strasser and Strasser,
386
1995; Strasser et al., 2004) is the main explanatory model used for explaining OJIP transients
387
(Baker, 2008; Baker and Rosenqvist, 2004; Maxwell and Johnson, 2000). The model compares
388
the photosynthetic activities of stressed and control plants and the test is a good, non-invasive
389
tool for analyzing the effects of a variety of stress factors on plants (Goltsev et al., 2012; Ranjan
390
et al., 2014; Toth et al., 2011; Zivcak et al., 2014a; Zivcak et al., 2014b). An analysis of
391
transgenic potato lines with altered photosystem b O (PsbO) production indicated a possible role
392
for this protein in enhanced potato tuberization and abiotic stress tolerance (Gururani et al., 2012;
393
Gururani et al., 2013). The exact mechanism behind the biochemical changes triggered by altered
394
production of PsbO, however, requires further investigation. A hypothetical model is provided
395
for the putative changes in the photosynthetic apparatus based on OJIP analyses (Figure 4).
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Chlorophyll a fluorescence transients provide extremely relevant information about PSII photochemistry and the events in the ETC. OJIP analysis simplifies this information through a
398
series of theoretical assumptions and mathematical calculations using specialized software. The
399
validity of some OJIP parameters has been a subject of debate among biophysicists (Stirbet and
400
Govindjee, 2011), but the acceptance of this analytical assessment of plant photosynthetic
401
efficiency and vitality will likely increase.
403 404
6. ROLE OF EXTRINSIC PROTEINS OF PSII IN D1 TURNOVER
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It is also imperative to recognize the role of extrinsic PSII proteins in D1 turnover in order to
406
fully understand the PSII repair cycle. The extrinsic proteins of PSII in higher plants mainly
407
include Psb subunits, PsbO, PsbP and PsbQ (Bricker et al., 2012). In vitro experiments with
408
spinach indicate that PSII devoid of PsbO becomes more vulnerable to photoinhibition and
409
accumulates significant amounts of D1 and CP43 (Henmi et al., 2004). PsbO may prevent
410
unnecessary interactions between photodamaged D1 and CP43, and the extended structure of
411
PsbO might protect the surface of D1 from reactive oxygen species (Yamamoto et al., 2008).
412
Moreover, PsbO has been proposed to function as GTPase and to regulate the phosphorylation
413
state of the D1 protein; a process that is associated with the efficient turnover of D1 protein
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during PSII repair (Aro et al., 2005; Bricker and Frankel, 2011; Lundin et al., 2007; Lundin et al.,
415
2008). PsbO-deficient potato plants exhibited reduced D1 and CP43 gene expression under a
416
normal light regimen (Gururani et al., 2012; Gururani et al., 2013). Specific roles for various
417
PsbO isoforms in oxygen evolution, PSII stability and plant growth have been identified (Lundin
418
et al., 2008). The precise mechanism of PsbO turnover and its putative role, in addition to the
419
stabilization of the oxygen-evolving complex, remains contentious and yet to be determined
420
(Kangasjarvi et al., 2012). Recent studies showed that removal of two intrinsic PSII proteins, the
421
PsbQ and PsbR, although resulted in only minor changes in terms of oxygen evolution and plant
422
growth, but showed a significant reduction in PSII activity and in PSII–LHCII super-complex
423
accumulation (Allahverdiyeva et al., 2013). Ishihara et al. (2007) demonstrated that a PsbP-like
424
protein 1 (PPL1) is required for the efficient repair of photodamaged PSII although the
425
underlying mechanism is not fully understood. PsbP, PsbQ and PsbR can be phosphorylated in
426
the thylakoid lumen (Ifuku, 2014; Reiland et al., 2009), indicating that their phosphorylation
427
might affect the assembly of PSII. On the other hand, removal of PsbP and PsbQ can induce
428
conformational changes in the arrangement of PSII protein assembly which includes the D1and
429
D2 proteins (Boekema et al., 2000; Bricker et al., 2012; Tomita et al., 2009). The addition or
430
removal of a phosphate group can alter protein conformation. Hence, examining putative
431
conformational changes in these extrinsic proteins during the PSII repair cycle would help
432
determine the state of phosphorylation of these proteins.
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7. INVOLVEMENT OF HORMONAL REGULATORY NETWORKS IN THE
435
RESPONSE OF PHOTOSYNTHETIC MACHINERY TO ABIOTIC STRESS
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Increasing evidence suggests that the interaction between phytohormones and cellular redox is an
438
essential aspect of the response of the photosynthetic structures to various abiotic stresses (Kim
439
et al., 2012; Krumova et al., 2013; Mayzlish-Gati et al., 2010). Recent studies using Arabidopsis
440
mutants with impaired photosynthetic light-harvesting indicated a strong interaction between the
441
control of excitation energy transfer and hormonal regulation (Tikkanen et al., 2014a). The
442
regulation of hormone metabolism by ROS generation and the intricacies of the crosstalk among
443
various hormones in response to various abiotic stresses have been extensively studied (Figure
444
5; Supplementary Table 2). In addition, a number of TFs have been shown to regulate 15
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photosynthesis through major hormonal pathways (Figure 5). For instance, TFs such as BZR1
446
and AtWRKY, were found to influence cell-wall and photosynthesis/chloroplast-related genes,
447
while a few TFs, for example GhDREB and CRF6 were shown to regulate PSII efficiency and
448
chlorophyll accumulation (Nguyen et al., 2014; Toledo-Ortiz et al., 2014; Waters et al., 2009;
449
Zhang et al., 2008). Supplementary Table 3 summarizes information on the recently identified
450
TFs that were found to be associated with the regulation of photosynthetic machinery under
451
normal and abiotic stress conditions.
452
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Brassinosteroids (BRs) play important roles in plant growth, defense, abiotic stress
tolerance, and the maintenance of high PSII efficiency and photosynthetic carbon fixation in
454
higher plants (Choudhary et al., 2012; Hu et al., 2013; Krumova et al., 2013; Oh et al., 2010).
455
Studies of BR-treated plants and BR-deficient mutants indicate a connection between BRs and
456
genes involved in photosynthesis (Bai et al., 2012; Oh et al., 2011). An Arabidopsis
457
brassinosteroid-insensitive 1(bri1) mutant exhibited a down-regulation of genes associated with
458
the regulation of photosynthesis and was characterized by stunted growth, reduced
459
photosynthetic activity, and a disrupted PSII assembly (Kim et al., 2012). Extensive microscopic,
460
fluorescence spectroscopic, and polarographic analyses of Arabidopsis mutants with altered BR
461
responses revealed enlarged thylakoids, smaller PSII complexes, inhibited oxygen evolution, and
462
reduced PSII quantum yields (Krumova et al., 2013). Komatsu et al. (2010) demonstrated that
463
BR deficiency led to an increased accumulation of chlorophyll and photosynthetic proteins that
464
changed the leaf color from green to dark-green. A brassinazole-insensitive pale green2-1
465
(BPG2) gene was proposed to mediate light-regulated chloroplast protein translation under BR-
466
deficient conditions. Exogenous application of BRs in pepper (Capsicum annuum) plants appear
467
to mitigate the deleterious effects of drought on photosynthesis by maintaining or increasing the
468
efficient use of light and NPQ in PSII antennae (Hu et al., 2013). Several other studies have
469
demonstrated BR-induced changes in thylakoid structure and the regulation of PSII and ETC in
470
photosynthesis (Dobrikova et al., 2014; Rothova et al., 2014). Therefore, the role of BRs in PSII
471
damage repair and in modification of thylakoid structural dynamics deserves further
472
investigation.
473
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Strigolactones (SLs), another group of phytohormones, may play an important role in
474
plants in the positive regulation of genes associated with harvesting light (Mashiguchi et al.,
475
2009). Several genes encoding light-harvesting chlorophyll a/b binding (LHCB) precursors, 16
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RuBisCO, and components of PSI and PSII are induced by GR24, a synthetic SL compound
477
(Mayzlish-Gati et al., 2010). In the Arabidopsis SL-signaling max2 mutant, the expression of
478
many genes involved in photosynthesis that are repressed by drought, were up-regulated,
479
especially in response to dehydration, in comparison to WT plants. These data indicate a
480
correlation between the mis-regulation of these genes and the reduced drought tolerance
481
observed in the max2 plants (Ha et al., 2014). Max2 plants may be more sensitive to the high
482
energy demands of photosynthesis, and thus require more resources even when the supply of the
483
resource is inadequate.
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Gibberellins (GAs) have been shown to regulate photosynthesis in addition to their
485
promotion of cell division and seed germination (Huerta et al., 2008; Zhou et al., 2011). In
486
addition, GA and kinetin (a type of CK) were reported to promote PSI and PSII activities by
487
influencing development of the photosynthetic electron transport system in greening cucumber
488
cotyledons (Pedhadiya et al., 1987). Short-term application of GA3 has been found to enhance
489
the net photosynthetic rate as well as the photosynthetic oxygen evolution in isolated broad bean
490
protoplasts (Yuan and Xu, 2001). Transgenic Brassica napus plants with decreased GA
491
bioactivity exhibited a significant increase in photosynthetic capacity (Zhou et al., 2011). In
492
contrast, transgenic citrange (Citrus sinensis x Poncirus trifoliata) plants with higher levels of
493
endogenous GA exhibited significant up-regulation of many genes involved in photosynthesis
494
and water stress alleviation (Huerta et al., 2008). A study in Arabidopsis reported that GA3-
495
treated WT plants or transgenic plants overexpressing a GA-responsive gene showed improved
496
tolerance to salt, oxidative and heat stress (Alonso-Ramirez et al., 2009). The increase in stress
497
tolerance was associated with higher levels of salicylic acid (SA), however, it was unclear if
498
photosynthesis was altered by the GA3 treatment or the increased endogenous level of GA level,
499
which might contribute to the improvement in stress tolerance. Further studies are required to
500
understand the effect of GAs on the relationship of photosynthesis to abiotic stress responses.
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Abscisic acid (ABA) is the hormone most extensively studied in relation to plant
502
response to abiotic stress. ABA has been reported to directly influence the photosynthetic oxygen
503
evolution connected with the functioning of PS II centers by disrupting the granal chloroplast
504
structure in barley (Maslenkova et al., 1989). Thermostability of photosynthetic apparatus was
505
significantly increased in ABA-treated barley seedlings under heat stress. Light scattering and
506
fluorescence analyses showed a reduced heat damage of the chloroplast ultrastructure and a 17
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marked decline in heat-induced increase in initial fluorescence (Fo) (Ivanov et al., 1992).
508
Exogenous application of ABA increases the content of total carotenoids, xanthophylls, and
509
chlorophyll in leaves (Barickman et al., 2014), thereby ameliorating the impact of excessive
510
excitation energy on PSII. Application of ABA also protects PSII by inducing an increase in
511
NPQ through the enhancement of xanthophyll-cycle pools and the de-epoxidation of
512
xanthophyll-cycle components (Zhu et al., 2011). The LHCB protein family plays an important
513
role in adaptation to environmental stress (Liu et al., 2013; Voigt et al., 2010). Contrary to the
514
initial belief that ABA was a negative regulator of the expression of LHCB genes (Staneloni et
515
al., 2008), ABA is believed to be required for the full expression of various LHCB genes (Xu et
516
al., 2012). Down-regulation of LHCB genes decreases ABA signaling and response to drought,
517
perhaps partly by modulating ROS homeostasis (Xu et al., 2012). The discrepancy regarding the
518
role of ABA in the regulation of photosynthesis may be attributed to the different experimental
519
systems and methods used to determine photosynthetic output.
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SA is a common phenolic compound well studied for its biochemical, physiological and plant growth regulation activities (El-Tayeb, 2005; Arfan et al., 2007). However, very little is
522
known about the SA-related mechanisms that control the maintenance of photosynthesis under
523
abiotic stress. Increased accumulation of endogenous SA levels was associated with a sharp
524
decrease in maximum PSII quantum yield (Fv/Fm) in leaves of Phillyrea angustifolia plants
525
exposed to drought (Munné-Bosch and Peñuelas, 2003). Improved photosynthetic capacity was
526
observed in SA-treated wheat plants under high salinity stress (Arfan et al., 2007). Similarly,
527
exogenous application of SA was reported to induce pre-adaptive responses to salt stress,
528
consequently improving and retaining the integrity of cell membranes in barley plants (El-Tayeb,
529
2005). SA-treated grapevine leaves showed accelerated recovery of net photosynthetic rate and
530
donor and acceptor parameters of PSII under heat stress. The authors concluded that the effects
531
of SA pre-treatment might be related to the enhanced levels of chloroplastic heat shock proteins,
532
resulting in improved net photosynetic rate (Wang et al., 2010). In a similar study, SA treatment
533
of wheat leaves enhanced Fv/Fm, actual photochemical efficiency of PSII and photosynthetic
534
electron transport rate, as well as improved net photosynthetic rate and reduced damages of heat
535
and high light stresses on D1 protein and PSII (Zhao et al., 2011).
536 537
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A small number of studies have also indicated that auxin, CK, jasmonic acid (JA) and ethylene may also play important roles in the stability of PSI and PSII, and thus in improvement 18
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of photosynthesis in plants exposed to abiotic stress (Supplementary Table 2). Transgenic
539
tobacco plants with enhanced endogenous CK level were reported to have increased transcript
540
abundance of genes associated with PSI, PSII and Cytb6f complex under drought stress.
541
Enhanced endogenous level of CK in transgenic plants appeared to promote the protection of
542
photosynthetic apparatus under prolonged drought conditions (Rivero et al., 2007, 2010).
543
Exogenous application of indole acetic acid, a plant hormone of auxin class and GA3 was
544
reported to reduce the effects of excessive copper mainly by maintaining the Fv/Fm and net
545
photosynthetic rate in sunflower plants (Ouzounidou and Ilias, 2005). Similarly, exogenous
546
application of ethylene was reported to regulate the protection of photosynthesis against Ni- and
547
Zn-induced heavy metal stress in Brassica juncea plants (Khan and Khan, 2014). Monitoring the
548
effects of exogenously applied hormones on photosynthesis is a valuable strategy but the
549
transcriptomic analysis of plant response to hormones in photosynthetic mutants would provide a
550
more detailed and comprehensive picture of the role of hormones in photosynthesis under normal
551
and abiotic stress conditions.
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As described earlier, apart from inducing LHCB genes (Liu et al., 2013; Voigt et al., 2010), ABA has been reported to regulate carotenoid biosynthesis (Barickman et al., 2014), an
554
important LHC pigment. Since both ABA and SLs are carotenoid-derived hormones, potential
555
crosstalk may exist between SLs, ABA, and light harvesting pathways. A BR-dependent, GA-
556
regulated transcriptome was recently found to be enriched with light-regulated genes and genes
557
involved in cell-wall synthesis and photosynthesis. Similar lines of evidence indicate a strong
558
association between various hormones and light-harvesting pathways (Attaran et al., 2014;
559
Cortleven et al., 2014; Staneloni et al., 2008). While BRs have been reported to modulate PSII
560
efficiency and thylakoid architecture (Dobrikova et al., 2014; Krumova et al., 2013; Oh et al.,
561
2011), SLs were demonstrated to act as positive regulators of light harvesting (Mayzlish-Gati et
562
al., 2010). Coordinated crosstalk among SL-, ABA-, and CK-signaling networks regulates the
563
adaptive response of plants to adverse environmental conditions (Ha et al., 2014; Nishiyama et
564
al., 2011a). For instance, increased accumulation of ethylene in drought-treated plants not only
565
enhances senescence but also disrupts ABA-mediated regulation of photosynthesis and leaf
566
growth (Bartoli et al., 2013). Therefore, the ratio of ethylene and ABA determines the plant
567
responses to drought, which further warrants a better understanding of crosstalk between these
568
hormones. Future efforts to determine the points of intersection that are involved in the co-
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569
regulation of hormones and light on photosynthetic components would help to enable the
570
identification of candidate genes that could be utilized to limit the level of photoinhibition in
571
chloroplasts when plants are subjected to abiotic stress.
572
8. FUTURE PERSPECTIVES
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Designing plants with increased levels of abiotic stress tolerance has been a major challenge for
576
researchers. This is partly due to a substantial lack of information on the intricacies of ROS
577
signaling, which limits the ability to determine its regulatory role in abiotic stress response.
578
Previous efforts have largely focused on gene expression studies, but RNA data alone is
579
insufficient. Transcriptomic, proteomic, and metabolomic analyses, novel cellular-imaging
580
techniques, and real-time detection tools would substantially enhance our understanding of ROS
581
signaling.
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Increasing the level of chloroplastic antioxidants or the activity of ROS-scavenging enzymes is clearly not a productive approach to improve crops. Alternative approaches, such as
584
modifying LHC and PSII components, have also been suggested as an alternative approach
585
(Horton, 2012; Tikkanen and Aro, 2014). The complex events associated with phosphorylation,
586
dephosphorylation, and the migration of thylakoid membrane proteins and reaction centers,
587
however, remain largely speculative. For example, the roles of STN7 and STN8 are known, but
588
it remains unclear if crosstalk exists in the regulation of these proteins. Moreover, recent findings
589
have suggested that the interaction between STN7 and STN8 is different in monocots and dicots
590
(Nath et al., 2013b). These observations also hold true for the role of minor LHCII antennal
591
proteins, because the phosphorylation of CP29 was reported to be species-specific (Chen et al.,
592
2009). Currently, little information is available on the phosphorylation of other minor antennal
593
proteins of LHCII. Similar ambiguities exist for the proteolytic mechanism and involvement of
594
ATP-dependent proteases in the PSII repair cycle. Contrasting reports and insufficient
595
knowledge on various proteases and intrinsic PSII proteins raises many questions, which only
596
further studies can answer. A major challenge will be to elucidate the linkage between the
597
identified kinases and phosphatases and their influence on the redox state of the photosynthetic
598
ETC. Identification of the substrates of proteases and determining their specificity would help to
599
understand their mode of action. In order to assess damage to photosynthetic machinery at a
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600
bioenergetic level, techniques such as chlorophyll a transient kinetics analysis are expected to
601
significantly contribute to our knowledge (Figure 4). The redox state of the photosynthetic ETC regulates the complex events during PSII
603
repair cycle as well as several other responses that involve the chloroplast and nuclear gene
604
expression. While the redox state of ETC is regulated by various environmental factors, the
605
chloroplast and nuclear gene expression can be transduced by changes in hormonal signaling
606
pathways. Therefore, changes in photosynthesis and levels of hormones in plants subjected to
607
environmental stresses should not be seen as isolated events, particularly given the emerging
608
evidence that indicates the involvement of phytohormones in PSII damage repair (Cortleven et
609
al., 2014). However, the extensive molecular connections among the signaling networks of
610
various hormones make it a daunting task to unravel the central roles of individual hormones in
611
coordinating the expression of photosynthetic genes and regulation of PSII damage repair.
612
Moreover, the physiological significance of changes in expression recorded in many abiotic
613
stress-responsive genes, particularly in those encoding photosynthetic proteins, is yet to be
614
understood. Genome-wide transcriptomic analyses of integrated hormonal regulatory networks
615
could provide a global view of their functions and molecular links with putative functions in the
616
regulation of photosynthesis. Additionally, it is important to use metabolomic and proteomic
617
approaches for understanding the metabolic responses of plants for photosynthetic acclimation to
618
various abiotic stresses. Such integration of different datasets would improve our understanding
619
of the physiological significance of hormones in regulation of photosynthesis performance under
620
abiotic stresses. Cellular responses to abiotic stresses also involve the transcriptional regulation
621
of photosynthetic metabolism. Several reports suggest that improved abiotic stress tolerance can
622
be achieved by engineering the expression of TFs (Puranik et al., 2012; Zhang et al., 2008)
623
(Supplementary Table 3). The involvement of these TFs in the regulation of genes associated
624
with photosynthesis, however, is still not clear. Taken together, designing plants with improved
625
abiotic stress tolerance and enhanced photosynthetic production will require a more
626
comprehensive understanding of the way photosynthetic machinery mediates the environmental
627
cues and the inherent metabolic signaling. Hence, it is crucial to focus on combining
628
interdisciplinary strategies from different research areas of plant sciences which could facilitate
629
the engineering of plant architecture in a sustainable way.
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ACKNOWLEDGEMENTS
632
This work was supported by the Scientific Research C Grant (no. 25440149) from Japan Society
633
for the Promotion of Science to L.-S. P. Tran.
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FIGURE LEGENDS
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Figure 1. Schematic Representation of Photosynthetic Redox Signals and the Detoxification
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of Reactive Oxygen Species (ROS). ROS, such as hydrogen peroxide (H2O2), generated in
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response to various stress factors, such as high irradiance (indicated by the red lightning bolt),
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and redox signals from the electron transport chain (ETC), initiate signaling cascades that
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eventually lead to nuclear-gene expression. In photosystem II (PSII), the splitting of water (H2O)
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at oxygen-evolving complex (OEC) produces H+ ions that are transferred across the membrane
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to ATP synthase (ATP syn), while electrons (e-) are transferred to PSI via the cytochrome b6f
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(Cytb6f) protein complex. Plastoquinone (Pq) accepts two protons (H+) from the stromal side
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along with two electrons (e-) from PSII and transfers the protons to the luminal side, while
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electrons are transferred to PSI via Cytb6f complex and plastocyanin (PC) pool. Electrons
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removed from water are transferred to the single-electron carrier ferredoxin (Fd). Ferredoxin
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NADP+ reductase (FNR) then transfers an electron from each of the two Fd molecules to a single
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molecule of the two-electron carrier nicotineamide adenine dinucleotide phosphate H (NADPH).
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Similarly, H+ ions from PSI are transferred to ATP synthase where proton gradients are used for
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producing ATP molecules from ADP. Electrons transferred from PSI via Fd are also converted
1258
into superoxide (O2-) in the Mehler peroxidase reaction (MP reaction). The O2- is detoxified by
1259
superoxide dismutase (SOD), a ROS-scavenging enzyme. Another ROS-scavenging enzyme,
1260
ascorbate peroxidase (APX), uses ascorbate (Asc) to reduce H2O2 to H2O. The scavenging of
1261
free radicals by APX increases the levels of monodehydroascorbate (MDA) and
1262
dehydroascorbate (DHA). High levels of MDA and DHA are reduced by MDA reductase
1263
(MDAR), DHA reductase (DHAR) and glutathione reductase (GR). During ascorbate-
1264
glutathione recycling, GR catalyzes the reduction of oxidized glutathione (GSSG) to GSH in
1265
order to maintain a higher ratio of GSH:GSSG in the cytosol. Initial reports indicated that
1266
residual H2O2 from incomplete detoxification can initiate mitogen-activated protein (MAP)
1267
kinases that in turn direct cellular responses such as nuclear-gene expression. Thioredoxins
1268
(TRXs) accept electrons from PSI and utilize them to phosphorylate the light-harvesting complex
1269
and possibly to induce nuclear-gene expression. Similarly, the plastoquinone (Pq) pool induces
1270
the expression of certain protein kinases and transcription factors (TFs) which can, in turn,
1271
trigger transcriptional-signal transduction in the nucleus.
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1272
Figure 2. Schematic Illustrating the Successive Steps of the Photosystem II (PSII) Repair
1274
Cycle after High Light Stress-Induced Photodamage. The photosystem II-light harvesting
1275
supercomplex (PSII-LHCII) has two components: (i) LHCII consists of a protein trimer (denoted
1276
as II) and three less abundant minor antennal chloroplast proteins (CPs), CP24, CP26 and CP29
1277
(denoted as 24, 26 and 29), and (ii) PSII which mainly consists of a D1-D2 (or PsbA-PsbD
1278
where Psb is photosystem b) heterodimer coupled with chlorophyll a containing CP43, CP47,
1279
PsbP (P), PsbQ (Q) and PsbO (O). (A) Photodamage is caused when light-absorbing antennae
1280
receive high-intensity light that damages D1 (denoted by cross-hatching). (B) To counter this
1281
damage, LHC dissipates the excess excitation energy in the form of heat via non-photochemical
1282
quenching. (C) After photodamage has occurred, the protein trimer of LHCII is phosphorylated
1283
by STN7, and the PSII proteins D1, D2 and CP43 are phosphorylated by STN8. Recent studies
1284
indicate, however, that STN7 can also phosphorylate PSII proteins to some extent (Bonardi et al.,
1285
2005; Fristedt et al., 2009; Nath et al., 2013b). The phosphorylation of one of the minor proteins
1286
of LHCII, CP29 (denoted in gray) has been found to be responsible for the disassembly of the
1287
PSII-LHCII supercomplex (Fristedt and Vener, 2011). (D) Phosphorylated proteins of the PSII-
1288
LHCII supercomplex are then dephosphorylated. Thylakoid associated phosphatase 38 (TAP38,
1289
yellow boxes) dephosphorylates LHCII proteins, and Psb core phosphatase (PBCP, brown
1290
polygons) dephosphorylates PSII proteins. (E) Dephosphorylation results in the disassembling of
1291
the PSII-LHCII supercomplex into a PSII repair intermediate and a peripheral antennal complex.
1292
(F) A zinc metalloprotease FtsH then recognizes the N-terminal of the photodamaged D1and
1293
degrades it in a complex processive manner (Adam et al., 2011). (G) ATP-independent Deg5 and
1294
Deg8 endoproteases further assist the processive degradation of photodamaged D1 protein by
1295
FtsH (Kato et al., 2012). (H) The proteolytic degradation of D1 is followed by the synthesis of
1296
nascent copies of D1 protein, facilitated by a plant-specific chloroplastic protease ClpA, which is
1297
involved in processing the C-terminus of D1. Plants possess highly efficient ROS-scavenging
1298
mechanisms, but ROS pose a major obstacle in this step by inhibiting the de novo synthesis of
1299
new D1 proteins. (I) Once nascent copies of D1 protein are synthesized and the co-translational
1300
assembly of D1 is completed, they are inserted into PSII and are post-translationally modified.
1301
Lastly, after the reassembly of its core components, PSII migrates toward the grana in its
1302
functional form.
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Figure 3. A General Representation of Chlorophyll Fluorescence Induction Curve in Plant
1304
Samples. When a dark-adapted plant sample is exposed to light, certain characteristic changes in
1305
chlorophyll fluorescence are observed. These changes are known as fluorescence induction or
1306
fluorescence transient, generally seen as two transient phases that are labeled by using the
1307
observed inflection points: (i) fast chlorophyll fluorescence induction (up to few hundred
1308
milliseconds) or the so-called OJIP phase where, O (origin) is the first measured minimum
1309
fluorescence level, P is the peak and J and I are intermediate inflections (ii) slow chlorophyll
1310
fluorescence induction or the PSMT phase where S stands for steady state, M for a maximum,
1311
and T for a terminal steady state level.
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1312
Figure 4. Hypothetical Scheme of a Multistep Electron Transport Chain, Based on the
1314
Emission Kinetics of Chlorophyll a. According to this scheme, the conversion of light energy
1315
to chemical energy begins with three consecutive basic steps, (i) ABS, absorption of light energy
1316
(photons) by chlorophyll molecules in the light-harvesting complex of photosystem II (PSII)
1317
(LHCII), (ii) TR, trapping of the excitation energy by the reaction center (RC) and (iii) ET,
1318
electron transport via PSII RCs (PSII-RC). When plant tissues are exposed to a short pulse of
1319
strong light, chlorophyll a (Chl a) absorbs the light energy and uses it in photosynthesis (Chl a*
1320
excited). At the same time, some light is emitted at a lower energy level as a function of time (Ft),
1321
a phenomenon called fluorescence emission. The fluorescence kinetics data is analyzed, and
1322
changes in the photosynthetic apparatus, such as the primary reaction of photochemistry, are
1323
derived through a series of equations, commonly known as the OJIP test (Strasser and Strasser,
1324
1995). Potato plants with altered expression of a PSII-related gene encoding the manganese
1325
stabilizing protein were analyzed with the OJIP test and a hypothesis for the putative changes in
1326
PSII was provided (Gururani et al., 2012; Gururani et al., 2013). The integrity of PSII after the
1327
primary reactions of photochemistry creates a primary redox (Red, reduction; Ox, oxidation)
1328
potential within and around PSII between a primary electron donor pigment P680+ and an electron
1329
acceptor, Quinone (Qa). Re-reduction of the primary electron donor pigment P680+ by internal
1330
electron donors occurs in in vitro systems using Hill reaction agents such as hydroxylamine (HA),
1331
Mn2+ and diphenylcarbazone (DPC). Re-reduction of the primary electron donor pigment (P680+)
1332
by internal electron donors also occurs in vivo. For example, tyrosine, ascorbate (Asc) and
1333
proline (Pro) are generally available as internal electron donors. The first chemical step occurs
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when an excited donor pigment molecule with a light absorption peak of 680 nm (P680) donates
1335
an electron to pheophytin (Ph), producing oxidized P680 (P680+) and reduced Ph (Ph-) in PSII. The
1336
oxygen-evolving complex (OEC) competes with the internal electron donation, where the
1337
reaction constant for splitting water, kW, is much lower than that of non-water electron donors
1338
(kD>>kW). Under various abiotic stress conditions, PSII is damaged, and the OEC then
1339
presumably favors electron donation by non-water electron donors with a high rate constant, kD.
1340
The total electron transport then increases as OEC activity decreases, due to the easy
1341
accessibility of non-water electrons from molecules such as Asc and Pro. The fraction of
1342
electrons donated by water is lower in stressed samples. Under normal conditions, an intact
1343
manganese cluster (Mn4CaO5) at the OEC thus promotes electron donation from water to PSII-
1344
RC with a low kW and reduces the accessibility of non-water electron donation to the RC of PSII.
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1345
Figure 5. Putative Involvement of Phytohormones and Representative Transcription
1347
Factors (TFs) in the Regulation of the Photosynthetic Machinery in Plants Under Abiotic
1348
Stress Conditions. Red dotted lines indicate crosstalk between two hormones that are inhibitory
1349
to each other. Green dotted lines indicate crosstalk between two hormones that up-regulate each
1350
other. ABA, abscisic acid; ARF2, auxin response factor 2 (Lim et al., 2010); AtNAC2,
1351
Arabidopsis thaliana NAC [NAM (no apical meristem), ATAF (Arabidopsis transcription
1352
activation factor) and CUC (cup-shaped cotyledon)] 2 TF (Ha et al., 2014); BR, brassinosteroid;
1353
BZR1, brassinazole resistant 1 TF (Bai et al., 2012); CRF6, cytokinin response factor 6 (Zwack
1354
et al., 2013); CK, cytokinin; Cytb6f, cytochrome b6f complex; ERF6, ethylene response factor 6
1355
(Dubois et al., 2013); GA, gibberellic acid; GhDREB1, Gossypium hirusitum dehydration-
1356
responsive element binding protein 1 (Shan et al., 2007); JA, jasmonic acid; MYC 2,
1357
myelocytomatosis 2 TF (Dombrecht et al., 2007); PSI, photosystem I; PSII, photosystem II; ROS,
1358
reactive oxygen species; SA, salicylic acid; SL, strigolactone; SlZF2, Solanum lycopersicum
1359
Zinc Finger2 TF (Hichri et al., 2014); OsWRKY45 (Chao et al., 2010), Oryza sativa WRKY45,
1360
a TF belonging to the WRKY TF family that derives its name from the protein sequence motif
1361
WRKYGQK.
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Chloroplast
ATP ADP
Fd
SOD
MDAR
PS I NADP+
APx
MDA
DHA PC
DHAR
e-
TRs
PS II
2H2O lumen
stroma
Thylakoid
H2O
MDA
DHA
GSSG
GR
GSH
Asc-glutathione recycling
MAP Kinase
EP
OEC
H2O
MDAR
TFs, Kinases H+
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O2 + 4H+
Pq e-
Asc
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Cytb6f
APx
Asc
Asc
NADPH
e-
H2O2
SC
FNR
MP O2reaction
M AN U
O2
Nuclear gene expression
DHAR
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A
B
II
II
II
24 26 29
P
II
24 26 29
SC
D1 D2 47 43 damaged D1 Q P O
M AN U
Reconstitution of PSII components
I
C-terminal processing
H
D1 processing
D1 43
AC C
D2 47
Co-translational assembly CtpA
24 26 29
G
D2 47 P Q P O
P D1
43
P
STN8 Dephosphorylation TAP38 II
II
D
24 26 29
D1 43
D2 47
PBCP FtsH
EP
Post-translational assembly of PSII proteins ROS
D1 43
TE D
D1 D2 47 43 P Q O
Membrane insertion
II
Phosphorylation
D1 D2 47 43 Q P O
Protein trafficking
P
II
Photodamage
lumen
C
STN7
Heat
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stroma
D2 47
D1 43
Disassembly
D2 47
Proteolysis
PSII repair intermediate
Deg D1 degradtion
F
Peripheral antenna
E
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Chl a*
SC
Chl a
RI PT
ABS
*
Mn4CaO5
Ox O2 + H+ OEC
-
-
-
kD
Tyrosine
Asc
-
HA
QA -
ET
QA
P680Ph
-
kD DPC Pro Non-water electron donors
Mn2+
Ph-
P680+
EP
Red kW
AC C
H2O
TE D
Ft
M AN U
TR
LHCII
PSII-RC
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PS II
RI PT
Stress PS I
Cytb6f
SC
Stress signal perception
GA
JA
SA
ABA
TE D
Hormonal regulation
M AN U
ROS
AC C
Structural and functional adaptations
ARF2
BR
SL
BZR1
AtNAC2
CK
CRF6
EP
Transcriptional GhDREB1 OsWRKY45 MYC2 SlZF2 control
Auxin
Regulation of photosynthetic machinery
Ethylene
ERF6
S1674-2052(15)00238-5
DOI:
10.1016/j.molp.2015.05.005
Reference:
MOLP 136
To appear in:
MOLECULAR PLANT
Received Date: 22 January 2015 Revised Date:
12 May 2015
Accepted Date: 12 May 2015
Please cite this article as: Gururani M.A., Venkatesh J., and Tran L.-S.P. (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol. Plant. doi: 10.1016/ j.molp.2015.05.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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1
Regulation of photosynthesis during abiotic stress-induced photoinhibition
2
Mayank Anand Gururani1, Jelli Venkatesh2, Lam-Son Phan Tran3
3 1
School of Biotechnology, Yeungnam University, Gyeongsan, Gyeongbook 712-749, Korea
5
2
Department of Bioresource and Food Science, Konkuk University, Seoul, 143-701, Korea
6
3
7
Suehiro-cho, Tsurumi, Yokohama 230-0045, Japan
Running title: Photosynthesis under abiotic stress
10
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Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22,
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Corresponding author: Lam-Son Phan Tran
12
Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama,
13
Kanagawa, Japan Tel. +81-45-503-9593
14
Fax. +81-45-503-9591
15
Email: [email protected]
16
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Short Summary
18
The current understanding of abiotic stress-induced photoinhibition in higher plants is reviewed.
19
Furthermore, the mechanism of PSII damage-repair cycle and the involvement of various factors,
20
such as phytohormones and transcription factors in regulation of photosynthetic machinery are
21
discussed.
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ABSTRACT
23
Plants as sessile organisms are continuously exposed to abiotic stress conditions that impose
25
numerous detrimental effects on them, causing tremendous yield loss. Abiotic stresses, including
26
high sunlight, confer serious damage to the photosynthetic machinery of the plants. Photosystem
27
II (PSII) is one of the most susceptible components of the photosynthetic machinery that bears
28
the brunt of abiotic stress. In addition to the generation of reactive oxygen species (ROS) by
29
abiotic stress, ROS can also result from the absorption of excessive sunlight by the light-
30
harvesting complex (LHC). ROS can damage the photosynthetic apparatus, particularly PSII,
31
resulting in photoinhibition due to an imbalance in the photosynthetic redox signaling pathways
32
and the inhibition of PSII repair. Designing plants with improved abiotic stress tolerance will
33
require a comprehensive understanding of ROS signaling and regulatory functions of various
34
components, including protein kinases, transcription factors and phytohormones, in responses of
35
photosynthetic machinery to abiotic stress. Bioenergetics approaches, such as chlorophyll a
36
transient kinetics analysis, have facilitated our understanding of plant vitality and the assessment
37
of PSII efficiency under adverse environmental conditions. This review discusses the current
38
understanding and indicates potential areas of further studies on the regulation of the
39
photosynthetic machinery under abiotic stress.
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Key words: abiotic stress; chlorophyll a; fluorescence; hormones; light harvesting complex;
42
photosynthesis; photosystem; redox signaling; transcription factors
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1. INTRODUCTION
45
Photosynthesis is a multistep process of successive redox reactions that occur when the light-
47
harvesting complexes (LHCs) absorb photonic energy and transfer it to photosystem (PS)
48
reaction centers via excitons (Baker, 2008) (Figure 1). Abiotic stress caused by adverse
49
environmental conditions, such as drought, heat, heavy metal toxicity and high light (HL),
50
resulted in an over-reduction of the electron transport chain (ETC) which in turn leads to
51
photooxidation (Foyer et al., 2012; Foyer and Noctor, 2005; Kangasjarvi et al., 2012; Nishiyama
52
et al., 2006; Nishiyama and Murata, 2014; Rochaix, 2011; Takahashi and Murata, 2008). Plants
53
have several mechanisms to overcome this problem, e.g. reducing the rate of electron transport
54
by converting the excessively absorbed light into thermal energy. The dissipation of excess
55
excitation energy as heat is known as non-photochemical quenching (NPQ) of chlorophyll
56
fluorescence (Nath et al., 2013a; Rochaix, 2011; Spetea et al., 2014; Tikkanen et al., 2011). NPQ
57
is a major photoprotective response as it reduces the concentration of chlorophyll excited states
58
(Chl*) in PSII by activating a heat dissipation channel (Cazzaniga et al., 2013). Changes in the
59
distribution and molecular orientation of chlorophyll proteins in the thylakoid membrane lead to
60
the NPQ during HL stress (Herbstova et al., 2012; Johnson et al., 2011). Earlier studies have
61
indicated that during abiotic stress, energized electrons are allocated to dioxygen (O2) (Baker,
62
2008; Toth et al., 2011). This O2 is used in two vital photosynthetic reactions, photorespiration
63
and the Mehler peroxidase (MP) reaction. In the MP reaction, O2 is reduced to superoxide (O2-)
64
and the O2- to hydrogen peroxide (H2O2), both of which are potent reactive oxygen species
65
(ROS) molecules. Consequently, less nicotinamide adenine dinucleotide phosphate (NADP+) is
66
reduced which slows down the rate of CO2 fixation.
67
2O2 + 2Fdred −→ 2O2•− + 2Fdox, where Fd is ferredoxin.
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Plants perceive stress signals through receptors that trigger molecular cascades to
69
transmit the signals to regulatory systems via ion channels, signaling proteins, and secondary
70
messengers (Choudhary et al., 2012; Le et al., 2012; Schmutz et al., 2010). The regulatory
71
system is comprised of various components, including phytohormones, transcription factors
72
(TFs), mitogen-activated protein kinases, and photosynthetic protein kinases and phosphatases,
73
that regulate the expression of various stress-responsive genes (Foyer and Shigeoka, 2011;
74
Osakabe et al., 2014; Puranik et al., 2012). Although the generation of ROS by abiotic stress and 3
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their detoxification have been extensively studied, the precise mechanisms underlying the
76
distribution of ROS in specific cellular compartments are still unclear. Intracellular generation of
77
H2O2, the most stable ROS, has always been associated with chloroplasts but recent studies
78
suggest that peroxisomes may produce more H2O2 than other organelles (Noctor et al., 2014).
79
The production of ROS in leaf tissues is regulated by the harvesting and distribution of light
80
energy to the photosynthetic machinery (Tikkanen et al., 2014a). ROS are generated in
81
chloroplasts within the ETCs of PSII and PSI during the light reactions, and their production is
82
further increased during stress when carbon dioxide (CO2) is limited and ATP synthesis is
83
impaired (Nishiyama and Murata, 2014; Noctor et al., 2014; Takahashi and Murata, 2008;
84
Yamamoto et al., 2008). The damage to DNA, lipids and proteins by elevated levels of
85
intracellular ROS is known as a result of oxidative stress (Foyer and Shigeoka, 2011; Schmutz et
86
al., 2010). The detrimental effects of ROS accumulation in chloroplasts include the inhibition of
87
de novo synthesis of D1 protein (also known as photosystem b A or PsbA) which is needed for
88
PSII repair (Miyao, 1994; Nishiyama et al., 2011b; Tikkanen et al., 2011) (Figure 2),
89
suppression of ROS-responsive chloroplastic enzymes (Kato and Sakamoto, 2014; Yoshioka et
90
al., 2006), and the disarrangement of thylakoid architecture (Gratao et al., 2009). Recent studies
91
in various organisms suggest that ROS also play pivotal roles as signaling molecules in normal
92
biochemical and physiological responses (Foyer and Shigeoka, 2011; Schmutz et al., 2010;
93
Tikkanen et al., 2014a). The level of intracellular ROS can be regulated by modulating the
94
expression of genes that encode antioxidants, such as ascorbate or glutathione (Upadhyaya et al.,
95
2011), or ROS-scavenging enzymes, such as peroxidases or dismutases (Schmutz et al., 2010;
96
Takahashi and Murata, 2008). Even ROS-scavenging systems, however, do not completely
97
remove intracellular ROS. Numerous reports have documented an increase in abiotic stress
98
tolerance by the genetic manipulation of antioxidants and ROS-scavenging enzymes (Schmutz et
99
al., 2010; Toth et al., 2011; Upadhyaya et al., 2011). Associating such modifications with
101
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cellular redox homeostasis and redox signaling, however, may be a more appropriate approach.
102
2. IMPACT OF CELLULAR ROS PRODUCTION AND PHOTOINHIBITION ON THE
103
PHOTOSYNTHETIC APPARATUS
104
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The PSII complex accomplishes the unique task of splitting water molecules and liberating
106
molecular oxygen through an oxygen-evolving complex (OEC) (Gururani et al., 2012; Tikkanen
107
and Aro, 2014; Yamamoto et al., 2008; Yi et al., 2005). The released electrons are then
108
transferred to the PSI complex via ETC from plastocyanin to ferredoxin (Nellaepalli et al., 2014)
109
(Figure 1). These reactions generate a high level of reactive oxygen radicals in PSII, which
110
cause photodamage to the photosynthetic machinery (Henmi et al., 2004; Murata et al., 2007;
111
Takahashi and Badger, 2011; Takahashi and Murata, 2008). One of the primary sources of PSII
112
photodamage is the light-dependent disruption of OEC, which results in the release of
113
manganese ions (Hakala et al., 2005; Henmi et al., 2004; Murata et al., 2007; Takahashi and
114
Badger, 2011). The inhibition of PSII activity under continuous exposure to HL is commonly
115
known as photoinhibition (Murata et al., 2007).
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Environmental stresses do not directly affect photoinhibition but rather facilitate the inhibition of PSII damage repair (Murata et al., 2007; Nishiyama et al., 2011b; Nishiyama and
118
Murata, 2014). Several studies in plants and cyanobacteria have suggested that extent of
119
photodamage to PSII is directly proportional to the intensity of incident light and that this
120
proportionality remains unaffected by various environmental stresses (Allakhverdiev and Murata,
121
2004; Gombos et al., 1994; Nishiyama et al., 2004; Takahashi and Murata, 2008). When light
122
energy absorbed by the LHCII pigments is higher than the energy consumed, photoinhibition
123
increases exponentially, thus causing severe damage to PSII (Nishiyama and Murata, 2014;
124
Tikkanen and Aro, 2014). Superoxide anion radical or singlet oxygen (·O2-) is produced when
125
more electrons are released in the ETC than the electron-consuming capacity of the Calvin cycle.
126
The singlet oxygen is then converted to H2O2 by the action of superoxide dismutase (SOD)
127
(Figure 1) (Nishiyama and Murata, 2014). According to the currently accepted scheme of PSII
128
photoinhibition, ROS, such as superoxide radicals and singlet oxygen produced as a result of HL,
129
high salinity (Allakhverdiev and Murata, 2004; Allakhverdiev et al., 2002; Ohnishi and Murata,
130
2006), high or low temperature (Allakhverdiev et al., 2007; Allakhverdiev and Murata, 2004;
131
Mohanty et al., 2007; Takahashi et al., 2009; Yang et al., 2007) and limited CO2 fixation
132
(Takahashi and Murata, 2005; Takahashi and Murata, 2006; Wang et al., 2014), can inhibit the
133
translation of PsbA mRNA, thus inactivating the PSII repair process (Figure 2H) (Nishiyama et
134
al., 2006; Nishiyama et al., 2011b; Nishiyama and Murata, 2014; Takahashi and Murata, 2008).
135
Accumulation of intracellular ROS depends on a balance between the generation and
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detoxification of ROS via various ROS-scavenging enzymes (Figure 1). This postulation makes
137
the ROS-scavenging enzymes an obvious target to reduce the levels of ROS. Several studies
138
suggest that decreased levels of intracellular ROS and reduced rate of photoinhibition can be
139
achieved by engineering the production of ROS-scavenging enzymes, such as catalase (Al-
140
Taweel et al., 2007; Miyagawa et al., 2000; Shikanai et al., 1998) and APX (Kornyeyev et al.,
141
2003; Maruta et al., 2010; Murgia et al., 2004; Yabuta et al., 2002), in higher plants. Similarly,
142
increased levels of low molecular weight antioxidants, such as α-tocopherol (vitamin E)
143
(Demmig-Adams et al., 2013; Havaux et al., 2005) and carotenoids (Ramel et al., 2012; Stahl
144
and Sies, 2003; Triantaphylides and Havaux, 2009), have also been proposed to reduce the level
145
of singlet oxygen. On the basis of previous findings, it is reasonable to predict that increased
146
activity of ROS-scavenging enzymes and increased accumulation of antioxidants might reduce
147
the levels of intracellular ROS, thereby allowing the synthesis of D1 protein. PSI and PSII are
148
associated with their respective light-absorbing antenna systems, LHCI and LHCII (Klimmek et
149
al., 2006; Rochaix, 2014; Shapiguzov et al., 2010). In Arabidopsis thaliana, six and fifteen genes
150
encoding the components of LHCI and LHCII, respectively, have been identified (Klimmek et al.,
151
2006; Rochaix, 2014). The PSI complex is mainly comprised of 15 photosystem a (Psa) subunits,
152
(PsaA - L and PsaN-P) (Nellaepalli et al., 2014; Rochaix, 2014). Chlorophyll molecules bound to
153
PSI reaction centers act as light absorbing pigments, and the entire PSI complex is bound to its
154
corresponding LHCI proteins (Amunts et al., 2010). The compositions of PSII and PSI antenna
155
complexes are quite distinct, as LHCII mainly contains chlorophyll b while LHCI is enriched
156
with chlorophyll a (Rochaix, 2014; Xu et al., 2012). Additionally, PSII-LHCII supercomplex
157
contains a D1-D2 (or PsbA-PsbD) dimer coupled with two antennal proteins, the chlorophyll
158
proteins (CPs) CP43 and CP47, and three minor proteins CP24, CP26 and CP29 (Che et al.,
159
2013; de Bianchi et al., 2008). The entire PSII-LHCII supercomplex is embedded in the granum,
160
while PSI is localized in the stromal lamellae of the chloroplasts (Rochaix, 2014).
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Recent studies on the acclimation of PSII-LHCII supercomplex during photoinhibition
162
suggest that moderate phosphorylation of PSII under normal light results in efficient LHCII
163
activity and slower PSII damage (Grieco et al., 2012; Nath et al., 2013a; Tikkanen and Aro,
164
2014; Tikkanen et al., 2010). Under these conditions, the PSII-LHCII supercomplex remains
165
intact and moderates the transfer of energy from LHCII to PSI. Moderate phosphorylation of
166
LHCII allows the PSI complexes to move towards the grana margins, which ensures the transfer 6
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of adequate amounts of excitation energy to PSI. However, PSII proteins under HL conditions
168
are phosphorylated at a much higher rate in order to negate the effect of photodamaged PSII
169
complexes. The PSII-LHCII supercomplex loses its structural integrity, and the transfer of excess
170
excitation energy from PSII-LHCII to PSI becomes unlimited (Grieco et al., 2012; Tikkanen and
171
Aro, 2014; Tikkanen et al., 2010). Under conditions of continuous HL, dephosphorylation of
172
LHCII inhibits any further transfer of energy to PSI (Tikkanen and Aro, 2014).
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Unlike PSII, PSI is not frequently damaged due to a very efficient mechanism that
protects it from photoinhibition. Photodamage to PSI is primarily caused when the supply of
175
electrons from PSII exceeds the electron-accepting capacity of PSI, and once the PSI is damaged,
176
the consequent recovery of PSI centers becomes very slow (Sonoike, 2011; Tikkanen et al.,
177
2014b). Slow recovery of PSI centers in chilling stress-treated plant leaves has been reported in
178
Arabidopsis (Zhang and Scheller, 2004), cucumber (Terashima et al., 1994; Kudoh and Sonoike,
179
2002; Zhou et al., 2004, Zhang et al., 2014) and sweet pepper (Li et al., 2004). Apparently,
180
photoinhibition in isolated thylakoids has been reported to be promptly induced under non-
181
stressed conditions, whereas specific environmental conditions and specific plant species are
182
required to induce photoinhibition under in vivo conditions (Sonoike, 2011). This is one of the
183
most important factors that have limited our understanding of the putative protective mechanism
184
of PSI photoinhibition. Nevertheless, several studies have indicated that the proton gradient-
185
dependent or Cytb6f-mediated slowdown of ETC and LHCII-mediated excitation of PSII and
186
PSI via NPQ and LHCII phosphorylation regulate the photoprotection of PSI in higher plants
187
(Sonoike et al., 1995; Joliot and Johnson, 2011; Suorsa et al., 2012; Grieco et al., 2012).
188
Recently, Tikkannen et al. (2014b) demonstrated that in addition to the above mentioned
189
mechanisms, controlled photoinhibition of PSII regulates the ETC and prevents the formation of
190
ROS and photodamage to PSI. Increased PSI-mediated cyclic electron flow was reported in
191
Secale cereale plants subjected to chilling and high light stress, indicating the role of
192
temperature/light-dependent acclimation in the induction of selective tolerance to PSI
193
photoinhibition (Ivanov et al. 1998). Similarly, it has been reported that cyclic electron flow
194
around PSI is required to produce a proton gradient that in turn leads to an efficient NPQ under
195
heat stress in Ficus concinna trees (Jin et al., 2009).
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3. ROLE OF PSII PROTEIN PHOSPHORYLATION IN REGULATION OF D1
198
DEGRADATION
199
PSII, which is often referred to as the engine of life on earth, is the component of the
201
photosynthetic machinery that is most susceptible to abiotic stresses (Nath et al., 2013a). Plants
202
have evolved a mechanism for repairing PSII damage in order to attenuate photodamage and for
203
the efficient functioning of PSII (Yamamoto et al., 2008). Photodamage caused by HL in plants
204
can be determined by inhibiting the PSII repair process using chemicals like chloramphenicol or
205
lincomycin that can inhibit the protein synthesis in the exposed plant cells (Murata et al., 2007).
206
The PSII damage-repair cycle includes (i) phosphorylation and dephosphorylation of PSII
207
proteins, (ii) disassembling of the PSII complex, (iii) proteolysis and de novo synthesis of D1
208
protein, and (iv) reconstitution of the PSII complex (Bonardi et al., 2005; Nath et al., 2013a;
209
Nixon et al., 2010; Samol et al., 2012; Tikkanen et al., 2014b) (Figure 2).
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Synchronizing the photosynthetic apparatus requires a balance between the excitation energies of PSII and PSI. This balance has been attributed to the ability to regulate the level of
212
phosphorylation and dephosphorylation of LHCII and PSII proteins (Grieco et al., 2012;
213
Tikkanen et al., 2010; Tikkanen et al., 2014b). Phosphorylation of LHCII and PSII proteins in
214
Arabidopsis is facilitated by the state transition kinases, STN7 and STN8, respectively (Bonardi
215
et al., 2005), while their dephosphorylation is triggered by thylakoid associated phosphatase 38
216
(TAP38 or PPH1) (Pribil et al., 2010; Shapiguzov et al., 2010) and Psb core phosphatase (PBCP)
217
(Samol et al., 2012), respectively (Figure 2). A recent study has demonstrated that TAP38/PPH1
218
phosphatase was required to prevent the canonical state transition upon increase in light intensity
219
(Nageswara et al., 2015).
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4. PROTEASES INVOLVED IN THE DEGRADATION AND SYNTHESIS OF D1
222
PROTEIN
223 224
PSII phosphorylation regulates the functional folding and macroscopic structure of plant
225
thylakoid membranes (Fristedt et al., 2009; Nath et al., 2013a; Pribil et al., 2014). STN7-
226
dependent phosphorylation appears to provide adequate levels of excitation energy to PSI to
227
accomplish an efficient electron transfer from PSII to PSI (Grieco et al., 2012). Additionally, as a 8
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retrograde signaling kinase, STN7 is known to trigger the phosphorylation cascade, and thus
229
regulating the expression of photosynthesis-related genes and assembly of the photosynthetic
230
machinery (Tikkanen et al., 2012). The functional characterization of Arabidopsis stn8 single
231
and stn7 × stn8 double mutants indicated that STN7 can phosphorylate LHCII, as well as PSII
232
proteins to some extent, because complete inhibition of PSII phosphorylation was only observed
233
in the stn7 x stn8 double mutant (Bonardi et al., 2005; Fristedt et al., 2009). In contrast, studies
234
of a rice stn8 mutant revealed that Osstn8 alone can produce all of the phenotypes observed in
235
Arabidopsis stn7 x stn8 mutants, indicating that distinctly specific regulatory mechanisms
236
involving STN7 and STN8 exist in monocots vs. dicots (Nath et al., 2013b). Studies on
237
TAP38/PPH1 have indicated that PPH1 may have other unknown function(s) besides STN7-
238
mediated dephosphorylation of LHCII, as co-expression of PPH1 and STN7 was not detected
239
(Nath et al., 2013a; Obayashi et al., 2009). Recent studies using Arabidopsis mutants with
240
inactivated protein phosphatase 2C (PP2C)-type PBCP revealed that dephosphorylation of PSII
241
subunits is crucial for efficient degradation of D1 (Puthiyaveetil et al., 2014). Additionally,
242
PBCP has been found to regulate thylakoid stacking (Bonardi et al., 2005). Although the role of
243
LHCII phosphorylation in PSII repair is still not clear, the phosphorylation of CP29, a minor
244
subunit of LHCII, appears to be essential for the disassembly of the LHCII-PSII supercomplex
245
(Fristedt and Vener, 2011).
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Reaction-center D1 protein is a key player in the PSII repair cycle (Nath et al., 2013a; Nishiyama and Murata, 2014; Rochaix, 2014; Tikkanen and Aro, 2014). The proteolysis and de
248
novo synthesis of D1 protein during the PSII repair cycle are facilitated by chloroplastic
249
proteases in the lumen, stroma and the thylakoid envelope (Che et al., 2013; Kapri-Pardes et al.,
250
2007; Kato et al., 2009; Pribil et al., 2014; Schuhmann and Adamska, 2012; Sun et al., 2007).
251
Serine-, metallo- and putative cysteine- and aspartic acid-proteases, have been identified, some
252
of which require ATP (Pribil et al., 2014; Sakamoto, 2006; van der Hoorn, 2008). Presumably,
253
many other proteases remain to be discovered. Known protease functions include chloroplastic
254
biogenesis, degradation of signaling components, maintenance of chloroplastic homeostasis, and
255
degradation of damaged proteins (Che et al., 2013; Sun et al., 2010a; Sun et al., 2010b; Yin et al.,
256
2008). The current understanding of chloroplastic proteases that play pivotal roles in D1 protein
257
processing and degradation are summarized in the next section and in Supplementary Table 1.
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4.1. Degradation (Deg) proteases
260
Chloroplastic Deg proteases have received significant attention primarily due to their role in the
262
degradation of photodamaged PSII proteins. The function of many of these proteases, however,
263
remains to be determined. In plants, periplasmic degradation (Deg) proteases are ATP-
264
independent serine endopeptidases which are involved in the degradation of photodamaged
265
proteins (Haussuhl et al., 2001; Sakamoto, 2006; Schuhmann and Adamska, 2012; Sun et al.,
266
2010a; van der Hoorn, 2008) (Figure 2). Although these proteases were first discovered in
267
Escherichia coli, they are present in most organisms (Schuhmann and Adamska, 2012).
268
Arabidopsis contains 16 Deg proteases (Deg1-16) that, with the exception of Deg5, possess a C-
269
terminal protease domain and an N-terminal PDZ domain (Haussuhl et al., 2001). Deg proteases
270
are present in chloroplasts, mitochondria, peroxisomes and nuclei (Schuhmann and Adamska,
271
2012). Of the five known chloroplastic Deg proteases, Deg1, Deg5 and Deg8 are attached to the
272
luminal side of thylakoid membranes, and Deg2 and Deg7 are in the stroma (Chi et al., 2012).
273
Arabidopsis mutants with reduced levels of Deg1 exhibit enhanced sensitivity to photoinhibition
274
and an increased accumulation of D1 protein; indicating that Deg1 plays a role in the degradation
275
of D1 protein (Kapri-Pardes et al., 2007). In addition, recent studies in Arabidopsis have
276
indicated the involvement of Deg1in the degradation of CP29 and CP26 proteins under
277
photoinhibition (Zienkiewicz et al., 2012), and of Deg2 in degradation of CP24 under various
278
abiotic stress conditions (Lucinski et al., 2011). The Deg2 protease has been associated with
279
abiotic stress responses in plants. Arabidopsis deg2 mutants showed impaired activity to degrade
280
CP24 in response to various abiotic stresses, such as high salinity, HL and wounding, indicating
281
that Deg2 protease is required for plant growth and development under optimal as well as
282
stressed conditions (Lucinski et al., 2011). Interestingly, the effect of different abiotic stresses on
283
the accumulation of proteases is distinctive. For instance, 2- to 4-fold increase in the amount of
284
Deg2 was observed in Arabidopsis leaves treated with high salinity, desiccation or high
285
irradiance for 2 h, while heat-treated leaves exhibited only trace amounts of Deg2 in the
286
thylakoid membranes (Haussuhl et al., 2001).
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4.2. Filamentation temperature-sensitive H (FtsH) proteases
289
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FtsH proteases are ATP-dependent metalloproteases found in the thylakoids of higher-plant
291
chloroplasts. Twelve genes encoding FtsH proteins have been identified in the Arabidopsis
292
nuclear genome; nine of which (FtsH1, 2, 5-9, 11-12) are found in chloroplasts, three (FtsH3,4
293
and 10) in mitochondria and one (FtsH11) in both chloroplasts and mitochondria (Yoshioka-
294
Nishimura and Yamamoto, 2014). The exact location of the FtsH proteases in the thylakoid
295
membrane still remains to be elucidated. Given their large hexameric form (Kirchhoff et al.,
296
2011), however, it is most likely that they reside in the unstacked region of the thylakoid
297
membrane rather than in the stacked grana. Early studies of Arabidopsis proteases suggested that
298
Deg proteases initiated D1 degradation while further degradation was accomplished by FtsH
299
proteases (Kapri-Pardes et al., 2007; Sun et al., 2010a; Sun et al., 2007). In contrast, recent
300
studies, using Arabidopsis deg and ftsH mutants, have suggested that FtsH proteins act as the
301
initiating proteases and Deg as the assisting proteases in D1 protein degradation (Adam et al.,
302
2011; Kato et al., 2012) (Figure 2). A recent study using transmission electron microscopy and
303
immunogold labeling of FtsH in spinach leaves under HL stress revealed unstacking of
304
thylakoids on the marginal regions of grana stacks, indicating a prominent role of thylakoid for
305
efficient repair of photodamaged D1 proteins (Yoshioka-Nishimura et al., 2014). Interestingly,
306
several reports have corroborated D1 phosphorylation and protease activity with abiotic stress
307
tolerance. It has been proposed that protein phosphorylation of D1 plays an important role in
308
protection of plants against the oxidative damage (Chen et al., 2012). Superoxide anions, H2O2
309
and hydroxyl radical are reportedly involved in the D1degradation under HL as one of the
310
initiating factors (Miyao, 1994; Miyao et al., 1995). Increased levels of H2O2 were found in
311
Arabidopsis mutants with limited FtsH activity. Apparently, the protein instability caused by
312
partial cleavage of D1 proteins led to cytotoxicity that resulted in increased levels of ROS (Kato
313
and Sakamoto, 2014). Earlier, FtsH was reported to be involved in D1 turnover in response to
314
heat stress in spinach (Yoshioka et al., 2006). One of the 12 known FtsHs, FtsH11 was proposed
315
to have a direct role in thermo-tolerance in Arabidopsis plants (Chen et al., 2006) and that
316
FtsH11 protects the photosynthesis apparatus from heat stress at all stages of plant development
317
(Chen et al., 2006).
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4.3. C-terminus-processing (Ctp) proteases
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Further processing of D1 protein by Ctp proteases is essential for the formation of fully
322
functional PSII complexes that are capable of splitting water (Chi et al., 2012; Yin et al., 2008)
323
(Figure 2). Unlike bacteria, in which many types of Ctp proteases exist, in plants, such as
324
Arabidopsis, only CtpA-type proteases have been identified (Che et al., 2013). Three genes
325
encoding CtpA-type proteases have been identified in Arabidopsis (Chi et al., 2012; Yin et al.,
326
2008). Characterization of CtpA1(CtpA/At3g57680) indicated that D1degradation significantly
327
increased in the Arabidopsis AtctpA1loss-of-function mutant. CtpA1 thus appears to be essential
328
for the efficient repair of PSII under HL (Yin et al., 2008). Additionally, functional analysis of
329
another CtpA/At4g17740 in Arabidopsis revealed that the loss of its activity led to a recovery of
330
D1 protein in its precursor form, indicating that CtpA/At4g17740 is essential for D1 C-terminal
331
processing, and thus PSII damage repair (Che et al., 2013). In order to determine the role of
332
cytokinin (CK) in HL-induced stress, expression of several Deg (Deg5 and Deg8) and FtsH
333
(FtsH1, FtsH2, FtsH5 and FtsH8) genes, as well as that of all three identified CtpA genes, were
334
analyzed in CK-deficient and wild-type (WT) Arabidopsis plants (Cortleven et al., 2014). No
335
significant difference in the expression of the examined FtsH and Deg genes were observed
336
between the WT and CK-deficient plants exposed to HL. While differences in the level of
337
expression of CtpA/At4g17740 and CtpA/At5g46390 in response to HL were non-significant in
338
the WT and CK-deficient plants, expression of AtCtpA1 was more strongly up-regulated by HL
339
in WT than in CK-deficient plants. These data suggest that HL-responsive expression of AtCtpA1
340
is CK-dependent. Additionally, AtCtpA1 mutants exhibited a WT-like response to HL (Cortleven
341
et al., 2014), indicating that AtCtpA1might act in concert with other proteins to regulate plant
342
response to HL.
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5. ASSESSMENT OF PHOTOSYSTEM II EFFICIENCY: MEASUREMENT OF
345
CHLOROPHYLL A FLUORESCENCE
346 347
The chlorophyll a fluorescence induction reflects the variations in chlorophyll a fluorescence
348
intensity, which occur when a photosynthetic specimen is moved from darkness to light
349
(Papageorgiou et al., 2007). The fluorescence induction is divided into two phases: (i) the fast
350
induction phase or the OJIP phase, in which O is origin, P is peak and J-I are the intermediate
351
phases, and (ii) the slow induction phase or PSMT phase in which P is peak, S is steady, M is 12
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maximum and T is the terminal state (Figure 3). The fast induction kinetics expresses the
353
primary photochemistry of PSII, while the slow kinetics is a complex phase primarily related to
354
the interactions between processes in the thylakoids and in the reductive carbon cycle of the
355
stroma (Krause and Weis 1984). In other words, slow induction phase is the light that is emitted
356
from photosynthetic specimen in the red-infra-red region of the spectrum for a short time after
357
the fast fluorescence has decayed. The fast phase of the transient provides relevant information
358
of the events that take place during the reduction of electron acceptors during ETC. On the other
359
hand, the slow transient phase is very difficult to be interpreted, primarily because several
360
different processes like non-photochemical quenching, ATP synthesis and Calvin–Benson cycle
361
begin to be involved during this phase (Stirbet and Govindjee, 2011). Nevertheless, the slow
362
fluorescence emission of PSII is considered as a useful approach to quantitatively study the light-
363
induced electron transfer and related events, such as proton movement, which are not detectable
364
by conventional spectroscopic methods (Goltsev et al., 2009). Over the years, researchers have
365
analyzed the slow fluorescence method to assess the plant’s performance under low temperature
366
(Itoh, 1980), high salinity (Zhang and Xing 2008), heavy metal stress (Plekhanov and Chemeris
367
2003), heat stress (Goltsev et al., 1987; Bilger and Schreiber 1990), drought (Mladenova et al.
368
1998), light stress (Valikhanov et al., 2002) and UV irradiation (Zhang et al., 2007a). Zhang et
369
al. (2007b) described a technique for detecting plant senescence based on quantitative
370
measurements of slow fluorescence and proposed that the changes in slow fluorescence intensity
371
reflect the changes in photosynthetic capacity and chlorophyll content during age-dependent and
372
hormone-modulated senescence (Zhang et al., 2007b). PSII efficiency under normal and stress
373
conditions can also be determined by fast chlorophyll a transient kinetics (Baker, 2008; Gururani
374
et al., 2012; Gururani et al., 2013; Gururani et al., 2015) (Figure 4). Analysis of fast chlorophyll
375
a transients has the potential to reveal interesting details pertaining to the alteration and
376
adjustment of the photosynthetic machinery during stress conditions. The reactivity of the
377
photosynthetic apparatus is important to the physiological status and vitality of plants subjected
378
to environmental stress. Measuring alterations of fast chlorophyll a fluorescence transients has
379
become a widely applied technique for assessing reactivity. Fluorescence (F) increases sharply
380
from F0 (minimum) to Fm (maximum) in dark-adapted plants exposed to a strong saturating light
381
pulse [3000-12000 µmol photons m-2 s-1, 200-1000 milliseconds (ms)]. At high temporal
382
resolution (0 to 200 ms), this increase can be seen as a polyphasic OJIP transient in three phases:
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OJ (0-3 ms), JI (3-30 ms) and IP (30-200 ms). Recent findings indicate that the increase from F0
384
to Fm may indicate the reduction of quinone (QA), the primary electron acceptor of PSII
385
(Schansker et al., 2014). The OJIP (or JIP) test elaborated by Strasser et al. (Strasser and Strasser,
386
1995; Strasser et al., 2004) is the main explanatory model used for explaining OJIP transients
387
(Baker, 2008; Baker and Rosenqvist, 2004; Maxwell and Johnson, 2000). The model compares
388
the photosynthetic activities of stressed and control plants and the test is a good, non-invasive
389
tool for analyzing the effects of a variety of stress factors on plants (Goltsev et al., 2012; Ranjan
390
et al., 2014; Toth et al., 2011; Zivcak et al., 2014a; Zivcak et al., 2014b). An analysis of
391
transgenic potato lines with altered photosystem b O (PsbO) production indicated a possible role
392
for this protein in enhanced potato tuberization and abiotic stress tolerance (Gururani et al., 2012;
393
Gururani et al., 2013). The exact mechanism behind the biochemical changes triggered by altered
394
production of PsbO, however, requires further investigation. A hypothetical model is provided
395
for the putative changes in the photosynthetic apparatus based on OJIP analyses (Figure 4).
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Chlorophyll a fluorescence transients provide extremely relevant information about PSII photochemistry and the events in the ETC. OJIP analysis simplifies this information through a
398
series of theoretical assumptions and mathematical calculations using specialized software. The
399
validity of some OJIP parameters has been a subject of debate among biophysicists (Stirbet and
400
Govindjee, 2011), but the acceptance of this analytical assessment of plant photosynthetic
401
efficiency and vitality will likely increase.
403 404
6. ROLE OF EXTRINSIC PROTEINS OF PSII IN D1 TURNOVER
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It is also imperative to recognize the role of extrinsic PSII proteins in D1 turnover in order to
406
fully understand the PSII repair cycle. The extrinsic proteins of PSII in higher plants mainly
407
include Psb subunits, PsbO, PsbP and PsbQ (Bricker et al., 2012). In vitro experiments with
408
spinach indicate that PSII devoid of PsbO becomes more vulnerable to photoinhibition and
409
accumulates significant amounts of D1 and CP43 (Henmi et al., 2004). PsbO may prevent
410
unnecessary interactions between photodamaged D1 and CP43, and the extended structure of
411
PsbO might protect the surface of D1 from reactive oxygen species (Yamamoto et al., 2008).
412
Moreover, PsbO has been proposed to function as GTPase and to regulate the phosphorylation
413
state of the D1 protein; a process that is associated with the efficient turnover of D1 protein
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during PSII repair (Aro et al., 2005; Bricker and Frankel, 2011; Lundin et al., 2007; Lundin et al.,
415
2008). PsbO-deficient potato plants exhibited reduced D1 and CP43 gene expression under a
416
normal light regimen (Gururani et al., 2012; Gururani et al., 2013). Specific roles for various
417
PsbO isoforms in oxygen evolution, PSII stability and plant growth have been identified (Lundin
418
et al., 2008). The precise mechanism of PsbO turnover and its putative role, in addition to the
419
stabilization of the oxygen-evolving complex, remains contentious and yet to be determined
420
(Kangasjarvi et al., 2012). Recent studies showed that removal of two intrinsic PSII proteins, the
421
PsbQ and PsbR, although resulted in only minor changes in terms of oxygen evolution and plant
422
growth, but showed a significant reduction in PSII activity and in PSII–LHCII super-complex
423
accumulation (Allahverdiyeva et al., 2013). Ishihara et al. (2007) demonstrated that a PsbP-like
424
protein 1 (PPL1) is required for the efficient repair of photodamaged PSII although the
425
underlying mechanism is not fully understood. PsbP, PsbQ and PsbR can be phosphorylated in
426
the thylakoid lumen (Ifuku, 2014; Reiland et al., 2009), indicating that their phosphorylation
427
might affect the assembly of PSII. On the other hand, removal of PsbP and PsbQ can induce
428
conformational changes in the arrangement of PSII protein assembly which includes the D1and
429
D2 proteins (Boekema et al., 2000; Bricker et al., 2012; Tomita et al., 2009). The addition or
430
removal of a phosphate group can alter protein conformation. Hence, examining putative
431
conformational changes in these extrinsic proteins during the PSII repair cycle would help
432
determine the state of phosphorylation of these proteins.
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7. INVOLVEMENT OF HORMONAL REGULATORY NETWORKS IN THE
435
RESPONSE OF PHOTOSYNTHETIC MACHINERY TO ABIOTIC STRESS
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Increasing evidence suggests that the interaction between phytohormones and cellular redox is an
438
essential aspect of the response of the photosynthetic structures to various abiotic stresses (Kim
439
et al., 2012; Krumova et al., 2013; Mayzlish-Gati et al., 2010). Recent studies using Arabidopsis
440
mutants with impaired photosynthetic light-harvesting indicated a strong interaction between the
441
control of excitation energy transfer and hormonal regulation (Tikkanen et al., 2014a). The
442
regulation of hormone metabolism by ROS generation and the intricacies of the crosstalk among
443
various hormones in response to various abiotic stresses have been extensively studied (Figure
444
5; Supplementary Table 2). In addition, a number of TFs have been shown to regulate 15
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photosynthesis through major hormonal pathways (Figure 5). For instance, TFs such as BZR1
446
and AtWRKY, were found to influence cell-wall and photosynthesis/chloroplast-related genes,
447
while a few TFs, for example GhDREB and CRF6 were shown to regulate PSII efficiency and
448
chlorophyll accumulation (Nguyen et al., 2014; Toledo-Ortiz et al., 2014; Waters et al., 2009;
449
Zhang et al., 2008). Supplementary Table 3 summarizes information on the recently identified
450
TFs that were found to be associated with the regulation of photosynthetic machinery under
451
normal and abiotic stress conditions.
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Brassinosteroids (BRs) play important roles in plant growth, defense, abiotic stress
tolerance, and the maintenance of high PSII efficiency and photosynthetic carbon fixation in
454
higher plants (Choudhary et al., 2012; Hu et al., 2013; Krumova et al., 2013; Oh et al., 2010).
455
Studies of BR-treated plants and BR-deficient mutants indicate a connection between BRs and
456
genes involved in photosynthesis (Bai et al., 2012; Oh et al., 2011). An Arabidopsis
457
brassinosteroid-insensitive 1(bri1) mutant exhibited a down-regulation of genes associated with
458
the regulation of photosynthesis and was characterized by stunted growth, reduced
459
photosynthetic activity, and a disrupted PSII assembly (Kim et al., 2012). Extensive microscopic,
460
fluorescence spectroscopic, and polarographic analyses of Arabidopsis mutants with altered BR
461
responses revealed enlarged thylakoids, smaller PSII complexes, inhibited oxygen evolution, and
462
reduced PSII quantum yields (Krumova et al., 2013). Komatsu et al. (2010) demonstrated that
463
BR deficiency led to an increased accumulation of chlorophyll and photosynthetic proteins that
464
changed the leaf color from green to dark-green. A brassinazole-insensitive pale green2-1
465
(BPG2) gene was proposed to mediate light-regulated chloroplast protein translation under BR-
466
deficient conditions. Exogenous application of BRs in pepper (Capsicum annuum) plants appear
467
to mitigate the deleterious effects of drought on photosynthesis by maintaining or increasing the
468
efficient use of light and NPQ in PSII antennae (Hu et al., 2013). Several other studies have
469
demonstrated BR-induced changes in thylakoid structure and the regulation of PSII and ETC in
470
photosynthesis (Dobrikova et al., 2014; Rothova et al., 2014). Therefore, the role of BRs in PSII
471
damage repair and in modification of thylakoid structural dynamics deserves further
472
investigation.
473
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Strigolactones (SLs), another group of phytohormones, may play an important role in
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plants in the positive regulation of genes associated with harvesting light (Mashiguchi et al.,
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2009). Several genes encoding light-harvesting chlorophyll a/b binding (LHCB) precursors, 16
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RuBisCO, and components of PSI and PSII are induced by GR24, a synthetic SL compound
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(Mayzlish-Gati et al., 2010). In the Arabidopsis SL-signaling max2 mutant, the expression of
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many genes involved in photosynthesis that are repressed by drought, were up-regulated,
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especially in response to dehydration, in comparison to WT plants. These data indicate a
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correlation between the mis-regulation of these genes and the reduced drought tolerance
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observed in the max2 plants (Ha et al., 2014). Max2 plants may be more sensitive to the high
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energy demands of photosynthesis, and thus require more resources even when the supply of the
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resource is inadequate.
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Gibberellins (GAs) have been shown to regulate photosynthesis in addition to their
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promotion of cell division and seed germination (Huerta et al., 2008; Zhou et al., 2011). In
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addition, GA and kinetin (a type of CK) were reported to promote PSI and PSII activities by
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influencing development of the photosynthetic electron transport system in greening cucumber
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cotyledons (Pedhadiya et al., 1987). Short-term application of GA3 has been found to enhance
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the net photosynthetic rate as well as the photosynthetic oxygen evolution in isolated broad bean
490
protoplasts (Yuan and Xu, 2001). Transgenic Brassica napus plants with decreased GA
491
bioactivity exhibited a significant increase in photosynthetic capacity (Zhou et al., 2011). In
492
contrast, transgenic citrange (Citrus sinensis x Poncirus trifoliata) plants with higher levels of
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endogenous GA exhibited significant up-regulation of many genes involved in photosynthesis
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and water stress alleviation (Huerta et al., 2008). A study in Arabidopsis reported that GA3-
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treated WT plants or transgenic plants overexpressing a GA-responsive gene showed improved
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tolerance to salt, oxidative and heat stress (Alonso-Ramirez et al., 2009). The increase in stress
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tolerance was associated with higher levels of salicylic acid (SA), however, it was unclear if
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photosynthesis was altered by the GA3 treatment or the increased endogenous level of GA level,
499
which might contribute to the improvement in stress tolerance. Further studies are required to
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understand the effect of GAs on the relationship of photosynthesis to abiotic stress responses.
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Abscisic acid (ABA) is the hormone most extensively studied in relation to plant
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response to abiotic stress. ABA has been reported to directly influence the photosynthetic oxygen
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evolution connected with the functioning of PS II centers by disrupting the granal chloroplast
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structure in barley (Maslenkova et al., 1989). Thermostability of photosynthetic apparatus was
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significantly increased in ABA-treated barley seedlings under heat stress. Light scattering and
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fluorescence analyses showed a reduced heat damage of the chloroplast ultrastructure and a 17
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marked decline in heat-induced increase in initial fluorescence (Fo) (Ivanov et al., 1992).
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Exogenous application of ABA increases the content of total carotenoids, xanthophylls, and
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chlorophyll in leaves (Barickman et al., 2014), thereby ameliorating the impact of excessive
510
excitation energy on PSII. Application of ABA also protects PSII by inducing an increase in
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NPQ through the enhancement of xanthophyll-cycle pools and the de-epoxidation of
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xanthophyll-cycle components (Zhu et al., 2011). The LHCB protein family plays an important
513
role in adaptation to environmental stress (Liu et al., 2013; Voigt et al., 2010). Contrary to the
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initial belief that ABA was a negative regulator of the expression of LHCB genes (Staneloni et
515
al., 2008), ABA is believed to be required for the full expression of various LHCB genes (Xu et
516
al., 2012). Down-regulation of LHCB genes decreases ABA signaling and response to drought,
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perhaps partly by modulating ROS homeostasis (Xu et al., 2012). The discrepancy regarding the
518
role of ABA in the regulation of photosynthesis may be attributed to the different experimental
519
systems and methods used to determine photosynthetic output.
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SA is a common phenolic compound well studied for its biochemical, physiological and plant growth regulation activities (El-Tayeb, 2005; Arfan et al., 2007). However, very little is
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known about the SA-related mechanisms that control the maintenance of photosynthesis under
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abiotic stress. Increased accumulation of endogenous SA levels was associated with a sharp
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decrease in maximum PSII quantum yield (Fv/Fm) in leaves of Phillyrea angustifolia plants
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exposed to drought (Munné-Bosch and Peñuelas, 2003). Improved photosynthetic capacity was
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observed in SA-treated wheat plants under high salinity stress (Arfan et al., 2007). Similarly,
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exogenous application of SA was reported to induce pre-adaptive responses to salt stress,
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consequently improving and retaining the integrity of cell membranes in barley plants (El-Tayeb,
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2005). SA-treated grapevine leaves showed accelerated recovery of net photosynthetic rate and
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donor and acceptor parameters of PSII under heat stress. The authors concluded that the effects
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of SA pre-treatment might be related to the enhanced levels of chloroplastic heat shock proteins,
532
resulting in improved net photosynetic rate (Wang et al., 2010). In a similar study, SA treatment
533
of wheat leaves enhanced Fv/Fm, actual photochemical efficiency of PSII and photosynthetic
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electron transport rate, as well as improved net photosynthetic rate and reduced damages of heat
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and high light stresses on D1 protein and PSII (Zhao et al., 2011).
536 537
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A small number of studies have also indicated that auxin, CK, jasmonic acid (JA) and ethylene may also play important roles in the stability of PSI and PSII, and thus in improvement 18
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of photosynthesis in plants exposed to abiotic stress (Supplementary Table 2). Transgenic
539
tobacco plants with enhanced endogenous CK level were reported to have increased transcript
540
abundance of genes associated with PSI, PSII and Cytb6f complex under drought stress.
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Enhanced endogenous level of CK in transgenic plants appeared to promote the protection of
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photosynthetic apparatus under prolonged drought conditions (Rivero et al., 2007, 2010).
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Exogenous application of indole acetic acid, a plant hormone of auxin class and GA3 was
544
reported to reduce the effects of excessive copper mainly by maintaining the Fv/Fm and net
545
photosynthetic rate in sunflower plants (Ouzounidou and Ilias, 2005). Similarly, exogenous
546
application of ethylene was reported to regulate the protection of photosynthesis against Ni- and
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Zn-induced heavy metal stress in Brassica juncea plants (Khan and Khan, 2014). Monitoring the
548
effects of exogenously applied hormones on photosynthesis is a valuable strategy but the
549
transcriptomic analysis of plant response to hormones in photosynthetic mutants would provide a
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more detailed and comprehensive picture of the role of hormones in photosynthesis under normal
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and abiotic stress conditions.
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As described earlier, apart from inducing LHCB genes (Liu et al., 2013; Voigt et al., 2010), ABA has been reported to regulate carotenoid biosynthesis (Barickman et al., 2014), an
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important LHC pigment. Since both ABA and SLs are carotenoid-derived hormones, potential
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crosstalk may exist between SLs, ABA, and light harvesting pathways. A BR-dependent, GA-
556
regulated transcriptome was recently found to be enriched with light-regulated genes and genes
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involved in cell-wall synthesis and photosynthesis. Similar lines of evidence indicate a strong
558
association between various hormones and light-harvesting pathways (Attaran et al., 2014;
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Cortleven et al., 2014; Staneloni et al., 2008). While BRs have been reported to modulate PSII
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efficiency and thylakoid architecture (Dobrikova et al., 2014; Krumova et al., 2013; Oh et al.,
561
2011), SLs were demonstrated to act as positive regulators of light harvesting (Mayzlish-Gati et
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al., 2010). Coordinated crosstalk among SL-, ABA-, and CK-signaling networks regulates the
563
adaptive response of plants to adverse environmental conditions (Ha et al., 2014; Nishiyama et
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al., 2011a). For instance, increased accumulation of ethylene in drought-treated plants not only
565
enhances senescence but also disrupts ABA-mediated regulation of photosynthesis and leaf
566
growth (Bartoli et al., 2013). Therefore, the ratio of ethylene and ABA determines the plant
567
responses to drought, which further warrants a better understanding of crosstalk between these
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hormones. Future efforts to determine the points of intersection that are involved in the co-
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regulation of hormones and light on photosynthetic components would help to enable the
570
identification of candidate genes that could be utilized to limit the level of photoinhibition in
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chloroplasts when plants are subjected to abiotic stress.
572
8. FUTURE PERSPECTIVES
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Designing plants with increased levels of abiotic stress tolerance has been a major challenge for
576
researchers. This is partly due to a substantial lack of information on the intricacies of ROS
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signaling, which limits the ability to determine its regulatory role in abiotic stress response.
578
Previous efforts have largely focused on gene expression studies, but RNA data alone is
579
insufficient. Transcriptomic, proteomic, and metabolomic analyses, novel cellular-imaging
580
techniques, and real-time detection tools would substantially enhance our understanding of ROS
581
signaling.
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Increasing the level of chloroplastic antioxidants or the activity of ROS-scavenging enzymes is clearly not a productive approach to improve crops. Alternative approaches, such as
584
modifying LHC and PSII components, have also been suggested as an alternative approach
585
(Horton, 2012; Tikkanen and Aro, 2014). The complex events associated with phosphorylation,
586
dephosphorylation, and the migration of thylakoid membrane proteins and reaction centers,
587
however, remain largely speculative. For example, the roles of STN7 and STN8 are known, but
588
it remains unclear if crosstalk exists in the regulation of these proteins. Moreover, recent findings
589
have suggested that the interaction between STN7 and STN8 is different in monocots and dicots
590
(Nath et al., 2013b). These observations also hold true for the role of minor LHCII antennal
591
proteins, because the phosphorylation of CP29 was reported to be species-specific (Chen et al.,
592
2009). Currently, little information is available on the phosphorylation of other minor antennal
593
proteins of LHCII. Similar ambiguities exist for the proteolytic mechanism and involvement of
594
ATP-dependent proteases in the PSII repair cycle. Contrasting reports and insufficient
595
knowledge on various proteases and intrinsic PSII proteins raises many questions, which only
596
further studies can answer. A major challenge will be to elucidate the linkage between the
597
identified kinases and phosphatases and their influence on the redox state of the photosynthetic
598
ETC. Identification of the substrates of proteases and determining their specificity would help to
599
understand their mode of action. In order to assess damage to photosynthetic machinery at a
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bioenergetic level, techniques such as chlorophyll a transient kinetics analysis are expected to
601
significantly contribute to our knowledge (Figure 4). The redox state of the photosynthetic ETC regulates the complex events during PSII
603
repair cycle as well as several other responses that involve the chloroplast and nuclear gene
604
expression. While the redox state of ETC is regulated by various environmental factors, the
605
chloroplast and nuclear gene expression can be transduced by changes in hormonal signaling
606
pathways. Therefore, changes in photosynthesis and levels of hormones in plants subjected to
607
environmental stresses should not be seen as isolated events, particularly given the emerging
608
evidence that indicates the involvement of phytohormones in PSII damage repair (Cortleven et
609
al., 2014). However, the extensive molecular connections among the signaling networks of
610
various hormones make it a daunting task to unravel the central roles of individual hormones in
611
coordinating the expression of photosynthetic genes and regulation of PSII damage repair.
612
Moreover, the physiological significance of changes in expression recorded in many abiotic
613
stress-responsive genes, particularly in those encoding photosynthetic proteins, is yet to be
614
understood. Genome-wide transcriptomic analyses of integrated hormonal regulatory networks
615
could provide a global view of their functions and molecular links with putative functions in the
616
regulation of photosynthesis. Additionally, it is important to use metabolomic and proteomic
617
approaches for understanding the metabolic responses of plants for photosynthetic acclimation to
618
various abiotic stresses. Such integration of different datasets would improve our understanding
619
of the physiological significance of hormones in regulation of photosynthesis performance under
620
abiotic stresses. Cellular responses to abiotic stresses also involve the transcriptional regulation
621
of photosynthetic metabolism. Several reports suggest that improved abiotic stress tolerance can
622
be achieved by engineering the expression of TFs (Puranik et al., 2012; Zhang et al., 2008)
623
(Supplementary Table 3). The involvement of these TFs in the regulation of genes associated
624
with photosynthesis, however, is still not clear. Taken together, designing plants with improved
625
abiotic stress tolerance and enhanced photosynthetic production will require a more
626
comprehensive understanding of the way photosynthetic machinery mediates the environmental
627
cues and the inherent metabolic signaling. Hence, it is crucial to focus on combining
628
interdisciplinary strategies from different research areas of plant sciences which could facilitate
629
the engineering of plant architecture in a sustainable way.
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ACKNOWLEDGEMENTS
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This work was supported by the Scientific Research C Grant (no. 25440149) from Japan Society
633
for the Promotion of Science to L.-S. P. Tran.
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FIGURE LEGENDS
1242
Figure 1. Schematic Representation of Photosynthetic Redox Signals and the Detoxification
1244
of Reactive Oxygen Species (ROS). ROS, such as hydrogen peroxide (H2O2), generated in
1245
response to various stress factors, such as high irradiance (indicated by the red lightning bolt),
1246
and redox signals from the electron transport chain (ETC), initiate signaling cascades that
1247
eventually lead to nuclear-gene expression. In photosystem II (PSII), the splitting of water (H2O)
1248
at oxygen-evolving complex (OEC) produces H+ ions that are transferred across the membrane
1249
to ATP synthase (ATP syn), while electrons (e-) are transferred to PSI via the cytochrome b6f
1250
(Cytb6f) protein complex. Plastoquinone (Pq) accepts two protons (H+) from the stromal side
1251
along with two electrons (e-) from PSII and transfers the protons to the luminal side, while
1252
electrons are transferred to PSI via Cytb6f complex and plastocyanin (PC) pool. Electrons
1253
removed from water are transferred to the single-electron carrier ferredoxin (Fd). Ferredoxin
1254
NADP+ reductase (FNR) then transfers an electron from each of the two Fd molecules to a single
1255
molecule of the two-electron carrier nicotineamide adenine dinucleotide phosphate H (NADPH).
1256
Similarly, H+ ions from PSI are transferred to ATP synthase where proton gradients are used for
1257
producing ATP molecules from ADP. Electrons transferred from PSI via Fd are also converted
1258
into superoxide (O2-) in the Mehler peroxidase reaction (MP reaction). The O2- is detoxified by
1259
superoxide dismutase (SOD), a ROS-scavenging enzyme. Another ROS-scavenging enzyme,
1260
ascorbate peroxidase (APX), uses ascorbate (Asc) to reduce H2O2 to H2O. The scavenging of
1261
free radicals by APX increases the levels of monodehydroascorbate (MDA) and
1262
dehydroascorbate (DHA). High levels of MDA and DHA are reduced by MDA reductase
1263
(MDAR), DHA reductase (DHAR) and glutathione reductase (GR). During ascorbate-
1264
glutathione recycling, GR catalyzes the reduction of oxidized glutathione (GSSG) to GSH in
1265
order to maintain a higher ratio of GSH:GSSG in the cytosol. Initial reports indicated that
1266
residual H2O2 from incomplete detoxification can initiate mitogen-activated protein (MAP)
1267
kinases that in turn direct cellular responses such as nuclear-gene expression. Thioredoxins
1268
(TRXs) accept electrons from PSI and utilize them to phosphorylate the light-harvesting complex
1269
and possibly to induce nuclear-gene expression. Similarly, the plastoquinone (Pq) pool induces
1270
the expression of certain protein kinases and transcription factors (TFs) which can, in turn,
1271
trigger transcriptional-signal transduction in the nucleus.
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Figure 2. Schematic Illustrating the Successive Steps of the Photosystem II (PSII) Repair
1274
Cycle after High Light Stress-Induced Photodamage. The photosystem II-light harvesting
1275
supercomplex (PSII-LHCII) has two components: (i) LHCII consists of a protein trimer (denoted
1276
as II) and three less abundant minor antennal chloroplast proteins (CPs), CP24, CP26 and CP29
1277
(denoted as 24, 26 and 29), and (ii) PSII which mainly consists of a D1-D2 (or PsbA-PsbD
1278
where Psb is photosystem b) heterodimer coupled with chlorophyll a containing CP43, CP47,
1279
PsbP (P), PsbQ (Q) and PsbO (O). (A) Photodamage is caused when light-absorbing antennae
1280
receive high-intensity light that damages D1 (denoted by cross-hatching). (B) To counter this
1281
damage, LHC dissipates the excess excitation energy in the form of heat via non-photochemical
1282
quenching. (C) After photodamage has occurred, the protein trimer of LHCII is phosphorylated
1283
by STN7, and the PSII proteins D1, D2 and CP43 are phosphorylated by STN8. Recent studies
1284
indicate, however, that STN7 can also phosphorylate PSII proteins to some extent (Bonardi et al.,
1285
2005; Fristedt et al., 2009; Nath et al., 2013b). The phosphorylation of one of the minor proteins
1286
of LHCII, CP29 (denoted in gray) has been found to be responsible for the disassembly of the
1287
PSII-LHCII supercomplex (Fristedt and Vener, 2011). (D) Phosphorylated proteins of the PSII-
1288
LHCII supercomplex are then dephosphorylated. Thylakoid associated phosphatase 38 (TAP38,
1289
yellow boxes) dephosphorylates LHCII proteins, and Psb core phosphatase (PBCP, brown
1290
polygons) dephosphorylates PSII proteins. (E) Dephosphorylation results in the disassembling of
1291
the PSII-LHCII supercomplex into a PSII repair intermediate and a peripheral antennal complex.
1292
(F) A zinc metalloprotease FtsH then recognizes the N-terminal of the photodamaged D1and
1293
degrades it in a complex processive manner (Adam et al., 2011). (G) ATP-independent Deg5 and
1294
Deg8 endoproteases further assist the processive degradation of photodamaged D1 protein by
1295
FtsH (Kato et al., 2012). (H) The proteolytic degradation of D1 is followed by the synthesis of
1296
nascent copies of D1 protein, facilitated by a plant-specific chloroplastic protease ClpA, which is
1297
involved in processing the C-terminus of D1. Plants possess highly efficient ROS-scavenging
1298
mechanisms, but ROS pose a major obstacle in this step by inhibiting the de novo synthesis of
1299
new D1 proteins. (I) Once nascent copies of D1 protein are synthesized and the co-translational
1300
assembly of D1 is completed, they are inserted into PSII and are post-translationally modified.
1301
Lastly, after the reassembly of its core components, PSII migrates toward the grana in its
1302
functional form.
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Figure 3. A General Representation of Chlorophyll Fluorescence Induction Curve in Plant
1304
Samples. When a dark-adapted plant sample is exposed to light, certain characteristic changes in
1305
chlorophyll fluorescence are observed. These changes are known as fluorescence induction or
1306
fluorescence transient, generally seen as two transient phases that are labeled by using the
1307
observed inflection points: (i) fast chlorophyll fluorescence induction (up to few hundred
1308
milliseconds) or the so-called OJIP phase where, O (origin) is the first measured minimum
1309
fluorescence level, P is the peak and J and I are intermediate inflections (ii) slow chlorophyll
1310
fluorescence induction or the PSMT phase where S stands for steady state, M for a maximum,
1311
and T for a terminal steady state level.
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1312
Figure 4. Hypothetical Scheme of a Multistep Electron Transport Chain, Based on the
1314
Emission Kinetics of Chlorophyll a. According to this scheme, the conversion of light energy
1315
to chemical energy begins with three consecutive basic steps, (i) ABS, absorption of light energy
1316
(photons) by chlorophyll molecules in the light-harvesting complex of photosystem II (PSII)
1317
(LHCII), (ii) TR, trapping of the excitation energy by the reaction center (RC) and (iii) ET,
1318
electron transport via PSII RCs (PSII-RC). When plant tissues are exposed to a short pulse of
1319
strong light, chlorophyll a (Chl a) absorbs the light energy and uses it in photosynthesis (Chl a*
1320
excited). At the same time, some light is emitted at a lower energy level as a function of time (Ft),
1321
a phenomenon called fluorescence emission. The fluorescence kinetics data is analyzed, and
1322
changes in the photosynthetic apparatus, such as the primary reaction of photochemistry, are
1323
derived through a series of equations, commonly known as the OJIP test (Strasser and Strasser,
1324
1995). Potato plants with altered expression of a PSII-related gene encoding the manganese
1325
stabilizing protein were analyzed with the OJIP test and a hypothesis for the putative changes in
1326
PSII was provided (Gururani et al., 2012; Gururani et al., 2013). The integrity of PSII after the
1327
primary reactions of photochemistry creates a primary redox (Red, reduction; Ox, oxidation)
1328
potential within and around PSII between a primary electron donor pigment P680+ and an electron
1329
acceptor, Quinone (Qa). Re-reduction of the primary electron donor pigment P680+ by internal
1330
electron donors occurs in in vitro systems using Hill reaction agents such as hydroxylamine (HA),
1331
Mn2+ and diphenylcarbazone (DPC). Re-reduction of the primary electron donor pigment (P680+)
1332
by internal electron donors also occurs in vivo. For example, tyrosine, ascorbate (Asc) and
1333
proline (Pro) are generally available as internal electron donors. The first chemical step occurs
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when an excited donor pigment molecule with a light absorption peak of 680 nm (P680) donates
1335
an electron to pheophytin (Ph), producing oxidized P680 (P680+) and reduced Ph (Ph-) in PSII. The
1336
oxygen-evolving complex (OEC) competes with the internal electron donation, where the
1337
reaction constant for splitting water, kW, is much lower than that of non-water electron donors
1338
(kD>>kW). Under various abiotic stress conditions, PSII is damaged, and the OEC then
1339
presumably favors electron donation by non-water electron donors with a high rate constant, kD.
1340
The total electron transport then increases as OEC activity decreases, due to the easy
1341
accessibility of non-water electrons from molecules such as Asc and Pro. The fraction of
1342
electrons donated by water is lower in stressed samples. Under normal conditions, an intact
1343
manganese cluster (Mn4CaO5) at the OEC thus promotes electron donation from water to PSII-
1344
RC with a low kW and reduces the accessibility of non-water electron donation to the RC of PSII.
M AN U
SC
RI PT
1334
1345
Figure 5. Putative Involvement of Phytohormones and Representative Transcription
1347
Factors (TFs) in the Regulation of the Photosynthetic Machinery in Plants Under Abiotic
1348
Stress Conditions. Red dotted lines indicate crosstalk between two hormones that are inhibitory
1349
to each other. Green dotted lines indicate crosstalk between two hormones that up-regulate each
1350
other. ABA, abscisic acid; ARF2, auxin response factor 2 (Lim et al., 2010); AtNAC2,
1351
Arabidopsis thaliana NAC [NAM (no apical meristem), ATAF (Arabidopsis transcription
1352
activation factor) and CUC (cup-shaped cotyledon)] 2 TF (Ha et al., 2014); BR, brassinosteroid;
1353
BZR1, brassinazole resistant 1 TF (Bai et al., 2012); CRF6, cytokinin response factor 6 (Zwack
1354
et al., 2013); CK, cytokinin; Cytb6f, cytochrome b6f complex; ERF6, ethylene response factor 6
1355
(Dubois et al., 2013); GA, gibberellic acid; GhDREB1, Gossypium hirusitum dehydration-
1356
responsive element binding protein 1 (Shan et al., 2007); JA, jasmonic acid; MYC 2,
1357
myelocytomatosis 2 TF (Dombrecht et al., 2007); PSI, photosystem I; PSII, photosystem II; ROS,
1358
reactive oxygen species; SA, salicylic acid; SL, strigolactone; SlZF2, Solanum lycopersicum
1359
Zinc Finger2 TF (Hichri et al., 2014); OsWRKY45 (Chao et al., 2010), Oryza sativa WRKY45,
1360
a TF belonging to the WRKY TF family that derives its name from the protein sequence motif
1361
WRKYGQK.
AC C
EP
TE D
1346
1362 1363 1364 39
ACCEPTED MANUSCRIPT
RI PT
Chloroplast
ATP ADP
Fd
SOD
MDAR
PS I NADP+
APx
MDA
DHA PC
DHAR
e-
TRs
PS II
2H2O lumen
stroma
Thylakoid
H2O
MDA
DHA
GSSG
GR
GSH
Asc-glutathione recycling
MAP Kinase
EP
OEC
H2O
MDAR
TFs, Kinases H+
AC C
O2 + 4H+
Pq e-
Asc
TE D
Cytb6f
APx
Asc
Asc
NADPH
e-
H2O2
SC
FNR
MP O2reaction
M AN U
O2
Nuclear gene expression
DHAR
ACCEPTED MANUSCRIPT
A
B
II
II
II
24 26 29
P
II
24 26 29
SC
D1 D2 47 43 damaged D1 Q P O
M AN U
Reconstitution of PSII components
I
C-terminal processing
H
D1 processing
D1 43
AC C
D2 47
Co-translational assembly CtpA
24 26 29
G
D2 47 P Q P O
P D1
43
P
STN8 Dephosphorylation TAP38 II
II
D
24 26 29
D1 43
D2 47
PBCP FtsH
EP
Post-translational assembly of PSII proteins ROS
D1 43
TE D
D1 D2 47 43 P Q O
Membrane insertion
II
Phosphorylation
D1 D2 47 43 Q P O
Protein trafficking
P
II
Photodamage
lumen
C
STN7
Heat
RI PT
stroma
D2 47
D1 43
Disassembly
D2 47
Proteolysis
PSII repair intermediate
Deg D1 degradtion
F
Peripheral antenna
E
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
Chl a*
SC
Chl a
RI PT
ABS
*
Mn4CaO5
Ox O2 + H+ OEC
-
-
-
kD
Tyrosine
Asc
-
HA
QA -
ET
QA
P680Ph
-
kD DPC Pro Non-water electron donors
Mn2+
Ph-
P680+
EP
Red kW
AC C
H2O
TE D
Ft
M AN U
TR
LHCII
PSII-RC
ACCEPTED MANUSCRIPT
PS II
RI PT
Stress PS I
Cytb6f
SC
Stress signal perception
GA
JA
SA
ABA
TE D
Hormonal regulation
M AN U
ROS
AC C
Structural and functional adaptations
ARF2
BR
SL
BZR1
AtNAC2
CK
CRF6
EP
Transcriptional GhDREB1 OsWRKY45 MYC2 SlZF2 control
Auxin
Regulation of photosynthetic machinery
Ethylene
ERF6
