Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions.

Photosynth Res DOI 10.1007/s11120-015-0125-x

REVIEW

Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions Leonid V. Kurepin1,2 • Alexander G. Ivanov1 • Mohammad Zaman3 • Richard P. Pharis4 • Suleyman I. Allakhverdiev5,6,7 • Vaughan Hurry2 Norman P. A. Hu¨ner1

•

Received: 15 December 2014 / Accepted: 20 March 2015 Ó Springer Science+Business Media Dordrecht 2015

Abstract Plants subjected to abiotic stresses such as extreme high and low temperatures, drought or salinity, often exhibit decreased vegetative growth and reduced reproductive capabilities. This is often associated with decreased photosynthesis via an increase in photoinhibition, and accompanied by rapid changes in endogenous levels of stressrelated hormones such as abscisic acid (ABA), salicylic acid (SA) and ethylene. However, certain plant species and/or genotypes exhibit greater tolerance to abiotic stress because they are capable of accumulating endogenous

& Leonid V. Kurepin [email protected] & Alexander G. Ivanov [email protected] 1

Department of Biology and The Biotron Center for Experimental Climate Change Research, University of Western Ontario (Western University), 1151 Richmond Street N., London, ON N6A 5B7, Canada

2

Department of Plant Physiology, Umea˚ Plant Science Centre, Umea˚ University, Umea˚, Sweden

3

Soil and Water Management and Crop Nutrition Section, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Department of Nuclear Sciences and Applications, International Atomic Energy Agency, Vienna International Centre, PO Box 100, 1400 Vienna, Austria

4

Department of Biological Sciences, University of Calgary, Calgary, AB, Canada

5

Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia

6

Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region 142292, Russia

7

Department of Plant Physiology, Faculty of Biology, M. V. Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow 119991, Russia

levels of the zwitterionic osmolyte—glycinebetaine (GB). The accumulation of GB via natural production, exogenous application or genetic engineering, enhances plant osmoregulation and thus increases abiotic stress tolerance. The final steps of GB biosynthesis occur in chloroplasts where GB has been shown to play a key role in increasing the protection of soluble stromal and lumenal enzymes, lipids and proteins, of the photosynthetic apparatus. In addition, we suggest that the stress-induced GB biosynthesis pathway may well serve as an additional or alternative biochemical sink, one which consumes excess photosynthesis-generated electrons, thus protecting photosynthetic apparatus from overreduction. Glycinebetaine biosynthesis in chloroplasts is up-regulated by increases in endogenous ABA or SA levels. In this review, we propose and discuss a model describing the close interaction and synergistic physiological effects of GB and ABA in the process of cold acclimation of higher plants. Keywords Abscisic acid Cold acclimation Glycinebetaine Environmental stress Photosynthetic apparatus Plant hormones

Introduction To improve plant tolerance to abiotic stresses such as excess light, drought, extreme environmental temperatures or salinity, the osmotic potential of plant cells must increase, usually by increasing the concentration of cell solutes. However, increasing the concentrations of common solutes, such as organic acids, carbohydrates and inorganic ions, can inhibit enzymatic activity. These solutes are therefore usually found within plant cell vacuoles where their increasing concentration does not harm cell metabolism. In contrast to

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common solutes, compatible osmolytes (osmoregulators) are membrane-impermeable solutes which accumulate in the cytoplasm at high concentrations (C C 0.2 M), do not adversely affect functional activities in the cell and as such they are considered to be valuable osmoprotectors (Yancey et al. 1982). The unique properties of glycinebetaine (GB), i.e. antichaotropic function related to its zwitterionic (double ion) nature (Papageorgiou et al. 1985), low molecular weight, high solubility and low viscosity of its solution makes GB one of the most efficient osmoregulator (Yancey et al. 1982; Yancey 2005). In fact, a range of abiotic stresses have been shown to cause an accumulation of GB in plants that have a functional GB biosynthetic pathway (Rhodes and Hanson 1993). Furthermore, the extent of GB accumulation can often be directly correlated with a plant’s tolerance to abiotic stress (Rhodes and Hanson 1993; Sakamoto and Murata 2002; Giri 2011; Chen and Murata 2011). For example, a test of various cotton (Gossypium hirsutum L.) genotypes demonstrated that endogenous GB levels varied greatly between genotypes, as did tolerance to drought stress, and genotypes with increased drought tolerance had higher endogenous GB levels (Sarwas et al. 2006). Supporting this protective role for GB accumulation, overproducing GB in transgenic cotton plants was associated with increased drought stress tolerance, relative to wild-type (WT) plants— a phenomenon that was also accompanied by enhanced seedling growth and increased cotton seed and boll yield (Lv et al. 2007). Thus, there appears to be a direct link between a plant’s GB biosynthesis and its ability to increase tolerance to abiotic stresses. The ability of a plant to increase abiotic stress tolerance can also be dependent on the biosynthesis and action of plant hormones, such as abscisic acid (ABA), ethylene and possibly salicylic acid (SA) (Abeles et al. 1992; Dodd and Davies 2010; Kurepin et al. 2013a). For example, the pathway for the biosynthesis of choline, a biosynthetic precursor of GB in plant tissues, is integrated with the biosynthesis of ethylene (Sahu and Shaw 2009). More importantly, plant hormones are known to regulate the biosynthesis and action of secondary metabolites, which includes osmolytes such as GB. For example, ABA applied to barley (Hordeum vulgare L.) plants increased tolerance of the plant to several abiotic stresses, and this increased tolerance was accompanied by increases in relative expression levels of a key gene in the GB biosynthesis pathway (Ishitani et al. 1995), as well as increases in an accumulation of endogenous GB (Jagendorf and Takabe 2001). Thus, the GB-mediated increase in a plant’s abiotic stress tolerance appears to be regulated by stress-induced ABA. The regulation of GB biosynthesis by ABA during abiotic stress is also important because ABA plays an important role of regulating stomatal closure in response to osmotic stress (Dodd and Davies 2010).

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One important aspect of GB-mediated enhancement of plant tolerance to abiotic stress is the ability of chloroplastproduced GB to protect the photosynthetic apparatus, i.e. protect the enzymes and lipids that are required to maintain the optimal linear electron flow through thylakoid membranes and also maintain the assimilation of CO2 (Sakamoto and Murata 2002; Chen and Murata 2011). In addition, the protective functions of GB in chloroplasts are especially important for the stability of photosystem II (PSII), the most vulnerable component of the photosynthetic apparatus, and one which is believed to play a key role in the photosynthetic response of plants to various abiotic stresses (Baker 1991; Adams et al. 2013). In fact, several studies have indicated the stabilizing and protective role of exogenous GB on stressinduced inactivation of the PSII complex (Murata et al. 1992; Mamedov et al. 1993; Papageorgiou and Murata 1995; Allakhverdiev et al. 1996, 2003, 2007). This review summarizes and evaluates the abiotic stressalleviating effects of GB, especially effects that are likely to occur via its interaction with stress-related plant hormones. It also emphasises the key role of GB in protecting the photosynthetic apparatus from low-temperature-stress effects, as well as, the synergistic effects of ABA and GB in the actual process of cold acclimation by higher plants.

Gycinebetaine: natural abundance, biosynthesis and accumulation in response to abiotic stresses Glycinebetaine (N,N0 ,N00 -trimethylglycine) belongs to a class of small molecules often referred to as ‘‘compatible osmolytes’’, a group that includes several amino acids such as proline, as well as quaternary ammonium compounds, such as prolinebetaine, b-alaninebetaine, choline-o-sulphate and the tertiary sulphonium compound, 3-dimethylsulphoniopropionate (DMSP). Glycinebetaine has been found in many organisms, including bacteria, haemophilic archaebacteria, marine invertebrates, plants and mammals (Rhodes and Hanson 1993; Chen and Murata 2011). In plants, GB is reported to function in the protection of cells against osmotic inactivation, i.e. GB increases water retention by acting as a compatible osmolyte (Liu and Bolen 1995; Sakamoto and Murata 2002; Ashraf and Foolad 2007). The compatible osmolytes are uncharged (or zwitterionic, such as GB) at a neutral pH and are highly soluble in water (Ballantyne and Chamberlin 1994; Yancey et al. 1982; Yancey 2005). They are excluded from the hydration sphere of proteins and can act to stabilize folded protein structures (Low 1985). In addition to its role as an osmoregulator, GB is also an efficient antichaotropic agent, protecting plant membranes and proteins against structural randomization by salts, high temperature, and low temperature (Papageorgiou et al. 1985, 1991; Mamedov et al.

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1991; Murata et al. 1992; Stamatakis and Papageorgiou 1993). Thus, compatible osmolytes increase the tolerance of plants to both biotic and abiotic stress by acting as nontoxic cytoplasmic osmolytes (Jones et al. 1977). In higher plants, GB is synthesized from choline via betaine aldehyde (BA) (Sahu and Shaw 2009). An early precursor of choline, ethanolamine (EA), is converted to monomethyl EA by the addition of a methyl group from S-adenosylmethionine (SAM). The monomethyl EA conversion to choline occurs in the cytosol. Choline is then transported to the chloroplast via a choline-transporter, where the final biosynthesis site of GB is thought to occur in a two-step synthesis (Fig. 1). The first step yields BA in a reaction catalysed by a choline monooxygenase (CMO). The second step converts BA to GB in a reaction catalysed by a BA dehydrogenase (BADH) (Weretilnyk et al. 1989; Rhodes and Hanson 1993). Once produced, GB can be translocated throughout the plant via the phloem (Makela et al. 1996b; Hattori et al. 2009). The accumulation of endogenous GB in plants, which increases appreciably following osmotic stress events, occurs mainly in younger leaf tissues (Chen and Murata 2011). In barley, stress-induced GB biosynthesis occurs mainly in vascular tissues of leaves and the pericycle of roots, with major accumulations of GB being detected in younger leaves (Hattori et al. 2009). Translocation studies with (14C)-labelled GB in tomato (Solanum lycopersicum L.), pea (Pisum sativum L.), soybean [Glycine max (L.) Merr.] and turnip (Brassica rapa ssp. Oleifera) plants demonstrated that leaf to root translocation via the phloem occurs within 2 h, with labelled GB being found throughout the plant by 24 h (Makela et al. 1996b). While GB biosynthesis occurs in many kingdoms of living organisms, it does not appear to be ubiquitous across plant species, as certain species exhibited undetectable levels of GB following the initiation of abiotic stress. The functional GB biosynthesis pathway, and therefore the presence of endogenous GB, occurs in many higher plant

Fig. 1 A schematic model for the biosynthesis of glycinebetaine. BADH betaine aldehyde dehydrogenase; CMO choline monooxygenase; SAM S-adenosylmethionine

species, such as alfalfa (Medicago sativa L.; Wood et al. 1991), algorrobo (Prosopis alba Griseb.; Meloni et al. 2004), barley (Hordeum vulgare L.; Ladyman et al. 1983; Kishitani et al. 1994; Nomura et al. 1995; Hattori et al. 2009), bean (Phaseolus vulgaris L.; Gadallah 1999), cotton (Desingh and Kanagaraj 2007), corn (Zea mays L.; Quan et al. 2004b; Rhodes et al. 1989), pea (Pisum sativum L.; Takhtajan 1980), sorghum [Sorghum bicolor (L.) Moench; Grote et al. 1994; Mickelbart et al. 2003], spinach (Spinacia oleracea L.; Weigel et al. 1986; McCue and Hanson 1990), strawberry (Fragaria x ananassa Duchesne; Rajashekar et al. 1999), townsend’s cordgrass (Spartina x townsendii H. Groves and J. Groves; Storey et al. 1977) and wheat (Triticum aestivum L.; McDonnell and Jones 1988; Allard et al. 1998; Wang et al. 2010a). However, other plant species, such as Arabidopsis thaliana (Hibino et al. 2002), eggplant (Solanum melongena L.; de Zwart et al. 2003), potato (Solanum tuberosum L.; de Zwart et al. 2003), tobacco (Nicotiana tabacum L.; Nuccio et al. 1998), tomato (Solanum lycopersicum L.; Park et al. 2004) and rice (Oryza sativa L.; Sakamoto and Murata 1998) are reported to have no detectable accumulation of GB in response to abiotic stress. The accumulation of GB can also be cultivar or genotype specific. For example, some genotypes of sorghum and corn accumulate GB, whereas others do not (Grote et al. 1994; Saneoka et al. 1995). The fact that there are genotypic differences in GB accumulation may explain the occurrence of stress-tolerant and stress-susceptible genotypes within individual plant species. For example, pre-soaking sugarcane (Saccharum arundinaceum L.) seeds with GB prior to germination, followed by foliar GB application at the seedling stage, increased the growth of one cultivar, had no effect on another cultivar and inhibited the shoot growth of a third cultivar (Campbell et al. 1999). Interestingly, a study with GB-accumulating and -non-accumulating genotypes of sorghum demonstrated that genetically crossing these two categories of genotypes resulted in progeny which possessed a wide range of levels of GB accumulation (Mickelbart et al. 2003). The use of molecular genetic technology, where plant or bacterial genes involved in GB biosynthesis are introduced into plant genotypes that lack stress-induced GB accumulation, has played a key role in understanding the importance of this unique molecule in the stress-related responses of plants (Chen and Murata 2011). For example, heatstressed transgenic A. thaliana plants which were over expressing the bacterial codA gene, produced seeds that, during germination, yielded 10- to 15-fold higher levels of GB accumulation than heat-stressed wild type (WT) plants (Hayashi et al. 1998). These transgenic seeds also demonstrated an increased heat stress tolerance during germination (Hayashi et al. 1998). While transformation of

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plant genotypes that do not have a functional GB biosynthetic pathway results in increased abiotic stress tolerance, there is some disagreement as to which transgenes are more potent in causing GB accumulation—those of plant origin or those from bacteria. Transgenic plants of A. thaliana, rice and tobacco, all expressing plant choline monooxygenase (CMO), accumulated relatively low levels of GB unless exogenous choline was supplied (Nuccio et al. 1998; McNeil et al. 2001; Hibino et al. 2002; Shirasawa et al. 2006). Yet those same plant species, when genetically engineered to express bacterial choline oxidase (COD), accumulated relatively high amounts of GB, even without administration of exogenous choline (Hayashi et al. 1997; Nuccio et al. 1998; Sakamoto and Murata 1998; Huang et al. 2000; Mohanty et al. 2002; Hibino et al. 2002). More importantly, transformation of A. thaliana, rice and tobacco plants with a bacterial gene encoding the COD enzyme resulted in substantially increased stress tolerance, relative to a comparable transformation with a plant gene encoding the CMO enzyme. In addition to the importance of the origin of the GB transgene in non-GB-accumulating genotypes, another factor—the cellular localization of the transgene product— can determine the extent of GB accumulation. For example, transgenic tomato plants which accumulate codA in the cytosol only, or in both the cytosol and in chloroplasts, exhibited a 5–6 fold higher GB accumulation than transgenic plants that accumulate COD enzyme only in chloroplasts (Park et al. 2007a). However, a cold or salt stress treatment applied to the transgenic tomato lines showed that plants that accumulate COD enzyme only in chloroplasts were just as tolerant to stress as plants that accumulate the COD protein only in the cytosol, or in both the cytosol and chloroplasts (Park et al. 2007a). Thus, while localization of the introduced gene was important for GB accumulation, it did not affect the physiological response to the stress.

Interaction of glycinebetaine with photosynthesis under abiotic stress conditions To improve plant tolerance to the dehydration effects associated with salinity, drought and cold stresses, it would be necessary to modify the osmolarity of plant cells by increasing the concentration of cell solutes. Indeed, exogenous application of GB has been shown to improve plant stress tolerance (Rhodes and Hanson 1993; Hanson et al. 1994; Kishitani et al. 1994; Zaman et al. 2015), i.e. either increase or maintain plant growth rates under various abiotic stresses for numerous species of economic importance (Table 1). In addition, increased GB levels are also associated with an increase in the rate of photosynthesis,

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which is considered to be one of the major mechanisms of attaining relief from abiotic stress. Drought stress Drought-stressed soybean plants have reduced reproductive yield, decreased leaf area growth and reduced biomass accumulation (Muchow et al. 1986; Sinclair et al. 1987), and these effects were associated with a reduction in photosynthesis and N2 fixation (Weisz et al. 1985; Frederick et al. 1989). In contrast, field-grown soybean plants supplemented with a foliar spray of GB showed increased reproductive yield, as well as increased leaf area growth, both effects being accompanied by an increased rate of photosynthesis and enhanced N2 fixation (Agboma et al. 1997a). Foliar pre-treatment of pot-grown, drought-stressed tobacco plants using a spray of GB enhanced their stress tolerance (improved shoot biomass and increased stem height), and these effects were associated with an enhanced photosynthesis, greater stomatal conductance, higher carboxylation efficiency of CO2 assimilation, and an increased efficiency of PSII (Ma et al. 2007). Salt stress Responses to application of GB to bean plants with the objective of alleviating high-salinity stress included increases in stomatal conductance, transpiration and photosynthesis rates, as well as increased leaf relative water content (Lopez et al. 2002). Roots’ pre-treatment of saltstressed rice plants with GB prevented ultrastructural chloroplasts damage, such as swelling of thylakoids, the disintegration of grana stacks and intergranal lamellae, and the destruction of mitochondria (Rahman et al. 2002). In another experiment, pre-treatment of salt-stressed rice plants with GB increased shoot height, and this effect was associated with enhanced CO2 assimilation and better photosynthetic performance (Cha-Um et al. 2007). Tobacco plants transformed with the spinach BADH gene exhibited an enhanced accumulation of GB (Yang et al. 2005) and were also more stress tolerant than WT tobacco plants, a finding that was attributed to the enhanced CO2 assimilation shown by the transgenic plants (Yang et al. 2008). Application of GB to salt-stressed wheat plants was followed by increases in all of photosynthetic capacity, stomatal conductance, transpiration rate and activities of enzymes associated with antioxidant effects (Ashraf et al. 2008). Also, application of GB alleviated the salt stressinduced inhibition of photosynthesis in wheat plants (Rajasekaran et al. 1997). Finally, transgenic Italian ryegrass (Lolium multiflorum Lam.) plants which were expressing the BADH gene (ZBD1) of zoysiagrass (Zoysia tenuifolia Willd. ex Trin.), showed improved PSII photochemistry

Photosynth Res Table 1 The effects of exogenous GB on growth and other physiological parameters when applied to abiotically stressed crop and forage plant species grown in a controlled environment or under field conditions

Abiotic stress

Plant species

Growth and physiological effect(s)

Drought

Hordeum vulgare L.

Increase in leaf area index (Makela et al. 1996a)

Drought

Zea mays L.

Increase in grain yield (Agboma et al. 1997b)

Drought

Pisum sativum L.

Increase in shoot biomass (Makela et al. 1997)

Drought

Oryza sativa L.

Increase in grain yield (Zhang et al. 2009)

Drought

Sorghum bicolor (L.) Moench

Increase in grain yield (Agboma et al. 1997b)

Drought

Glycine max L.

Increase of photosynthesis (Agboma et al. 1997a)

Drought

Nicotiana tabacum L.

Increase in shoot biomass (Ma et al. 2007)

Drought

Brassica rapa ssp. Oleifera

Increased shoot growth rate (Makela et al. 1997)

Drought

Triticum aestivum L.

Increased shoot biomass (Shahbaz and Zia 2011)

Salinity

Brassica napus L.

Increase in shoot biomass (Athar et al. 2009)

Salinity

Solanum melongena L.

Increase in fruit yield (Abbas et al. 2010)

Salinity

Zea mays L.

Increased shoot biomass (Nawaz and Ashraf 2007)

Salinity

Zea mays L.

Increase in photosynthesis (Ashraf et al. 2008)

Salinity

Capsicum annuum L.

Increased germination (Korkmaz and Sirikci 2011)

Salinity Salinity

Lolium perenne L. Oryza sativa L.

Increase in plant biomass (Hu et al. 2012) Increase in shoot biomass (Demiral and Turkan 2004)

Salinity

Helianthus annuus L.

Increase in shoot biomass (Ibrahim et al. 2006)

Salinity


Increase in photosynthesis (Raza et al. 2007)

Cold

Zea mays L.

Increase in plant biomass (Farooq et al. 2008)

Cold

Zea mays L.

Increase in shoot biomass (Chen et al. 2000)

Cold

Solanum lycopersicum L.

Increase in shoot height (Park et al. 2006)

Cold


Increased freezing tolerance (Allard et al. 1998)

Heat

Hordeum vulgare L.

Increase in shoot biomass (Wahid and Shabbir 2005)

relative to WT plants, when both were subjected to salt stress (Takahashi et al. 2010).

leakage and greater membrane injury, all relative to a different corn variety which did accumulate GB (Yang et al. 1996).

Heat stress Cold stress Transgenic tomato plants expressing the codA gene and WT tomato plants supplemented with exogenously applied GB both showed a greater heat stress tolerance than WT plants that did not receive supplemental GB application (Li et al. 2011). Similarly, transgenic A. thaliana plants over expressing the codA gene (and thus accumulating GB) exhibited an increased tolerance to a short-term heat stress (Hayashi et al. 1998). Barley seeds pre-treated with GB produced seedlings that had a greater shoot biomass and also showed an increased rate of net photosynthesis when the seeds were germinated under heat stress conditions, relative to untreated barley seeds (Wahid and Shabbir 2005). Furthermore, tobacco plants carrying the BADH transgene from spinach accumulated more GB than WT tobacco plants, and coincidentally they exhibited increased heat stress tolerance, both events being associated with increased CO2 assimilation, higher RuBisCO activity and a more stable PSII (Yang et al. 2005). Finally, a cultivar of corn that does not accumulate GB in response to stress showed a reduced heat stress tolerance, as well as a decrease in photochemical activity of PSII, higher electrolyte

Transgenic manipulation with GB biosynthesis can also increase a plant’s tolerance to short-term cold stress, or to a freezing stress which follows a period of cold acclimation. For example, transformation of tomato plants with a chloroplast-targeted codA gene increased the chilling tolerance of the transgenic tomato, relative to WT plants (Park et al. 2004). Similarly, transformation of corn plants with the betA gene resulted in a significantly higher tolerance to cold stress relative to WT plants (Quan et al. 2004a), and this increased tolerance was accompanied by increased efficiency of photosynthesis and a higher total soluble sugar accumulation (Quan et al. 2004b). Foliar applications of GB to tomato seedlings prior to a 3-day cold (3 °C) stress treatment gave a better post-stress recovery after transfer of the GB-treated plants to 25 °C growth conditions, relative to the recovery seen for untreated control plants (Park et al. 2006). Moreover, the pretreatment with GB maintained high rates of photosynthesis under the cold-stress conditions, as well as during the subsequent growth period at 25 °C (Park et al. 2006).

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Furthermore, wheat plants subjected to long-term (6 weeks) cold acclimation at 6 °C gradually and consistently increased their endogenous GB levels in shoot tissues. These cold-acclimated wheat plants also exhibited increased rates of photosynthesis and had better survival rates when exposed to freezing (-10 °C) stress, both relative to non-acclimated plants of the same developmental stage (Allard et al. 1998). Interestingly, the involvement of GB in the protection of photosynthetic processes that are affected by abiotic stress is not just limited to higher plants. For example, cells of the cyanobacterium, Synechococcus sp. PCC7942, showed elevated levels of GB and these high levels of GB were positively correlated with increased stabilization of the activity of RuBisCO in a salt-stressed transgenic, GBoverproducing line (Nomura et al. 1998). Thus, plants subjected to most common types of abiotic stresses, such as drought, salinity and extreme high and low temperatures, show increased GB accumulation that, in turn, is positively associated with an overall increase in photosynthetic performance.

Glycinebetaine and the photosynthetic apparatus Plant growth and development are regulated by plant hormones and also determined by a combination of photosynthetic capacity accompanied by adequate supplies of water and mineral nutrients. Plants subjected to environmental stresses often have a reduced biosynthesis of ‘‘growth’’ hormones, such as gibberellins and auxins (Kurepin et al. 2013b), and these plants also exhibit an increase in photoinhibition of the photosynthetic apparatus (Baker 1991; Long et al. 1994). Chronic photoinhibition is defined as a state in which the photons absorbed by the photosynthetic apparatus exceed the number of photons utilized in carbon assimilation, thereby reducing both plant growth and productivity, mainly due to photodamage that is primarily associated with PSII (Aro et al. 1993; Long et al. 1994). The most vulnerable part of the photosynthetic apparatus is PSII, which is believed to play a key role in a plant’s photosynthetic responses to abiotic stresses (see e.g. Baker 1991; Adams et al. 2013 and cited literature). Glycinebetaine, synthesized in chloroplasts, has been associated with an increased protection of functional proteins, enzymes and lipids of the photosynthetic apparatus that are necessary for maintaining light-dependent linear electron flow (Chen and Murata 2011). In spinach, the first step in GB synthesis, the oxidation of choline to BA, requires reduced ferredoxin generated by photosystem I (Brouquisse et al. 1989; Rathinasabapathi et al. 1997). Thus, there is a direct link between GB biosynthesis and

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photosynthetic electron transport, with GB biosynthesis representing an additional sink for the consumption of photosynthetically generated electrons. Furthermore, exogenously applied GB has been shown to stabilize the oxygen-evolving complex of PSII (Murata et al. 1992; Papageorgiou and Murata 1995) and counteract the stressinduced inactivation of the PSII complex (Mamedov et al. 1993; Allakhverdiev et al. 1996, 2003). Genetic manipulations have also confirmed that GB may decrease PSII susceptibility to photoinhibition most probably functioning as an antichaotropic agent, protecting PSII complex from high light-induced structural damage. Insertion of the codA gene into chloroplast genome of Indian mustard [Brassica juncea (L.) Czern.] plants led to an increased tolerance of PSII to high light intensity under either salt or cold stress (Prasad and Saradhi 2004). Moreover, studies with transgenic rice (Sakamoto and Murata 1998), Arabidopsis (Kondo et al. 1999) and tobacco (Holmstrom et al. 2000) plants which had been genetically modified with either plant or bacterial genes that regulate GB biosynthesis, have demonstrated that the transgenic plants were more tolerant of the photoinhibition that was caused by a range of abiotic stresses. Exogenous application of GB increased the relative area of starch granules and also increased chlorophyll content in salt-stressed tomato leaflets (Makela et al. 2000). Further, application of GB minimized photodamage to the PSI submembrane particles in cold-stressed spinach leaves (Rajagopal and Carpentier 2003). Foliarly applied GB also prevented photoinhibition in wheat during both freezing (Allard et al. 1998) and drought stresses (Ma et al. 2006). GB-treated wheat plants maintained a higher net photosynthesis rate during drought stress than untreated control plants and the maximal photochemistry efficiency of PSII, measured as Fv/Fm, was also increased (Ma et al. 2006). Furthermore, GB-treated wheat plants recovered more rapidly from a drought stress-induced photoinhibition of PSII (Ma et al. 2006). The response of the GB-treated wheat plants to freezing stress was accompanied by an improved tolerance to photoinhibition of PSII and the steady-state yield of electron transport (Allard et al. 1998). In another study, a 100 mM foliar application of GB increased chlorophyll content, modified the lipid composition within the thylakoid membranes, and increased both gas exchange and photosynthesis in drought-stressed wheat (Zhao et al. 2007). Moreover, GB applied to corn plants increased all of CO2 assimilation rate, stomatal conductance, PSII efficiency and photochemical quenching (Yang and Lu 2006). When the photosynthetic fixation of CO2 is limited under various abiotic stresses, excitation pressure is enhanced due to the accumulation of excess reductants at the

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acceptor-side of PSI (Hu¨ner et al. 1996, 1998; Wilson et al. 2006). This results in an increased probability for production of reactive oxygen species (ROS), which can then directly damage both cell and chloroplast membranes (Fig. 2). Several mechanisms exist which can account for the GB-dependent counteraction of the negative impact of high ROS activity during stress events. These mechanisms are stabilization and improvement of photosynthetic performance, and an enhancement of the plant’s abiotic stress tolerance (Sakamoto and Murata 2002; Giri 2011; Chen and Murata 2011) (Fig. 2). First, GB participates in osmoregulation (Liu and Bolen 1995), stabilizing folded protein structures (Low 1985) and protecting the integrity of biological membranes against the well-known direct

Fig. 2 A simplified schematic model for the versatile mode of actions of glycinebetaine (GB) in protecting plant cells and photosynthetic apparatus against damaging effects of abiotic stresses. There are potentially six major routes for GB to increase plant abiotic stress tolerance by counter-acting ROS activity. First, GB participates in osmoregulation and also in stabilizing and protecting the integrity of biological membranes against the well-known direct negative effects of abiotic stresses and ROS. Second, GB may protect the structure and/or functional integrity of the major CO2-fixing enzymes, thus sustaining higher rates of CO2 fixation under abiotic stress. Third, GB plays a vital role in protecting the repair cycle of photodamaged PSII by ROS-induced inhibition of the synthesis of the psbA (D1) protein at the translation step. Fourth, GB may protect the transcription machinery from abiotic stresses and GB likely activates the expression of genes for ROS-scavenging enzymes, resulting in lower levels of ROS, thus mitigating the negative effects of the abiotic stress on the photosynthetic machinery. Fifth, GB may also limit ROS-induced efflux of K? ions by protecting membrane integrity or by a channelblocking function. Finally, GB biosynthesis consumes photosynthesis-generated electrons, which may prevent overreduction of the photosynthetic electron transport chain, thus lowering the probability for generation of ROS. Cyt cytochrome; D1 reaction centre protein of photosystem II encoded by the psbA gene; DNA deoxyribonucleic acid; Fd ferredoxin; FNR ferredoxin NADP? oxidoreductase; mRNA messenger ribonucleic acid; NAD(P)H nicotinamide adenine dinucleotide phosphate; QA, QB primary and secondary electron acceptors of PSII; PC plastocyanin; PQ plastoquinone; PS photosystem; ROS reactive oxygen species

negative effects of abiotic stresses and ROS-induced lipid peroxidation (Chen et al. 2000). Second, GB may protect the structure and/or functional integrity of the major CO2fixing enzymes (Rubisco, Rubisco activase, FBPase, FBP aldolase, and PRKase) by acting as a molecular chaperone, thus sustaining higher rates of CO2 fixation under conditions of abiotic stress (Makela et al. 2000). Consequently, the production of ROS will be decreased. Third, GB plays a vital role in protecting the repair cycle of photodamaged PSII, i.e. damage by ROS-induced inhibition of the synthesis of the psbA (D1) protein of the PSII reaction centre at the translation step (Ohnishi and Murata 2006). Fourth, GB may protect the transcriptional machinery from abiotic stresses, and GB also likely activates the expression of genes which encode for ROS-scavenging enzymes. This will result in lower levels of ROS, thus mitigating the negative effects of the abiotic stress on the photosynthetic machinery. Fifth, GB may also limit ROS-induced efflux of K? ions by protecting membrane integrity or by a channelblocking function (Cuin and Shabala 2007). In addition to these already identified mechanisms, an earlier study has provided direct evidence for a CMO being present in the spinach chloroplast stroma (Brouquisse et al. 1989). Moreover, the first step in GB biosynthesis (the oxidation of choline to BA by CMO) requires reduced ferredoxin (Lerma et al. 1988; Brouquisse et al. 1989; Rathinasabapathi et al. 1997), a finding that links GB synthesis with photosynthetic electron transport. In addition, since the overreduction of chloroplast stroma and/or the photosynthetic synthesis of GB from choline consumes reducing energy, GB biosynthesis process may alleviate electron transport chain. Hence, we suggest that the stressinduced GB biosynthesis pathway may well serve as an additional, alternative biochemical sink, one which consumes photosynthesis-generated electrons. If so, this will lower the excitation pressure and reduce the harmful levels of ROS under unfavourable environmental conditions when the acceptor site capacity of photosystem I (PSI), i.e. CO2 assimilation is limited (Wilson et al. 2006).

Glycinebetaine interaction with plant hormones and photosynthesis The increased abiotic stress tolerance seen for plants that are capable of accumulating GB in response to stress, either naturally or by means of genetic transformation, often translates into increased vegetative growth and/or reproductive yield. This GB accumulation occurs not only for stressed plants, but also in unstressed plants grown under optimal conditions. For example, introduction of a spinach gene for CMO production into rice plants that have a nonfunctional gene for CMO biosynthesis, and thus do not

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accumulate GB (Sakamoto and Murata 1998), caused accumulation of endogenous GB in response to either salt or temperature stress (Shirasawa et al. 2006). These transgenic, stressed rice plants also exhibited enhanced shoot dry weight and tillering, although they had slightly less root growth (Shirasawa et al. 2006). Growth and developmental events in plants, such as shoot biomass growth, tillering or root expansion, are regulated by plant hormones (Davies 2010). The biosynthesis and action of plant hormones are tightly controlled by abiotic cues, such as light, water availability, or temperature status (Kurepin et al. 2011, 2012a, Kurepin and Pharis 2014; Qaderi et al. 2006; 2012). Thus, it is not surprising that in addition to accumulation of endogenous GB, abiotic stress will also cause changes in endogenous plant hormone levels (Abeles et al. 1992; Dodd and Davies 2010; Kurepin et al. 2013c; Hu¨ner et al. 2014). While accumulation of endogenous GB is typically associated with abiotic stress events that yield increased plant stress tolerance and also an increased or sustained growth, there is increasing evidence that genetically induced GB accumulation in non-stressed plants is also associated with an increase in plant growth. For example, over expression of the codA gene in tomato plants caused an accumulation in GB levels and concomitantly produced larger flowers (due to an increase in both cell size and number of cells) and also larger fruits, even when the plants were grown under optimal, non-stress conditions (Park et al. 2007b). However, based on the available literature, it seems unlikely that there is a direct growth-promotive role for GB Instead, it is quite possible that accumulation of GB in non-stressed plants can modify production of endogenous plant hormones involved in plant stress response(s), i.e. ABA, ethylene and SA, just as it does in abiotically stressed plants (Abeles et al. 1992; Dodd and Davies 2010; Kurepin et al. 2013c; Hu¨ner et al. 2014). Abscisic acid Abscisic acid plays a major role in seed development and acclimation of higher plants to several abiotic stresses. For example, a plant’s response to drought stress includes rapid de novo synthesis of ABA, which occurs in leaves of stressed plants, and this quickly leads to stomatal closure, which helps to protect the plant from rapid desiccation (Schwartz and Zeevaart 2010). Thus, manipulation of ABA biosynthesis or ABA signal transduction could, logically, be causal for enhanced plant resistance to abiotic stresses. Indeed, overexpression of genes involved in ABA biosynthesis in wild tobacco (Nicotiana plumbaginifolia Viv.) and tomato plants gave increases in endogenous ABA levels by as much as 10-fold (Thompson et al. 2000; Qin and Zeevaart 2002). Associated with these increases in

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ABA content were increases in the tolerance of both species to drought stress (Thompson et al. 2000; Qin and Zeevaart 2002). Interestingly, an increase in plant ABA content that was caused by providing (daily) supplements of exogenous ABA decreased the stomatal conductance, but had no negative effect on photosynthetic capacity of Virginia spiderwort (Tradescantia virginiana L.) leaves (Franks and Farquhar 2001). Furthermore, exogenously applied ABA increased thermostability of barley chloroplasts (Ivanov et al. 1992) and enhanced the resistance of barley seedlings to photoinhibition of PSII (Ivanov et al. 1995). However, constitutive overproduction of ABA may act differently from exogenously applied ABA. For example, a constitutive overproduction of ABA could negatively influence the biosynthesis or action of other plant growthpromoting hormones, such as gibberellins and auxins (Schwartz and Zeevaart 2010), thereby leading to reduced growth and delayed reproductive development (Thompson et al. 2000; Qin and Zeevaart 2002). A simplistic conclusion, then, is that plants which naturally overproduce ABA should only outperform ‘normal’ plants when both are grown in environments characterized by constant abiotic stress. For barley (Hordeum vulgare L.) plants, GB has been shown to play an important role in protecting this species from abiotic stresses such as high salt levels, drought and freezing (Hitz et al. 1982; Arakawa et al. 1990; Kishitani et al. 1994). Thus, barley plants that were subjected to high-salt or drought stress conditions showed appreciable increases in BADH mRNA levels in both their leaves and roots. These high BADH mRNA levels, however, were reduced if plants were removed from the stress conditions (Ishitani et al. 1995). Of interest, also is the finding that exogenously applied ABA also substantially increased the BADH mRNA levels in leaves and roots of barley plants (Ishitani et al. 1995). In another study, with barley plants grown hydroponically, application of ABA also caused significant increases in GB accumulation in salt-, drought-, or cold-stressed plants (Jagendorf and Takabe 2001). Thus, exogenous applications of ABA can cause both an accumulation of endogenous GB and a significant increase in the barley plant’s tolerance to stress, without causing any obvious negative side effects (Jagendorf and Takabe 2001). Foliar application of either GB or ABA to a turf field populated mainly by creeping bentgrass (Agrostis stolonifera) and Kentucky bluegrass (Poa pratensis) similarly increased plant stress tolerance to drought and salinity (Yang et al. 2012). Sorghum plants subjected to high salt stress had increased BADH mRNA transcript with an accompanying increase in endogenous GB levels, again implying de novo biosynthesis of GB in response to stress (Saneoka et al. 2001). The high salt stress of the sorghum

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plants also increased endogenous ABA levels (Saneoka et al. 2001). Cold acclimation of A. thaliana plants resulted in elevated levels of endogenous GB and an enhanced tolerance to freezing (Xing and Rajashekar 2001). Freezing tolerance was also increased by exogenous application of either GB or ABA. Application of ABA also increased endogenous GB accumulation in non-acclimated control plants (Xing and Rajashekar 2001). Fluridone [1-methyl-3phenyl-5-(3-(trifluoromethyl)phenyl)-4(1H)-pyridinone], an inhibitor of carotenoid biosynthesis, not only lowered endogenous ABA levels, but also reduced BADH mRNA transcript levels (Saneoka et al. 2001). Drought-stressed corn plants showed a temporal difference in ABA and GB accumulation: a drought stress-induced ABA accumulation was observed first, and this was followed by a stimulation of BADH activity and increased GB accumulation (Zhang et al. 2012). In contrast, application of fluridone, which inhibits ABA biosynthesis (Gamble and Mullet 1986), reduced endogenous ABA concentration as well as the levels of accumulated GB (Zhang et al. 2012). In a separate experiment, exogenously applied ABA increased the BADH activity in corn plants and also increased the accumulation of GB, shoot dry biomass and leaf’s relative water content. Thus, there appears to be a direct interaction between ABA and GB, one where abiotic stress first increases the plant’s ABA biosynthesis, which then leads to enhanced BADH activity and thus an increased GB accumulation, both ABA and GB being positively associated with an increased stress tolerance. Also, accumulation of another osmoregulator, proline, can be enhanced by exogenously applied ABA in abiotically stressed plants. For example, high proline levels were associated with increased concentrations of endogenous ABA, the latter being caused by salt stress (Savoure et al. 1997). However, there was no correlation of endogenous proline levels and ABA with cold or osmotic stresses (Savoure et al. 1997). Hare et al. (1999) thus concluded that proline biosynthesis can be mediated by both ABA-dependent and ABA-independent signalling pathways. This is contrary to GB biosynthesis which appears to be directly upregulated by ABA. Ethylene Ethylene is a gaseous plant hormone that is required, at low levels, for optimal plant growth (Lee and Reid 1997; Walton et al. 2012). Increased ethylene production is typically associated with plant abiotic stress responses (Abeles et al. 1992; Morgan and Drew 1997). In higher plants, ethylene is biosynthesized by a pathway that is now well defined. There is an initial conversion of L-methionine

to S-adenosylmethionine (SAM), also sometimes called AdoMet (Adams and Yang 1979). As noted earlier, SAM is also an early precursor in GB biosynthesis. SAM is converted to 1-aminocyclopropane-1-carboxylic acid (ACC), a step catalysed by ACC synthase. The final step is the conversion of ACC to ethylene, where ACC oxidase acts as the catalytic enzyme (Kende 1993). However, species that exhibit increases in ethylene production during cold acclimation, such as tobacco and tomato (Ciardi et al. 1997; Zhang and Huang 2010), do not accumulate GB in response to abiotic stress (Nuccio et al. 1998; Park et al. 2004). In direct contrast, species that show a decreased ethylene production during cold acclimation, such as bean and wheat (Field 1984; Machacckova et al. 1989; Collins et al. 1995), do accumulate GB in response to abiotic stresses (McDonnell and Jones 1988; Allard et al. 1998; Wang et al. 2010a). These very contrasting responses are also of interest because during ethylene biosynthesis, SAM donates a methyl group to choline, a phenomenon which suggests a potential interaction between ethylene and GB at the level of hormone biosynthesis. Salicylic acid Abiotic stresses such as drought, extreme temperatures, reductions in light irradiance or quality, and treatment with UV light, can also yield increases in endogenous SA levels in plant shoots (Yalpani et al. 1994; Scott et al. 2004; Wang et al. 2005; Kurepin et al. 2010, 2012b, 2013a). The role of SA as an endogenous signalling molecule in plant defence mechanism(s) against pathogens, as well as, its effect on the physiology and reproductive development of some higher plants has been well described (Raskin 1995; Delaney 2010). More interesting, though, is the fact that abiotic stress-induced increases in endogenous SA levels are paralleled by similar increases in endogenous ABA levels (Kurepin et al. 2013a). Thus, SA and ABA may function in the same physiological processes that are influenced by abiotic stress. In fact, elevated levels of SA and ABA were positively associated with increased GB accumulation in stressed barley plants (Jagendorf and Takabe 2001). The negative effect of exogenously applied SA on photosynthesis of intact leaves of unstressed plants is likely concentration-dependent. For example, SA applied to unstressed tobacco leaves induced stomatal closure, thus decreasing both CO2 assimilation and PSII electron transport (Janda et al. 2012). Yet, SA applied to unstressed grapevine (Vitis vinifera L.) leaves had no effect on photosynthesis (Wang et al. 2010b). These apparently contradictory results are best explained by the difference in the concentrations of applied SA: 10 mM SA was used for the tobacco study (Janda et al. 2012), whereas only 0.1 mM SA was used in

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the grapevine study (Wang et al. 2010b). As with most other plant hormone classes, application of SA at above optimal levels can cause inhibitory effects on growth, physiology or metabolic processes of plant tissues. In contrast, SA applied at lower levels (close to optimal) can often have beneficial effects on these processes, especially for stressed plants (Kurepin et al. 2013a). Indeed, as described by Mateo et al. (2006), low SA levels are required for optimal photosynthesis and redox homeostasis.

Conclusions In brief, stress-induced accumulation of GB coincides with elevated amounts of a number of stress-responsive hormones (Jagendorf and Takabe 2001). Abscisic acid has been reported to increase the expression of the BADH gene in response to both osmotic (Ishitani et al. 1995) and salt (Saneoka et al. 2001) stresses. ABA is also involved in the water stress-induced GB accumulation in wheat (Nayyar and Walia 2004) and pear leaves (Gao et al. 2004b). Salicylic acid increases GB accumulation in stressed barley plants (Jagendorf and Takabe 2001). There is also an indication that jasmonic acid (JA) is involved in droughtinduced GB accumulation (Gao et al. 2004a). Thus, it appears that the increased abundance of GB under some, if not all, abiotic stress conditions may be under hormonal control, although further research is needed to validate this proposition. However, although plant hormone-induced abiotic stress alleviation may well depend on the ability of ABA and SA (and, potentially, ethylene), to increase GB biosynthesis, these plant hormones may also act independently of GB in influencing the plant’s photosynthetic performance in response to abiotic stress. It appears that a first response of a plant to abiotic stress is an increase in endogenous ABA levels, thereby leading to an increase in the accumulation of GB. High levels of ABA function to close stomata which prevent excessive water loss, while GB protects the photosynthetic apparatus. This suggests a close interaction between GB and ABA in plant stress response(s). A schematic model representing the potential synergistic roles of GB and ABA in the protection of plants against low-temperature stress and in the process of cold acclimation is presented in Fig. 3. Exposure of plants to low-temperature stress induces upregulation of ABA and GB biosynthesis. Abscisic acid alone can also induce GB biosynthesis, thereby increasing its endogenous levels (Xing and Rajashekar 2001). This suggests that low-temperature-induced GB accumulations may be regulated by ABA. In addition, since elevated ABA levels have often been associated with a decrease in shoot growth (Trewavas and Jones 1991; Munns and Cramer 1996), the increased levels of endogenous ABA in cold-

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Fig. 3 A schematic model for the synergistic roles of GB and ABA in the protection of plants against low-temperature stress and cold acclimation. Exposure of plants to low-temperature stress induces upregulation of ABA and GB biosynthesis. It appears that ABA alone can also induce GB biosynthesis, thus suggesting that low-temperature-induced GB enhancement may be regulated by ABA. The physiological effects of elevated GB successfully counteract the negative stress responses imposed by the low temperature and induce higher freezing tolerance of cold-stressed plants. In addition, elevated levels of ABA at low temperature can effectively suppress growth promoting gibberellins (GA) causing the appearance of a dwarf phenotype typical for cold acclimated plants. Taken together, the close interaction and synergistic physiological effects of GB and ABA resulting in increased freezing tolerance and dwarf phenotype are the major factors leading to effective cold acclimation of higher plants

stressed plants may play a critical role in the development of the dwarf cold-acclimated phenotype (Fig. 3). Historically, gibberellins (GAs) and ABA have been reported to act antagonistically in the regulation of shoot growth, and both plant hormones can down-regulate each other’s biosynthetic genes (Zentella et al. 2007; Kurepin et al.

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2013c). Indeed, ABA inhibits the expression of GA biosynthetic genes, GA20ox and GA3ox, during seed germination, and thus, reduces the levels of growth-active endogenous GAs (Toh et al. 2008). Antagonistic association between ABA and GA20ox and GA3ox genes was also found in sunflower hypocotyls subjected to a range of low temperatures (Kurepin et al. 2011). Similarly, cold tolerance was strongly associated with higher endogenous ABA levels and lower endogenous GA1 and GA4 levhighels in four bamboo species (Zhang and Huang 2010). Thus, while the low-temperature-mediated increase in the endogenous levels of GB accounts for an increased freezing tolerance and may occur independently of ABA, the elevated levels of ABA at low temperature can effectively reduce the levels of growth-promoting GAs through an antagonistic interaction with GA. Taken together, we suggest that the close interaction and synergistic physiological effects of GB and ABA resulting in increased freezing tolerance and a dwarf phenotype are the major factors leading to effective cold acclimation of higher plants. Acknowledgments We would like to acknowledge the financial support from the Ballance Agri-Nutrients, New Zealand (MZ, LVK, RPP), KEMPE Foundation, Sweden (VMH, LVK, NPAH), Natural Sciences and Engineering Research Council of Canada (NPAH), the Canada Research Chairs Program (NPAH) and the Canada Foundation for Innovation (NPAH). SIA was supported by Grants from the Russian Foundation for Basic Research (Nos: 14-04-01549, 14-0492690) and by Molecular and Cell Biology Programs of the Russian Academy of Sciences.

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Current Understanding of the Interplay between Phytohormones and Photosynthesis under Environmental Stress.

Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance.

Regulation of Photosynthesis during Abiotic Stress-Induced Photoinhibition.

Organization and Regulation of Soybean SUMOylation System under Abiotic Stress Conditions.

Regulation of Banana Phytoene Synthase (MaPSY) Expression, Characterization and Their Modulation under Various Abiotic Stress Conditions.

Functional characterization of a plastid-specific ribosomal protein PSRP2 in Arabidopsis thaliana under abiotic stress conditions.

Identification of Cassava MicroRNAs under Abiotic Stress.

Accumulation of Flavonols over Hydroxycinnamic Acids Favors Oxidative Damage Protection under Abiotic Stress.

Photoinhibition of photosynthesis in willow leaves under field conditions.

The role of glycinebetaine in the protection of spinach thylakoids against freezing stress.

Cytochrome P-450 under conditions of oxidative stress: role of antioxidant recycling in the protection mechanisms.

Abiotic methanogenesis from organosulphur compounds under ambient conditions.

Grape Composition under Abiotic Constrains: Water Stress and Salinity.

Brassinosteroid Mediated Cell Wall Remodeling in Grasses under Abiotic Stress.

Evaluation of the yield of abiotic-stress-tolerant AtDREB1A transgenic potato under saline conditions in advance of field trials.

Identification of candidate reference genes in perennial ryegrass for quantitative RT-PCR under various abiotic stress conditions.

ABA signal in rice under stress conditions.

Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance.

ATHB17 enhances stress tolerance by coordinating photosynthesis associated nuclear gene and ATSIG5 expression in response to abiotic stress.

Adrenosympathetic overactivity under conditions of work stress.

Protein quality control under oxidative stress conditions.

Abiotic synthesis of amino acids under hydrothermal conditions and the origin of life: a perpetual phenomenon?

Abiotic synthesis of amino acids and self-crystallization under prebiotic conditions.

Stress and photosynthesis.