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ScienceDirect Transcriptional networks in leaf senescence Jos HM Schippers Plant senescence is a natural phenomenon known for the appearance of beautiful autumn colors and the ripening of cereals in the field. Senescence is a controlled process that plants utilize to remobilize nutrients from source leaves to developing tissues. While during the past decades, molecular components underlying the onset of senescence have been intensively studied, knowledge remains scarce on the agedependent mechanisms that control the onset of senescence. Recent advances have uncovered transcriptional networks regulating the competence to senesce. Here, gene regulatory networks acting as internal timing mechanisms for the onset of senescence are highlighted, illustrating that early and late leaf developmental phases are highly connected. Address Institute of Biology I, RWTH Aachen University, Worringerweg 1, 52074 Aachen, Germany Corresponding author: Schippers, Jos HM ([email protected])

Current Opinion in Plant Biology 2015, 27:77–83 This review comes from a themed issue on Cell signalling and gene regulation Edited by Xiaofeng Cao and Blake C Meyers

http://dx.doi.org/10.1016/j.pbi.2015.06.018 1369-5266/# 2015 Elsevier Ltd. All rights reserved.

Introduction Plants are self-sustaining by taking up nutrients from their direct surroundings and harvesting light for their energy metabolism. Still, due to fluctuating environmental conditions, plants are morphologically highly plastic and follow a developmental strategy that is largely defined by their surroundings. One of these adaptive mechanisms is represented by the senescence syndrome, which involves the controlled dismantling of a leaf for nutrient remobilization. Under optimal conditions, the onset of leaf senescence occurs in an age-dependent manner, however, the process can be induced prematurely by endogenous and exogenous stimuli. In response to severe stress, survival of the plant can be achieved by recycling of older leaves via senescence. In addition, as gathering nutrients is a large investment, it makes sense to re-use them or pass them on to the next generation during reproductive senescence. www.sciencedirect.com

Strict control over the progression of senescence allows for coordinated dismantling of leaf cells to reach a high level of nutrient remobilization [1]. Chloroplast are the first organelles to be dismantled and form a rich source of nitrogen. In addition, degradation of proteins results in increased amounts of free amino acids which are either used by the senescing leaf as alternative respiratory substrates or are transported to sink tissues such as developing seeds [2,3]. Furthermore, remobilization of phosphate during reproductive senescence through degradation of organelle DNA and ribosomal RNA supports the viability of newly developing seeds [4]. Likewise, micronutrients, essential for the plant and the nutritional quality of crops, are efficiently transported to developing grains during senescence [5]. During the developmental course of the leaf, including the onset and progression of leaf senescence, continuous reprogramming of gene expression occurs [6]. Although a description of transcript level changes at the onset of senescence is available, we are only starting to understand which transcriptional regulators control which part of the dynamic gene network underlying senescence. Transcription factors in general control a subset of genes, however, the promoter of a single gene can be recognized by hundreds of transcription factors [7]. Thus, transcriptional networks are very complex as many factors exert control over a single promoter. Still, by unraveling gene networks, we can shed light on the mechanisms underlying senescence, which allows for novel biotechnological applications. In this review, an overview of the current transcriptional networks that regulate leaf senescence is given. Special emphasis is placed on how these networks regulate the competence to senesce during development. Furthermore, several key transcriptional networks integrating environmental cues with the onset of senescence are presented.

Senescence window concept The observation that senescence induction depends on the developmental phase of the leaf can be explained by the ‘senescence window’ concept (Figure 1). This concept assumes three distinct leaf developmental phases in relation to the induction of senescence. During the first phase, the leaf is undergoing proliferation and cell expansion and is consequently not able to perceive cues from senescence-inducing factors [8]. Upon maturation, the leaf becomes competent for signals that induce premature senescence (Figure 1). The competence to senesce increases with leaf age. In an attempt to explain Current Opinion in Plant Biology 2015, 27:77–83

78 Cell signalling and gene regulation

Figure 1

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The senescence window concept. As the leaf ages, it becomes permissive to the induction of senescence by external factors. This establishment of competence to senesce is explained by the accumulation of age-related changes (ARCs). During early leaf development, phase I, external factors cannot promote senescence. Upon maturation, phase II, the leaf becomes competent for the perception of environmental signals that can cause premature senescence. Inevitable, phase III, the steadily increase in ARCs will result in the initiation of developmental senescence, independent from external factors.

this observation, the term age-related changes (ARCs) was introduced [9,10]. During the development of the leaf, ARCs accumulate up to a level that senescence will be initiated, even under optimal conditions, as illustrated by the final phase of the senescence window (Figure 1). Of note, ARCs do not represent deleterious changes per se, as during the phase of senescence, the leaf remains able to perceive signals that delay or revert senescence progression [11,12].

Developmental senescence networks Studying transcription factors that control the onset of senescence has resulted in the identification of senescence-associated gene networks. In several cases, the uncovered transcriptional networks can explain the increasing commitment of the leaf to undergo senescence. The here presented age-dependent networks are drawn in relation to the senescence window concept and the plant hormones involved (Figure 2). Ethylene accumulates during leaf ageing, resulting in the activation of ETHYLENE-INSENSITIVE 3 (EIN3), a positive regulator of leaf senescence [13]. The induction of senescence by EIN3 in part depends on the action of the transcription factor ORESARA 1 (ORE1). Previously, it was shown that ORE1 transcript accumulation is regulated by the activity of miR164 in an ethylene-dependent and age-dependent manner [14]. While ethylene levels gradually increase during leaf ageing, miR164 levels Current Opinion in Plant Biology 2015, 27:77–83

decline, allowing for the accumulation of ORE1 transcripts. EIN3 represses the expression of miR164, but at the same time stimulates ORE1 expression [13,15,16]. In addition, a recent genome-wide binding analysis for EIN3 [17] revealed the presence of many senescenceassociated genes (SAGs) encoding transcription factors among direct EIN3 targets. Interestingly, in several cases, EIN3 binds to the same promoter as the downstream transcription factor ORE1. For example, both ORE1 and EIN3 regulate NAC083, NAC102 and SAG29 [16,17], forming a coherent feed-forward loop. Among ABA-associated senescence modules, the network built around NAC-LIKE ACTIVATED BY AP3/ PI (NAP) is the best studied (Figure 2). Transcript levels of NAP increase with leaf age, which in part occurs through activation of ABA INSENSITIVE 5 (ABI5) [18,19]. In addition, also ethylene seems to promote NAP expression, as EIN3 was shown to act upstream of NAP [15,16,20]. Interestingly, protein levels of ABI5 are repressed by cytokinin through the action of ARABIDOPSIS RESPONSE REGULATOR 12 (ARR12) [21], which could explain why NAP transcript levels are not detectable in young leaves, since they contain high levels of cytokinin. NAP itself activates several target genes, including SAG113, encoding a protein phosphatase 2C protein that negatively regulates ABA-mediated stomatal closure to promote water loss in leaves during senescence [22,23]. Furthermore, NAP stimulates ABA biosynthesis www.sciencedirect.com

Transcriptional networks in leaf senescence Schippers 79

by upregulating the expression of ABSCISIC ALDEHYDE OXIDASE 3 (AAO3) [20]. Next to that, NAP promotes chlorophyll degradation through induction of NON-YELLOW COLORING 1 (NYC1) together with ABI5 [15,20,24]. Another leaf age timing mechanism in Arabidopsis is established by TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) transcription factors that antagonistically regulate the expression of the JA biosynthesis gene LIPOXYGENASE2 (LOX2) [25,26]. Class II TCP transcription factors, including TCP4, are repressed by miR319 during early leaf establishment, while class I TCPs, like TCP9 and TCP20, are active to promote cell proliferation. Interestingly, overexpression of miR319 or loss of multiple class II TCP genes results in delayed senescence [25,27]. On the other hand, loss of TCP9 and TCP20 leads to precocious senescence. Whereas TCP4 activates LOX2, TCP9 and TCP20 were found to bind to the LOX2 promoter and repress the JA biosynthesis pathway. As class II TCPs accumulate with age, the JA pathway is gradually activated, contributing to the onset of senescence. A classical developmental senescence network is regulated by the salicylic acid (SA) inducible WRKY53 transcription factor, which promotes senescence by activating the expression of SAG12, CATALASE 1/2/3 and ORE9 [28]. Recently, it was found that WRKY53 expression is stimulated by hydrogen peroxide in an REVOLUTA (REV)dependent manner [29]. Although REV is mainly known for its role in meristem maintenance and organ polarity, loss-of-function mutant plants of REV display a delayed onset of leaf senescence. Potentially, positive regulation of WRKY53 during the early stages of leaf development is linked to protecting the plants from oxidative stress. WRKY53 activity is inhibited through interaction with EPITHIOSPECIFYING SENESCENCE REGULATOR (ESR), whose transcript levels decrease with leaf age [30]. Interestingly, ETHYLENE RESPONSE FACTOR 4 (ERF4) and ERF8 are required for repression of ESR during leaf development [31]. In the erf4/erf8 double mutant, the level of ESR is maintained, resulting in delayed senescence. In addition, WHIRLY1 (WHY1), acts as a direct negative transcriptional regulator of WRKY53 in an age-dependent manner [32]. The WRKY53-induced ORE9 gene encodes an F-box protein that is involved in degradation of the central brassinosteroid (BR) signal regulators BRASSINAZOLE-RESISTANT 1 (BZR1) and BRI1-EMS-SUPPRESSOR 1 (BES1) [33]. In line with this, bes1 mutant plants display early senescence [34], while exogenous application of BR represses the expression of a large set of senescence-related NAC genes, including NAC002, NAC019, NAC055 and NAC072 [35]. Moreover, both BZR1 and BES1 directly bind to the promoters of www.sciencedirect.com

these NAC genes [36,37]. In addition, BZR1 positively regulates the expression of WRKY57 [38], which in turn acts to prevent precocious developmental senescence by directly repressing SAG4 and SAG12 [39]. Interestingly, protein levels of WRKY57 are antagonistically controlled by JA and auxin. JA treatment reduces WRKY57 protein amounts, while auxin results in accumulation of WRKY57 protein. Taken together, transcriptional networks directed by different plant hormones represent age-dependent mechanisms that control the competence to senesce.

Environmentally induced senescence Transcriptional changes during developmental senescence largely overlap with those observed during senescence induced by environmental signals [40]. Still, the initial gene expression profiles of induced senescence and developmental senescence differ significantly, indicating that the primary response of the plant upon stress is preservation of the leaf, and that only under prolonged stress conditions, senescence is induced. Here, several examples of environmental-related transcriptional networks controlling senescence during abiotic stress are summarized (Figure 3). Plants contain a diverse set of photoreceptors to measure light conditions and adjust their growth and development accordingly. Phytochrome A (phyA) and phyB play central roles in light-directed plant development [41]. Lightactivated phyA and phyB target PHYTOCHROME INTERACTING FACTORs (PIFs) for protein degradation [42]. During prolonged darkness, PIF4 and PIF5 can accumulate and initiate a robust senescence program [15]. Interestingly, both PIFs directly activate ABI5 and EIN3, which together activate ORE1 (Figure 3). In addition, PIFs stimulate chlorophyll degradation through the activation of STAY-GREEN 1 (SGR1) and NYC1 by ABI5. Notably, short pulses of red light, which activate phyB, prevent the onset of senescence even when plants are kept for 10 days in darkness. Furthermore, the action of PIF4 and PIF5 is repressed by the circadian clock through a transcriptional complex including EARLYFLOWERING 3 (ELF3) [43]. Indeed, overexpression of ELF3 represses dark-induced senescence by inhibiting PIF4 and PIF5 at the transcriptional level [15]. Taken together, the PIF4/PIF5-initiated feed-forward loops demonstrate that plants integrate signals from light or abiotic stress with ARCs to time the onset of senescence. Drought represents a frequently occurring abiotic stress impairing plant growth due to a reduction in sink strength of young organs and assimilate accumulation in source leaves [44,45], resulting in premature senescence. It was recently shown that NAC WITH TRANSMEMBRANE MOTIF 1-LIKE 4 (NTL4) is a positive regulator of senescence during drought stress [46]. Although NTL4 Current Opinion in Plant Biology 2015, 27:77–83

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Figure 2

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Transcriptional networks controlling developmental senescence in Arabidopsis. Leaf development starts with the never senescence phase (green), which is followed by a senescence competence phase (light-green), and then goes into the always senescence phase (yellow). This progression of leaf ageing involves a steady build-up of age-related changes (ARCs), and an increase in the level of hormones that promote senescence or a decrease in those that delay senescence. A gradual decline of miR164 levels results in the ethylene-dependent activation of ORE1 (orange). Ultimately, EIN3 and Current Opinion in Plant Biology 2015, 27:77–83

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Transcriptional networks in leaf senescence Schippers 81

Figure 3

Light/darkness SGRI ELF3

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Current Opinion in Plant Biology

Transcriptional networks controlling the onset of senescence in response to the environment. Deprivation of light (violet) results in stabilization of PIF4 and PIF5, which, under light exposure, are targeted for degradation by phyB. In addition, at the transcriptional level, both PIF genes are repressed by the evening clock transcription factor ELF3. Prolonged darkness results in a PIF-controlled feed-forward cascade that activates the expression of ABI5, EIN3 and ORE1, resulting in a robust onset of senescence. During drought stress (green), the NAC transcription factor NTL4 is activated both at the transcriptional as well as the post-translational level. Subsequently, NTL4 induces the expression of RbohC and RbohE, resulting in the accumulation of ROS and subsequent onset of senescence and cell death. Upon salinity (blue), VNI2 is activated in an ABA-dependent manner to protect leaves from precious senescence. For this, VNI2 promotes the expression of COR15A/B and RD29A/B, providing salt stress tolerance.

represents a developmental SAG, its loss or overexpression under optimal conditions does not affect the timing of age-induced senescence [46]. NTL4 activates the expression of the NADPH oxidase-encoding genes

RESPIRATORY BURST OXIDASE HOMOLOG C (RbohC) and RbohE, resulting in an increase in reactive oxygen species (ROS) production and subsequent onset of senescence and cell death.

( Figure 2 Legend Continued ) ORE1 build a feed-forward loop that initiates the onset of senescence. The role of ABA (light-blue) in regulating leaf senescence is established through the action of NAP. During early stages of leaf development, the levels of the NAP upstream regulator ABI5 are repressed through the action of cytokinin. The gradual decline in cytokinin and increase in ABA levels result in the activation of NAP that not only stimulates ABA biosynthesis but also the degradation of chlorophyll. JA biosynthesis (green) is repressed during early stages of leaf development by class I TCP transcription factors (TCP9 and TCP20) and miR319. With age, the action of miR319 is reduced and class II TCP transcription factors (TCP4) exert positive control over JA biosynthesis, causing the induction of senescence. WRKY53 represents a central regulator of SA (yellow) and ROS, whose activity is limited by ESR and positively regulated by REV. The age-dependent increase in the activity of ERF4 and ERF8 results in the repression of ESR and the release of WRKY53 activity to provoke the onset of senescence. One the direct targets of WRKY53, ORE9, encodes an F-box protein that represses BR responses (blue) during late leaf developmental stages by targeting BZR1 and BES1 for degradation. BZR1 and BES1 are known to directly repress the activity of several senescence-related NAC genes. Furthermore, BZR1 activates the transcriptional repressor WRKY57, which blocks the expression of SAG4 and SAG12. www.sciencedirect.com

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Similar to drought stress, salinity impairs plant growth and sink strength of young tissues, leading to precocious senescence of older tissues. VND-INTERACTING2 (VNI2)/NAC083 acts as a negative regulator of developmental senescence [47]. In addition, VNI2 is specifically induced during salt stress in an ABA-dependent manner and its loss-of-function mutation results in premature saltinduced senescence. Interestingly, under salt stress, VNI2 promotes leaf longevity by activating COLD-REGULATED (COR) and RESPONSIVE TO DEHYDRATION (RD) genes [47,48]. Thus, VNI2 modulates leaf senescence by integrating environmental stress with leaf ageing.

Concluding remarks Apart from the current characterized gene networks implicated in the regulation of leaf senescence, only a small fraction of the complex transcriptional network controlling senescence has been explored. As illustrated above, mechanisms resulting in the competence to senesce are established in an age-dependent manner, with early leaf stage networks affecting those controlling late leaf stages. To better understand the interplay between ARCs and the onset of senescence, one should not only characterize single components activated during senescence, but also focus on molecular network dynamics during the whole lifespan of the leaf. Another challenge is filling the molecular knowledge gap of senescence regulation in crops. Present molecular studies on senescence in crops clearly demonstrate the importance of this process for crop productivity and grain quality [5,24]. In addition, little is known concerning the evolution of the senescence program, besides that the process itself is employed by many different plant species to efficiently use nutrients. It was recently reported that the function of NAP is conserved in rice and Arabidopsis [24], indicating that the transcriptional regulation of senescence is in part conserved between dicots and monocots. Finally, as SAGs often have roles in plant stress tolerance, their exploration might help to understand how plants adapt to a changing environment.

Acknowledgements I thank Romy Schmidt of the RWTH Aachen University for her critical reading and contributions to the manuscript.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest

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Transcriptional networks in leaf senescence.

Plant senescence is a natural phenomenon known for the appearance of beautiful autumn colors and the ripening of cereals in the field. Senescence is a...
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