Plant leaf senescence and death - regulation by multiple layers of control and implications for aging in general.
TL;DR: This Commentary discusses the latest understandings and insights into the underlying molecular mechanisms, and presents the perspectives necessary to enable system-level understanding of leaf senescence, together with their possible implications for aging in general.
Abstract: How do organisms, organs, tissues and cells change their fate when they age towards senescence and death? Plant leaves provide a unique window to explore this question because they show reproducible life history and are readily accessible for experimental assays. Throughout their lifespan, leaves undergo a series of developmental, physiological and metabolic transitions that culminate in senescence and death. Leaf senescence is an 'altruistic death' that allows for the degradation of the nutrients that are produced during the growth phase of the leaf and their redistribution to developing seeds or other parts of the plant, and thus is a strategy that has evolved to maximize the fitness of the plant. During the past decade, there has been significant progress towards understanding the key molecular principles of leaf senescence using genetic and molecular studies, as well as 'omics' analyses. It is now apparent that leaf senescence is a highly complex genetic program that is tightly controlled by multiple layers of regulation, including at the level of chromatin and transcription, as well as by post-transcriptional, translational and post-translational regulation. This Commentary discusses the latest understandings and insights into the underlying molecular mechanisms, and presents the perspectives necessary to enable our system-level understanding of leaf senescence, together with their possible implications for aging in general.
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TL;DR: This review describes recent progress in deciphering the mechanisms controlling ion homeostasis, cell activity responses, and epigenetic regulation in plants under salt stress and highlights research areas that require further research to reveal new determinants of salt tolerance in plants.
Abstract: Contents Summary 523 I. Introduction 523 II. Sensing salt stress 524 III. Ion homeostasis regulation 524 IV. Metabolite and cell activity responses to salt stress 527 V. Conclusions and perspectives 532 Acknowledgements 533 References 533 SUMMARY: Excess soluble salts in soil (saline soils) are harmful to most plants. Salt imposes osmotic, ionic, and secondary stresses on plants. Over the past two decades, many determinants of salt tolerance and their regulatory mechanisms have been identified and characterized using molecular genetics and genomics approaches. This review describes recent progress in deciphering the mechanisms controlling ion homeostasis, cell activity responses, and epigenetic regulation in plants under salt stress. Finally, we highlight research areas that require further research to reveal new determinants of salt tolerance in plants.
703 citations
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...Leaf senescence is crucial for plant fitness and is differentially modulated under different environmental conditions (Allu et al., 2014), which affects the facilitated recycling of nutrients to sink tissues and the duration of photosynthesis (Wu et al., 2012; Liang et al., 2014)....
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TL;DR: The aim of this review is to summarize how PAs improve plants' productivity, and to provide a basis for future research on the mechanism of action of PAs in plant growth and development.
Abstract: Polyamines (PAs) are low molecular weight aliphatic nitrogenous bases containing two or more amino groups. They are produced by organisms during metabolism and are present in almost all cells. Because they play important roles in diverse plant growth and developmental processes and in environmental stress responses, they are considered as a new kind of plant biostimulant. With the development of molecular biotechnology techniques, there is increasing evidence that PAs, whether applied exogenously or produced endogenously via genetic engineering, can positively affect plant growth, productivity, and stress tolerance. However, it is still not fully understood how PAs regulate plant growth and stress responses. In this review, we attempt to cover these information gaps and provide a comprehensive and critical assessment of the published literature on the relationships between PAs and plant flowering, embryo development, senescence, and responses to several (mainly abiotic) stresses. The aim of this review is to summarize how PAs improve plants' productivity, and to provide a basis for future research on the mechanism of action of PAs in plant growth and development. Future perspectives for PA research are also suggested.
442 citations
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...Polyamines appeared to delay senescence by inhibiting ethylene biosynthesis (Woo et al., 2013; Anwar et al., 2015)....
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TL;DR: This study identified and characterized a dominant premature leaf senescence mutant, prematurely senile 1 (ps1-D), and demonstrated that OsNAP is an ideal marker of naturalsenescence onset in rice and that it functions as an important link between ABA and leafSenescence in rice.
Abstract: It has long been established that premature leaf senescence negatively impacts the yield stability of rice, but the underlying molecular mechanism driving this relationship remains largely unknown. Here, we identified a dominant premature leaf senescence mutant, prematurely senile 1 (ps1-D). PS1 encodes a plant-specific NAC (no apical meristem, Arabidopsis ATAF1/2, and cup-shaped cotyledon2) transcriptional activator, Oryza sativa NAC-like, activated by apetala3/pistillata (OsNAP). Overexpression of OsNAP significantly promoted senescence, whereas knockdown of OsNAP produced a marked delay of senescence, confirming the role of this gene in the development of rice senescence. OsNAP expression was tightly linked with the onset of leaf senescence in an age-dependent manner. Similarly, ChIP-PCR and yeast one-hybrid assays demonstrated that OsNAP positively regulates leaf senescence by directly targeting genes related to chlorophyll degradation and nutrient transport and other genes associated with senescence, suggesting that OsNAP is an ideal marker of senescence onset in rice. Further analysis determined that OsNAP is induced specifically by abscisic acid (ABA), whereas its expression is repressed in both aba1 and aba2, two ABA biosynthetic mutants. Moreover, ABA content is reduced significantly in ps1-D mutants, indicating a feedback repression of OsNAP on ABA biosynthesis. Our data suggest that OsNAP serves as an important link between ABA and leaf senescence. Additionally, reduced OsNAP expression leads to delayed leaf senescence and an extended grain-filling period, resulting in a 6.3% and 10.3% increase in the grain yield of two independent representative RNAi lines, respectively. Thus, fine-tuning OsNAP expression should be a useful strategy for improving rice yield in the future.
401 citations
Cites background from "Plant leaf senescence and death - r..."
...Thus, senescence is not a passive process but rather is a developmentally programmed procedure that has a strong adaptive advantage (7, 8)....
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TL;DR: It is demonstrated that melatonin acts as a potent agent to delay leaf senescence and cell death in rice and enhances abiotic stress tolerance via directly or indirectly counteracting the cellular accumulation of H2O2.
Abstract: Melatonin, an antioxidant in both animals and plants, has been reported to have beneficial effects on the aging process. It was also suggested to play a role in extending longevity and enhancing abiotic stress resistance in plant. In this study, we demonstrate that melatonin acts as a potent agent to delay leaf senescence and cell death in rice. Treatments with melatonin significantly reduced chlorophyll degradation, suppressed the transcripts of senescence-associated genes, delayed the leaf senescence, and enhanced salt stress tolerance. Genome-wide expression profiling by RNA sequencing reveals that melatonin is a potent free radical scavenger, and its exogenous application results in enhanced antioxidant protection. Leaf cell death in noe1, a mutant with over-produced H2O2, can be relieved by exogenous application of melatonin. These data demonstrate that melatonin delays the leaf senescence and cell death and also enhances abiotic stress tolerance via directly or indirectly counteracting the cellular accumulation of H2O2.
233 citations
TL;DR: A rice NAC transcription factor, OsNAC2, that participates in ABA-induced leaf senescence and elucidates the transcriptional network of ABA production during leaf senesence in rice is demonstrated.
Abstract: It is well known that abscisic acid (ABA)-induced leaf senescence and premature leaf senescence negatively affect the yield of rice (Oryza sativa). However, the molecular mechanism underlying this relationship, especially the upstream transcriptional network that modulates ABA level during leaf senescence, remains largely unknown. Here, we demonstrate a rice NAC transcription factor, OsNAC2, that participates in ABA-induced leaf senescence. Overexpression of OsNAC2 dramatically accelerated leaf senescence, whereas its knockdown lines showed a delay in leaf senescence. Chromatin immunoprecipitation-quantitative PCR, dual-luciferase, and yeast one-hybrid assays demonstrated that OsNAC2 directly activates expression of chlorophyll degradation genes, OsSGR and OsNYC3. Moreover, ectopic expression of OsNAC2 leads to an increase in ABA levels via directly up-regulating expression of ABA biosynthetic genes (OsNCED3 and OsZEP1) as well as down-regulating the ABA catabolic gene (OsABA8ox1). Interestingly, OsNAC2 is upregulated by a lower level of ABA but downregulated by a higher level of ABA, indicating a feedback repression of OsNAC2 by ABA. Additionally, reduced OsNAC2 expression leads to about 10% increase in the grain yield of RNAi lines. The novel ABA-NAC-SAGs regulatory module might provide a new insight into the molecular action of ABA to enhance leaf senescence and elucidates the transcriptional network of ABA production during leaf senescence in rice.
230 citations
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...Although senescence is an active process to salvage nutrients from old tissues, precocious senescence will shorten the growth stage of crops and be unfavorable to agronomic production (Woo et al., 2013)....
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References
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TL;DR: The structure, assembly, and function of the posttranslational modification with ubiquitin, a process referred to as ubiquitylation, controls almost every process in cells.
Abstract: The posttranslational modification with ubiquitin, a process referred to as ubiquitylation, controls almost every process in cells. Ubiquitin can be attached to substrate proteins as a single moiety or in the form of polymeric chains in which successive ubiquitin molecules are connected through specific isopeptide bonds. Reminiscent of a code, the various ubiquitin modifications adopt distinct conformations and lead to different outcomes in cells. Here, we discuss the structure, assembly, and function of this ubiquitin code.
2,762 citations
"Plant leaf senescence and death - r..." refers background in this paper
...Ubiquitin-mediated post-translational modification is being recognized as a key regulatory step in diverse physiological processes, including cell cycle progression, environmental stress responses and hormone signaling (Komander and Rape, 2012)....
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TL;DR: Evidence is presented that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigOLactone application restores the wild-type branching phenotype to ccd8 mutants, and that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack striglactone response.
Abstract: A carotenoid-derived hormonal signal that inhibits shoot branching in plants has long escaped identification. Strigolactones are compounds thought to be derived from carotenoids and are known to trigger the germination of parasitic plant seeds and stimulate symbiotic fungi. Here we present evidence that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigolactone application restores the wild-type branching phenotype to ccd8 mutants. Moreover, we show that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack strigolactone response, and are not deficient in strigolactones. These responses are conserved in Arabidopsis. In agreement with the expected properties of the hormonal signal, exogenous strigolactone can be transported in shoots and act at low concentrations. We suggest that endogenous strigolactones or related compounds inhibit shoot branching in plants. Furthermore, ccd8 mutants demonstrate the diverse effects of strigolactones in shoot branching, mycorrhizal symbiosis and parasitic weed interaction.
1,873 citations
"Plant leaf senescence and death - r..." refers background in this paper
...…work showed that ORE9, also referred to as MORE AXILLARY GROWTH 2 (MAX2), is also involved in photomorphogenesis (Shen et al., 2007), branching (Stirnberg et al., 2002), as well as signaling by strigolactone (Gomez-Roldan et al., 2008; Umehara et al., 2008) and karrikin (Nelson et al., 2011)....
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TL;DR: It is proposed that strigolactones act as a new hormone class—or their biosynthetic precursors—in regulating above-ground plant architecture, and also have a function in underground communication with other neighbouring organisms.
Abstract: Shoot branching is a major determinant of plant architecture and is highly regulated by endogenous and environmental cues. Two classes of hormones, auxin and cytokinin, have long been known to have an important involvement in controlling shoot branching. Previous studies using a series of mutants with enhanced shoot branching suggested the existence of a third class of hormone(s) that is derived from carotenoids, but its chemical identity has been unknown. Here we show that levels of strigolactones, a group of terpenoid lactones, are significantly reduced in some of the branching mutants. Furthermore, application of strigolactones inhibits shoot branching in these mutants. Strigolactones were previously found in root exudates acting as communication chemicals with parasitic weeds and symbiotic arbuscular mycorrhizal fungi. Thus, we propose that strigolactones act as a new hormone class-or their biosynthetic precursors-in regulating above-ground plant architecture, and also have a function in underground communication with other neighbouring organisms.
1,742 citations
"Plant leaf senescence and death - r..." refers background in this paper
..., 2002), as well as signaling by strigolactone (Gomez-Roldan et al., 2008; Umehara et al., 2008) and karrikin (Nelson et al....
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...…work showed that ORE9, also referred to as MORE AXILLARY GROWTH 2 (MAX2), is also involved in photomorphogenesis (Shen et al., 2007), branching (Stirnberg et al., 2002), as well as signaling by strigolactone (Gomez-Roldan et al., 2008; Umehara et al., 2008) and karrikin (Nelson et al., 2011)....
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TL;DR: The positional cloning of Gpc-B1, a wheat quantitative trait locus associated with increased grain protein, zinc, and iron content, is reported here, and reduction in RNA levels of the multiple NAM homologs by RNA interference delayed senescence by more than 3 weeks and reduced wheat grain protein and zinc content.
Abstract: Enhancing the nutritional value of food crops is a means of improving human nutrition and health. We report here the positional cloning of Gpc-B1, a wheat quantitative trait locus associated with increased grain protein, zinc, and iron content. The ancestral wild wheat allele encodes a NAC transcription factor (NAM-B1) that accelerates senescence and increases nutrient remobilization from leaves to developing grains, whereas modern wheat varieties carry a nonfunctional NAM-B1 allele. Reduction in RNA levels of the multiple NAM homologs by RNA interference delayed senescence by more than 3 weeks and reduced wheat grain protein, zinc, and iron content by more than 30%.
1,377 citations
"Plant leaf senescence and death - r..." refers background in this paper
...dicoccoides), promotes senescence and facilitates nutrient remobilization from leaves to grains, thereby improving the protein, zinc, and iron content of the grain (Uauy et al., 2006; Waters et al., 2009)....
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...NAM-B1, an NAC transcription factor in ancestral wild wheat (Triticum turgidum L. ssp. dicoccoides), promotes senescence and facilitates nutrient remobilization from leaves to grains, thereby improving the protein, zinc, and iron content of the grain (Uauy et al., 2006; Waters et al., 2009)....
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TL;DR: Future studies will no doubt continue to identify the functional and biochemical properties of new chromatin domains as well as to elucidate the principles that govern their maintenance and propagation.
1,259 citations
"Plant leaf senescence and death - r..." refers background in this paper
...Chromatin structure is modified by the binding of histones to DNA and histone posttranslational modifications, including acetylation, methylation and phosphorylation, as well as by DNA methylation, which affects the ability of proteins to bind to the chromatin (Peterson and Laniel, 2004)....
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