Leaf senescence is a genetically controlled dismantling programme that enables plants to efficiently remobilise nutrients to new growing sinks. It involves substantial metabolic reprogramming whose timing is affected by developmental and environmental signals. Plant hormones have long been known to affect the timing of leaf senescence, but they also affect plant development and stress responses. It has therefore been difficult to tease apart how the different hormones regulate the onset and progression of leaf senescence, i.e., whether they directly affect leaf senescence or affect it indirectly by altering the developmental programme or by altering plants' response to stress. Here we review research on hormonal regulation of leaf senescence and propose that hormones affect senescence through differential responses to developmental and environmental signals. We suggest that leaf senescence strictly depends on developmental changes, after which senescence can be induced, depending on the type of hormonal and environmental cues.

Hormonal regulation of leaf senescence through integration of developmental and stress signals.

Leaf senescence, the last stage of leaf development, is a type of postmitotic senescence and is characterized by the functional transition from nutrient assimilation to nutrient remobilization which is essential for plants’ fitness. The initiation and progression of leaf senescence are regulated by a variety of internal and external factors such as age, phytohormones, and environmental stresses. Significant breakthroughs in dissecting the molecular mechanisms underpinning leaf senescence have benefited from the identification of senescence-altered mutants through forward genetic screening and functional assessment of hundreds of senescence-associated genes (SAGs) via reverse genetic research in model plant Arabidopsis thaliana as well as in crop plants. Leaf senescence involves highly complex genetic programs that are tightly tuned by multiple layers of regulation, including chromatin and transcription regulation, post-transcriptional, translational and post-translational regulation. Due to the significant impact of leaf senescence on photosynthesis, nutrient remobilization, stress responses, and productivity, much effort has been made in devising strategies based on known senescence regulatory mechanisms to manipulate the initiation and progression of leaf senescence, aiming for higher yield, better quality, or improved horticultural performance in crop plants. This review aims to provide an overview of leaf senescence and discuss recent advances in multi-dimensional regulation of leaf senescence from genetic and molecular network perspectives. We also put forward the key issues that need to be addressed, including the nature of leaf age, functional stay-green trait, coordination between different regulatory pathways, source-sink relationship and nutrient remobilization, as well as translational researches on leaf senescence.

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Leaf senescence: progression, regulation, and application

Chlorophyll degradation is an important part of leaf senescence, but the underlying regulatory mechanisms are largely unknown. Excised leaves of an Arabidopsis thaliana NAC-LIKE, ACTIVATED BY AP3/PI (NAP) transcription factor mutant (nap) exhibited lower transcript levels of known chlorophyll degradation genes, STAY-GREEN1 (SGR1), NON-YELLOW COLORING1 (NYC1), PHEOPHYTINASE (PPH), and PHEIDE a OXYGENASE (PaO), and higher chlorophyll retention than the wild type during dark-induced senescence. Transcriptome coexpression analysis revealed that abscisic acid (ABA) metabolism/signaling genes were disproportionately represented among those positively correlated with NAP expression. ABA levels were abnormally low in nap leaves during extended darkness. The ABA biosynthetic genes 9-CIS-EPOXYCAROTENOID DIOXYGENASE2, ABA DEFICIENT3, and ABSCISIC ALDEHYDE OXIDASE3 (AAO3) exhibited abnormally low transcript levels in dark-treated nap leaves. NAP transactivated the promoter of AAO3 in mesophyll cell protoplasts, and electrophoretic mobility shift assays showed that NAP can bind directly to a segment (−196 to −162 relative to the ATG start codon) of the AAO3 promoter. Exogenous application of ABA increased the transcript levels of SGR1, NYC1, PPH, and PaO and suppressed the stay-green phenotype of nap leaves during extended darkness. Overexpression of AAO3 in nap leaves also suppressed the stay-green phenotype under extended darkness. Collectively, the results show that NAP promotes chlorophyll degradation by enhancing transcription of AAO3, which leads to increased levels of the senescence-inducing hormone ABA.

/pdf/a-nap-aao3-regulatory-module-promotes-chlorophyll-20dfoojkrh.pdf

A NAP-AAO3 Regulatory Module Promotes Chlorophyll Degradation via ABA Biosynthesis in Arabidopsis Leaves

Heat stress is one of the devastating abiotic stresses that cause substantial crop loss around the world. The frequency and magnitude of heat stress are being intensifi ed due to global climate change. Heat stress induces excessive production of reactive oxygen species that cause damage to lipids, proteins, and nucleic acids in plants. Plants have evolved various sophisticated mechanisms to sense heat stimuli and activate different defense responses rapidly to protect its vital cellular structures from heat-induced damage. Phytohormones are the endogenous messenger molecules that precisely mediate plant growth, development, and responses to various biotic and abiotic stresses including heat stress. With the advancement of molecular technologies, several hormones that were previously known only for their roles in plant growth and development have also been implicated in the heat stress response. To date, all major hormones such as abscisic acid, auxin, gibberellins, cytokinins, salicylic acid, jasmonic acid, ethylene, and brassinosteroids have been reported to play critical roles in response of plants to heat stress. In this chapter, we intend to review how various phytohormones are involved in plant adaptation to heat stress. Furthermore, we discuss the potential role of important plant hormones in the enhancement of heat tolerance. Hormone cross talk that mediates the response of plants to heat stress is also discussed. G. J. Ahammed (*) • J. Zhou Department of Horticulture , Zhejiang University , Zijingang Campus, Yuhangtang Road 866 , Hangzhou 310058 , People’s Republic of China e-mail: ahammed@zju.edu.cn X. Li Tea Research Institute , Chinese Academy of Agricultural Sciences , 9 Meiling Road , Hangzhou 310008 , People’s Republic of China Y.-H. Zhou • J.-Q. Yu Department of Horticulture , Zhejiang University , Zijingang Campus, Yuhangtang Road 866 , Hangzhou 310058 , People’s Republic of China Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology , Yuhangtang Road 866 , Hangzhou 310058 , People’s Republic of China

Plant Hormones under Challenging Environmental Factors

Plant leaves offer an exclusive windowpane to uncover the changes in organs, tissues, and cells as they advance towards the process of senescence and death. Drought-induced leaf senescence is an intricate process with remarkably coordinated phases of onset, progression, and completion implicated in an extensive reprogramming of gene expression. Advancing leaf senescence remobilizes nutrients to younger leaves thereby contributing to plant fitness. However, numerous mysteries remain unraveled concerning leaf senescence. We are not still able to correlate leaf senescence and drought stress to endogenous and exogenous environments. Furthermore, we need to decipher how molecular mechanisms of the leaf senescence and levels of drought tolerance are advanced and how is the involvement of SAGs in drought tolerance and plant fitness. This review provides the perspicacity indispensable for facilitating our coordinated point of view pertaining to leaf senescence together with inferences on progression of whole plant aging. The main segments discussed in the review include coordination between hormonal signaling, leaf senescence, drought tolerance, and crosstalk between hormones in leaf senescence regulation.

Roles of potential plant hormones and transcription factors in controlling leaf senescence and drought tolerance

Senescence of aerial parts is impeded by exogenous gibberellic acid in herbaceous perennial Paris polyphylla.

Chlorophyll (Chl) degradation was found to be related to the endogenous gibberellin (GA) content in shoots during senescence in the perennial plant Paris polyphylla var. yunnanensis (Franch.). Treatment with gibberellic acid (GA3) significantly increased the content of endogenous GAs (GA4 + GA7), retarded the senescence of shoots, and the degradation of proteins and Chl. Chlorophyllase, Mg-dechelation and peroxidase activities increased more in control plants than in those treated with GA3. GA3 treatment also protected lipoxygenase activity, which decreased significantly in control plants.

Gibberellin retards chlorophyll degradation during senescence of Paris polyphylla

Paris polyphylla Smith var. yunnanensis (Franch.) Hand.-Mazz. is a rhizomatous, herbaceous, perennial plant that is used as a medicinal plant with a variety of pharmacological activities. However, the functions of the green, leafy sepal of this plant are poorly understood. The main objectives of this study were to: (a) test the hypothesis that sepals make measurable contributions to fruit development and rhizome growth; and (b) investigate the allocation and partitioning of photosynthates produced by sepals and leaves to fruit and rhizome. Net photosynthetic rate, photosynthetic pigment composition and δ13C values were similar for sepals and leaves. Sepal-darkening and sepal-removal treatments resulted in smaller fruit size and decreased rhizome biomass, whereas fruit removal led to a decrease in calyx size and an increase in rhizome yield and saponin content. Fruit and seed mass were positively and linearly related to calyx size. These results indicate that photosynthates produced by sepals are involved in the fruit growth and seed development and that developing fruit and rhizomes compete for the photosynthates exported by leaves. We propose that the sepals of P. polyphylla function partly as leaves to compensate for reproductive costs. Fruit removal increased carbon partitioning to the rhizome and improved rhizome yield and quality, offering a useful strategy for the domestication of this valuable medicinal plant.

Function of leafy sepals in Paris polyphylla: photosynthate allocation and partitioning to the fruit and rhizome.

Senescence in perennials has not been extensively studied compared to that in annual plants, and the effects of delaying senescence on plant biomass and metabolic features in herbaceous perennials has also been poorly reported. We recently examined the effects of gibberellin A3 (GA3) on senescence of aerial parts of Paris polyphylla, which characterize the metabolic changes associated with senescence, and found antagonistic effects of GA and abscisic acid during this process. Rhizome yield and quality (saponin content) of Paris polyphylla were both improved by GA3-induced retardation of senescence. We propose that GA3-induced retardation of senescence increases green leaf area and prolongs the duration of photosynthesis, leading to increased rhizome yield. The increased saponin accumulation in GA3-treated plants may be explained by the longer growth phase and ensuing increased environmental stress.

Improving rhizome yield and quality of Paris polyphylla through gibberellic acid-induced retardation of senescence of aerial parts.

Nitrogen remobilization during senescence has been studied in perennial herb Paris polyphylla. We analyzed changes in N content, amino acids, N-remobilization enzymes and effects of gibberellic acid (GA) during natural senescence. There was a gradual decrease in the contents of N, chlorophyll and soluble proteins and activities of glutamine synthetase (GS; EC 6.3.1.2) and glutamate dehydrogenase (GLDH; EC 1.4.1.2). Activity staining and Western blots showed that GS2 activity decreased, whereas GS1 activity was relatively stable over time. In contrast, the C/N ratio and total amino acid content increased. Among individual amino acids, the proportions of glutamine (Gln) and asparagine (Asn) increased, and proportions of arginine, aspartate and glycine decreased. Treatment with GA slowed the senescence and retarded decreases in the activities of GS and GLDH and the contents of N, chlorophyll and soluble proteins. Conversely, this treatment slowed increases in the C/N ratio, total free amino acid content, and proportions of Gln and Asn. We conclude that low N resorption efficiency during senescence of P. polyphylla results from a sharp decrease in N remobilization enzyme activity.

Nitrogen remobilization in shoots of Paris polyphylla is altered by gibberellic acid application during senescence

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