Know when and how to die: gaining insights into the molecular regulation of leaf senescence

Abstract

Senescence is the ultimate phase in the life cycle of leaves which is crucial for recycling of nutrients to maintain plant fitness and reproductive success. The earliest visible manifestation of leaf senescence is their yellowing, which usually commences with the breakdown of chlorophyll. The degradation process involves a gradual and highly coordinated disassembly of macromolecules resulting in the accumulation of nutrients, which are subsequently mobilized from the senescing leaves to the developing organs. Leaf senescence progresses under overly tight genetic and molecular control involving a well-orchestrated and intricate network of regulators that coordinate spatio-temporally with the influence of both internal and external cues. Owing to the advancements in omics technologies, the availability of mutant resources, scalability of molecular analyses methodologies and the advanced capacity to integrate multidimensional data, our understanding of the genetic and molecular basis of leaf ageing has greatly expanded. The review provides a compilation of the multitier regulation of senescence process and the interrelation between the environment and the terminal phase of leaf development. The knowledge gained would benefit in devising the strategies for manipulation of leaf senescence process to improve crop quality and productivity.

Keywords: Crop productivity; Omics technologies; Regulation; Senescence.

Fig. 1

Leaf senescence paradigm. Leaf senescence is primarily governed by developmental age; however, leaf senescence onset and progression are also regulated by various internal and external stimuli (A). These stimuli engage different signaling pathways, activating transcription factors that control leaf senescence. The senescence process is associated with the down-regulation of SDGs, including photosynthesis-related and metabolic process-related genes. In addition, enhanced expression levels of SAGs (hydrolytic enzymes, TFs, transporters, etc.) are also reported during leaf senescence. The leaf senescence can be divided into three phases: initiation, degenerative and terminal (B). The initiation phase includes the sink/source transition and the decline in photosynthesis. The second stage, the degenerative phase is the degradation phase, where macromolecules and cell organelles undergo degradation. And the ultimate terminal phase involves cell death

Fig. 2

An overview of multi-tiered natural leaf senescence regulatory network. The signalling pathways of phytohormones JA, ethylene, ABA, SA, and GA initiate and promote leaf senescence in leaves. By binding to the promoters of important chlorophyll (Chl) catabolic genes (NYE1, NYC1 and PAO), MYC proteins regulate JA-induced Chl degradation downstream of JAZs in the JA signalling pathway. Moreover, MYCs indirectly regulate Chl degradation through the transcription factors ANAC019/055/072, which can trigger the activation production of the same Chl catabolic genes (CCGs). AtNAP positively regulates leaf senescence by promoting ABA production and SAG113 expression. ATAF1 contributes to ABA-induced senescence by activating the expression of genes involved in ABA biosynthesis and transport (NCED3 and ABCG40). ATAF1 enhances and suppresses the expression of ORE1 and GLK1, respectively, by directly binding to their promoter region. As a result, the expression of GLK target genes is hindered, resulting in an age-dependent drop in the expression of GLKs, whilst the expression of ORE1 target genes is increased, triggering senescence. ABA-induced senescence is mediated by the action of ABFs downstream of ABA signaling modules. EIN3, which is activated by EIN2, represses miR164 transcription by binding directly to the its promoter region which results in elevation of ORE1 transcript levels, thereby promoting leaf senescence as ORE1 activates the transcription of SAG29, SINA1 and SWEET15 and represses the expression of GLKs. PRR9 activates ORE1 and suppresses miR164 indirectly during leaf senescence. PIFs, whose expression is inhibited by ELF3, promote chloroplast deterioration by suppressing GLKs. Age and GA-induced WRKY45 promotes the expression of a number of SAGs. WRKY75 is involved in a tripartite amplification loop where it promotes SA synthesizing gene SID2. JA-induced TF, TCP4, positively regulates leaf senescence by enhancing the expression of LOX2. Whereas bHLHs, negatively regulate leaf senescence by repressing SAG29 expression. Leaf senescence is also regulated at epigenetic level. Expression of WRKY53 is partially mediated by methylation of histones via SUVH2. WRKY53, in turn along with PWR and HDA9, removes the acetylation marks from the histones of WRKY57 thereby leading to its suppression which influences the antagonistic regulation of leaf senescence by auxin and JA. Expression of WRKY57 protein level is positively mediated by auxin, whereas JA represses its expression at transcript level. The age-induced Ca²⁺ levels promote leaf senescence by activating the Ca-dependent protein kinase (CPK1), which in turn phosphorylates and activates the master regulator of senescence, ORE. The blue boxes represent the cytoplasmic/nuclear regulatory component of senescence; green boxes represent chloroplastic regulatory components; red boxes represent phytohormones associated with senescence. LOX: Lipoxygenase; IAA: INDOLE-3-ACETIC ACID INDUCIBLE; JAZ: JASMONATE ZIM-DOMAIN protein; ANAC: Arabidopsis NAC transcription factor; PIF: Phytochrome interacting factor; ACS: 1-aminocyclopropane-1-carboxylate synthase; EIN: Ethylene insensitive; ORE: Oresara; CPK: calcium dependent protein kinase; GLK: Golden2-like transcription factor; ATAF: Arabidopsis thaliana ACTIVATING FACTOR; ABCG40: ARABIDOPSIS THALIANA ATP-BINDING CASSETTE G40; NCED: 9-cis-epoxycarotenoid dioxygenase; ABA: Abscisic acid; AAO: Arabidopsis aldehyde oxidase; ABI: ABSCISIC ACID INSENSITIVE; PRR: PSEUDO-RESPONSE REGULATOR; ELF: early-flowering; PYL: pyrabactin resistance-like; ABF: ABRE-binding factors; NYC: NON-YELLOW COLORING; SGR: STAY GREEN; PPH: PHEOPHYTINASE; PAO: pheide a oxygenase; SOC: SUPPRESSOR OF OVEREXPRESSION OF CO; SAG: Senescence-associated gene: PCY: Plastocyanin; SUVH: SU(VAR)3–9 homolog; HDA: histone deacetylase; GID: GA INSENSITIVE DWARF; SID: SALICYLIC ACID INDUCTION DEFICIENT; ESP: Epithiospecifier protein; ERF: Ethylene-responsive element binding factors; JA: Jasmonic acid; GA: Gibberellic acid; SA: Salicylic acid