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The roles of ethylene and transcription factors in the regulation of onset of leaf senescence.

ABSTRACT: Leaf senescence is the last stage of leaf development and is accompanied by cell death. In contrast to senescence in individual organisms that leads to death, leaf senescence is associated with dynamic processes that include the translocation of nutrients from old leaves to newly developing or storage tissues within the same plant. The onset of leaf senescence is largely regulated by age and internal and external stimuli, which include the plant hormone ethylene. Earlier studies have documented the important role of ethylene in the regulation of leaf senescence. The production of ethylene coincides with the onset of leaf senescence, whereas the application of ethylene to plants induces precocious leaf senescence. Recently, many studies have described the components of ethylene signaling and biosynthetic pathways that are involved in modulating the onset of leaf senescence. Particularly, transcription factors (TFs) integrate ethylene signals with those from environmental and developmental factors to accelerate or delay leaf senescence. This review aims to discuss the regulatory cascade involving ethylene and TFs in the regulation of onset of leaf senescence.

SUBMITTER: Koyama T

PROVIDER: S-EPMC4243489 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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The roles of ethylene and transcription factors in the regulation of onset of leaf senescence.

Koyama Tomotsugu T

Frontiers in plant science 20141125

Leaf senescence is the last stage of leaf development and is accompanied by cell death. In contrast to senescence in individual organisms that leads to death, leaf senescence is associated with dynamic processes that include the translocation of nutrients from old leaves to newly developing or storage tissues within the same plant. The onset of leaf senescence is largely regulated by age and internal and external stimuli, which include the plant hormone ethylene. Earlier studies have documented ...[more]

PMID: 25505475

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Project description:BackgroundThe phytohormone ethylene controls many processes in plant development and acts as a key signaling molecule in response to biotic and abiotic stresses: it is rapidly induced by flooding, wounding, drought, and pathogen attack as well as during abscission and fruit ripening. In kiwifruit (Actinidia spp.), fruit ripening is characterized by two distinct phases: an early phase of system-1 ethylene biosynthesis characterized by absence of autocatalytic ethylene, followed by a late burst of autocatalytic (system-2) ethylene accompanied by aroma production and further ripening. Progress has been made in understanding the transcriptional regulation of kiwifruit fruit ripening but the regulation of system-1 ethylene biosynthesis remains largely unknown. The aim of this work is to better understand the transcriptional regulation of both systems of ethylene biosynthesis in contrasting kiwifruit organs: fruit and leaves.ResultsA detailed molecular study in kiwifruit (A. chinensis) revealed that ethylene biosynthesis was regulated differently between leaf and fruit after mechanical wounding. In fruit, wound ethylene biosynthesis was accompanied by transcriptional increases in 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS), ACC oxidase (ACO) and members of the NAC class of transcription factors (TFs). However, in kiwifruit leaves, wound-specific transcriptional increases were largely absent, despite a more rapid induction of ethylene production compared to fruit, suggesting that post-transcriptional control mechanisms in kiwifruit leaves are more important. One ACS member, AcACS1, appears to fulfil a dominant double role; controlling both fruit wound (system-1) and autocatalytic ripening (system-2) ethylene biosynthesis. In kiwifruit, transcriptional regulation of both system-1 and -2 ethylene in fruit appears to be controlled by temporal up-regulation of four NAC (NAM, ATAF1/2, CUC2) TFs (AcNAC1-4) that induce AcACS1 expression by directly binding to the AcACS1 promoter as shown using gel-shift (EMSA) and by activation of the AcACS1 promoter in planta as shown by gene activation assays combined with promoter deletion analysis.ConclusionsOur results indicate that in kiwifruit the NAC TFs AcNAC2-4 regulate both system-1 and -2 ethylene biosynthesis in fruit during wounding and ripening through control of AcACS1 expression levels but not in leaves where post-transcriptional/translational regulatory mechanisms may prevail.

Project description:Leaf senescence is the final stage of leaf development and an important step that relocates nutrients for grain filling in cereal crops. Senescence occurs in an age-dependent manner and under unfavorable environmental conditions such as deep shade, water deficit, and high salinity stresses. Although many transcription factors that modulate leaf senescence have been identified, the mechanisms that regulate leaf senescence in response to environmental conditions remain elusive. Here, we show that rice (Oryza sativa) ETHYLENE RESPONSE FACTOR 101 (OsERF101) promotes the onset and progression of leaf senescence. OsERF101 encodes a predicted transcription factor and OsERF101 transcript levels rapidly increased in rice leaves during dark-induced senescence (DIS), indicating that OsERF101 is a senescence-associated transcription factor. Compared with wild type, the oserf101 T-DNA knockout mutant showed delayed leaf yellowing and higher chlorophyll contents during DIS and natural senescence. Consistent with its delayed-yellowing phenotype, the oserf101 mutant exhibited downregulation of genes involved in chlorophyll degradation, including rice NAM, ATAF1/2, and CUC2 (OsNAP), STAY-GREEN (SGR), NON-YELLOW COLORING 1 (NYC1), and NYC3 during DIS. After methyl jasmonate treatment to induce rapid leaf de-greening, the oserf101 leaves retained more chlorophyll compared with wild type, indicating that OsERF101 is involved in promoting jasmonic acid (JA)-induced leaf senescence. Consistent with the involvement of JA, the expression of the JA signaling genes OsMYC2/JA INSENSITIVE 1 (OsJAI1) and CORONATINE INSENSITIVE 1a (OsCOI1a), was downregulated in the oserf101 leaves during DIS. Transient transactivation and chromatin immunoprecipitation assays revealed that OsERF101 directly binds to the promoter regions of OsNAP and OsMYC2, which activate genes involved in chlorophyll degradation and JA signaling-mediated leaf senescence. These results demonstrate that OsERF101 promotes the onset and progression of leaf senescence through a JA-mediated signaling pathway.

Dataset Information

The roles of ethylene and transcription factors in the regulation of onset of leaf senescence.

Publications

The roles of ethylene and transcription factors in the regulation of onset of leaf senescence.

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