Epigenetic control of plant senescence and linked processes
TL;DR: The review outlines the concept of epigenetic control of interconnected regulatory pathways steering stress responses and plant development and summarizes recent findings on global alterations in chromatin structure, histone and DNA modifications, and ATP-dependent chromatin remodelling during plant senescence and linked processes.
Abstract: Senescence processes are part of the plant developmental programme. They involve reprogramming of gene expression and are under the control of a complex regulatory network closely linked to other developmental and stressresponsive pathways. Recent evidence indicates that leaf senescence is regulated via epigenetic mechanisms. In the present review, the epigenetic control of plant senescence is discussed in the broader context of environmentsensitive plant development. The review outlines the concept of epigenetic control of interconnected regulatory pathways steering stress responses and plant development. Besides giving an overview of techniques used in the field, it summarizes recent findings on global alterations in chromatin structure, histone and DNA modifications, and ATPdependent chromatin remodelling during plant senescence and linked processes.
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TL;DR: The present knowledge on chromatin-based mechanisms potentially involved in the somatic-to-embryogenic developmental transition is summarized, emphasizing the potential role of the chromatin to integrate stress, hormonal, and developmental pathways leading to the activation of the embryogenic program.
352 citations
Cites background from "Epigenetic control of plant senesce..."
...The role of histone acetylation in plant senescence and stress adaptation has recently been reviewed [228]....
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Journal Article•
TL;DR: In this article, AtHD1 expression and deacetylation profiles were associated with various developmental abnormalities, including early senescence, ectopic expression of silenced genes, suppression of apical dominance, homeotic changes, heterochronic shift toward juvenility, flower defects, and male and female sterility.
Abstract: Histone acetylation and deacetylation play essential roles in eukaryotic gene regulation. Reversible modifications of core histones are catalyzed by two intrinsic enzymes, histone acetyltransferase and histone deacetylase (HD). In general, histone deacetylation is related to transcriptional gene silencing, whereas acetylation correlates with gene activation. We produced transgenic plants expressing the antisense Arabidopsis HD (AtHD1) gene. AtHD1 is a homolog of human HD1 and RPD3 global transcriptional regulator in yeast. Expression of the antisense AtHD1 caused dramatic reduction in endogenous AtHD1 transcription, resulting in accumulation of acetylated histones, notably tetraacetylated H4. Reduction in AtHD1 expression and AtHD1 production and changes in acetylation profiles were associated with various developmental abnormalities, including early senescence, ectopic expression of silenced genes, suppression of apical dominance, homeotic changes, heterochronic shift toward juvenility, flower defects, and male and female sterility. Some of the phenotypes could be attributed to ectopic expression of tissue-specific genes (e.g., SUPERMAN) in vegetative tissues. No changes in genomic DNA methylation were detected in the transgenic plants. These results suggest that AtHD1 is a global regulator, which controls gene expression during development through DNA-sequence independent or epigenetic mechanisms in plants. In addition to DNA methylation, histone modifications may be involved in a general regulatory mechanism responsible for plant plasticity and variation in nature.
247 citations
TL;DR: This review highlights some of the most recent findings on nuclear reorganization, histone variants, hist one chaperones, DNA- and histone modifications, and somatic and meiotic heritability in connection with stress.
135 citations
TL;DR: This review addresses the need for the integration of multi-omics techniques and physiological phenotyping into holistic phenomics approaches to dissect the complex phenomenon of senescence and to elucidate the underlying molecular processes.
Abstract: The study of senescence in plants is complicated by diverse levels of temporal and spatial dynamics as well as the impact of external biotic and abiotic factors and crop plant management. Whereas the molecular mechanisms involved in developmentally regulated leaf senescence are very well understood, in particular in the annual model plant species Arabidopsis, senescence of other organs such as the flower, fruit, and root is much less studied as well as senescence in perennials such as trees. This review addresses the need for the integration of multi-omics techniques and physiological phenotyping into holistic phenomics approaches to dissect the complex phenomenon of senescence. That became feasible through major advances in the establishment of various, complementary 'omics' technologies. Such an interdisciplinary approach will also need to consider knowledge from the animal field, in particular in relation to novel regulators such as small, non-coding RNAs, epigenetic control and telomere length. Such a characterization of phenotypes via the acquisition of high-dimensional datasets within a systems biology approach will allow us to systematically characterize the various programmes governing senescence beyond leaf senescence in Arabidopsis and to elucidate the underlying molecular processes. Such a multi-omics approach is expected to also spur the application of results from model plants to agriculture and their verification for sustainable and environmentally friendly improvement of crop plant stress resilience and productivity and contribute to improvements based on postharvest physiology for the food industry and the benefit of its customers.
88 citations
Cites background from "Epigenetic control of plant senesce..."
...…the analysis of regulation of senescence in plants by non-coding RNAs and epigenetic mechanisms very much lags behind understanding in animals (Ay et al., 2014a) and the link between telomere length and senescence is not yet clearly established, although an increasing number of studies with…...
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...Transcriptomics will need to be complemented also by consideration of epigenetics and small RNA regulatory mechanisms (Humbeck, 2013; Ay et al., 2014a)....
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...It has been proposed that the epigenetic regulation of senescence in plants should be considered within the broader context of environmental sensitivity of development due to their sessile lifestyle (Ay et al., 2014a)....
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TL;DR: A universal nature of senescence is demonstrated, despite this process occurring in organs that have completely different functions, it is very similar; this will provide a powerful tool for plant physiology research.
Abstract: Senescence is the final stage of plant ontogeny before death. Senescence may occur naturally because of age or may be induced by various endogenous and exogenous factors. Despite its destructive character, senescence is a precisely controlled process that follows a well-defined order. It is often inseparable from programmed cell death (PCD), and a correlation between these processes has been confirmed during the senescence of leaves and petals. Despite suggestions that senescence and PCD are two separate processes, with PCD occurring after senescence, cell death responsible for senescence is accompanied by numerous changes at the cytological, physiological and molecular levels, similar to other types of PCD. Independent of the plant organ analysed, these changes are focused on initiating the processes of cellular structural degradation via fluctuations in phytohormone levels and the activation of specific genes. Cellular structural degradation is genetically programmed and dependent on autophagy. Phytohormones/plant regulators are heavily involved in regulating the senescence of plant organs and can either promote [ethylene, abscisic acid (ABA), jasmonic acid (JA), and polyamines (PAs)] or inhibit [cytokinins (CKs)] this process. Auxins and carbohydrates have been assigned a dual role in the regulation of senescence, and can both inhibit and stimulate the senescence process. In this review, we introduce the basic pathways that regulate senescence in plants and identify mechanisms involved in controlling senescence in ephemeral plant organs. Moreover, we demonstrate a universal nature of this process in different plant organs; despite this process occurring in organs that have completely different functions, it is very similar. Progress in this area is providing opportunities to revisit how, when and which way senescence is coordinated or decoupled by plant regulators in different organs and will provide a powerful tool for plant physiology research.
66 citations
Cites background from "Epigenetic control of plant senesce..."
...Many stimuli that induce senescence exist, such as shortened days in autumn, drought, frost, and shading as well as ageing, phytohormone levels, higher-order epigenetic mechanisms, and the expression of specific environment-dependent genes (Ay et al. 2014; Guo & Gan 2005)....
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...Genes that are up-regulated during the process are termed senescence-associated genes (SAGs), whereas genes that are down-regulated are defined as senescence downregulated genes (SDGs) (Noh & Amasino 1999; Simeonova & Mostowska 2001; Ay et al. 2014)....
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References
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TL;DR: WRKY70 has a pivotal role in determining the balance between SA-dependent and JA-dependent defense pathways in plant response to bacterial pathogens.
Abstract: Cross-talk between signal transduction pathways is a central feature of the tightly regulated plant defense signaling network. The potential synergism or antagonism between defense pathways is determined by recognition of the type of pathogen or pathogen-derived elicitor. Our studies have identified WRKY70 as a node of convergence for integrating salicylic acid (SA)- and jasmonic acid (JA)-mediated signaling events during plant response to bacterial pathogens. Here, we challenged transgenic plants altered in WRKY70 expression as well as WRKY70 knockout mutants of Arabidopsis with the fungal pathogens Alternaria brassicicola and Erysiphe cichoracearum to elucidate the role of WRKY70 in modulating the balance between distinct defense responses. Gain or loss of WRKY70 function causes opposite effects on JA-mediated resistance to A. brassicicola and the SA-mediated resistance to E. cichoracearum. While the up-regulation of WRKY70 caused enhanced resistance to E. cichoracearum, it compromised plant resistance to A. brassicicola. Conversely, down-regulation or insertional inactivation of WRKY70 impaired plant resistance to E. cichoracearum. Over-expression of WRKY70 resulted in the suppression of several JA responses including expression of a subset of JA- and A. brassicicola-responsive genes. We show that this WRKY70-controlled suppression of JA-signaling is partly executed by NPR1. The results indicate that WRKY70 has a pivotal role in determining the balance between SA-dependent and JA-dependent defense pathways.
453 citations
TL;DR: FISH plays an increasingly important role in a variety of research areas, including cytogenetics, prenatal diagnosis, tumor biology, gene amplification and gene mapping.
434 citations
TL;DR: In this article, the authors show that treatment with acibenzolar S-methyl or pathogen infection of distal leaves induce chromatin modifications on defence gene promoters that are normally found on active genes, although the genes remain inactive.
Abstract: Priming of defence genes for amplified response to secondary stress can be induced by application of the plant hormone salicylic acid or its synthetic analogue acibenzolar S-methyl. In this study, we show that treatment with acibenzolar S-methyl or pathogen infection of distal leaves induce chromatin modifications on defence gene promoters that are normally found on active genes, although the genes remain inactive. This is associated with an amplified gene response on challenge exposure to stress. Mutant analyses reveal a tight correlation between histone modification patterns and gene priming. The data suggest a histone memory for information storage in the plant stress response.
428 citations
TL;DR: Evidence is provided that HDA19 may regulate gene expression involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis, and green fluorescent protein fusion is demonstrated thatHDA19 accumulated in the nuclei ofArabidopsis cells.
Abstract: Histone acetylation is modulated through the action of histone acetyltransferases and deacetylases, which play key roles in the regulation of eukaryotic gene expression. Previously, we have identified a yeast histone deacetylase REDUCED POTASSIUM DEPENDENCY3 (RPD3) homolog, HISTONE DEACETYLASE19 (HDA19) (AtRPD3A), in Arabidopsis thaliana . Here, we report further study of the expression and function of HDA19 . Analysis of Arabidopsis plants containing the HDA19 :β-glucuronidase fusion gene revealed that HDA19 was expressed throughout the life of the plant and in most plant organs examined. In addition, the expression of HDA19 was induced by wounding, the pathogen Alternaria brassicicola , and the plant hormones jasmonic acid and ethylene. Using green fluorescent protein fusion, we demonstrated that HDA19 accumulated in the nuclei of Arabidopsis cells. Overexpression of HDA19 in 35S : HDA19 plants decreased histone acetylation levels, whereas downregulation of HDA19 in HDA19 -RNA interference (RNAi) plants increased histone acetylation levels. In comparison with wild-type plants, 35S : HDA19 transgenic plants had increased expression of ETHYLENE RESPONSE FACTOR1 and were more resistant to the pathogen A. brassicicola . The expression of jasmonic acid and ethylene regulated PATHOGENESIS-RELATED genes, Basic Chitinase and β -1,3-Glucanase , was upregulated in 35S : HDA19 plants but downregulated in HDA19- RNAi plants. Our studies provide evidence that HDA19 may regulate gene expression involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis.
400 citations
TL;DR: It is suggested that the spread of H3K27me3 contributes to the mitotic heritability of Pc‐G silencing, and that the loss of silencing caused by transposon insertions at plant Pc-G targets reflects impaired spreading.
Abstract: The plant Polycomb-group (Pc-G) protein CURLY LEAF (CLF) is required to repress targets such as AGAMOUS (AG) and SHOOTMERISTEMLESS (STM). Using chromatin immunoprecipitation, we identify AG and STM as direct targets for CLF and show that they carry a characteristic epigenetic signature of dispersed histone H3 lysine 27 trimethylation (H3K27me3) and localised H3K27me2 methylation. H3K27 methylation is present throughout leaf development and consistent with this, CLF is required persistently to silence AG. However, CLF is not itself an epigenetic mark as it is lost during mitosis. We suggest a model in which Pc-G proteins are recruited to localised regions of targets and then mediate dispersed H3K27me3. Analysis of transgenes carrying AG regulatory sequences confirms that H3K27me3 can spread to novel sequences in a CLF-dependent manner and further shows that H3K27me3 methylation is not sufficient for silencing of targets. We suggest that the spread of H3K27me3 contributes to the mitotic heritability of Pc-G silencing, and that the loss of silencing caused by transposon insertions at plant Pc-G targets reflects impaired spreading.
396 citations