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: It is demonstrated that DRM activity is required for the initial establishment of RdDM in all sequence contexts including CpG, CpNpG and asymmetric sites, and that DRM and CMT3 act redundantly to maintain non-CpG methylation.
499 citations
TL;DR: A robust ChIP protocol and strategy to optimize the protocol for any type of tissue is provided and it is argued that quantitative real-time PCR (QPCR) is the best method to analyze the precipitates, and comprehensive insights into data normalization are presented.
Abstract: Chromatin remodeling, histone modifications and other chromatin-related processes play a crucial role in gene regulation. A very useful technique to study these processes is chromatin immunoprecipitation (ChIP). ChIP is widely used for a few model systems, including Arabidopsis, but establishment of the technique for other organisms is still remarkably challenging. Furthermore, quantitative analysis of the precipitated material and normalization of the data is often underestimated, negatively affecting data quality. We developed a robust ChIP protocol, using maize (Zea mays) as a model system, and present a general strategy to systematically optimize this protocol for any type of tissue. We propose endogenous controls for active and for repressed chromatin, and discuss various other controls that are essential for successful ChIP experiments. We experienced that the use of quantitative PCR (QPCR) is crucial for obtaining high quality ChIP data and we explain why. The method of data normalization has a major impact on the quality of ChIP analyses. Therefore, we analyzed different normalization strategies, resulting in a thorough discussion of the advantages and drawbacks of the various approaches. Here we provide a robust ChIP protocol and strategy to optimize the protocol for any type of tissue; we argue that quantitative real-time PCR (QPCR) is the best method to analyze the precipitates, and present comprehensive insights into data normalization.
493 citations
TL;DR: A simplified and optimized version of ChIP assay is described by reducing the number of experimental steps and isolation solutions and shortening preparation times and is easy to adapt for other systems as well.
Abstract: Chromatin immunoprecipitation (ChIP) is a powerful tool for the characterization of covalent histone modifications and DNA-histone interactions in vivo. The procedure includes DNA-histone cross-linking in chromatin, shearing DNA into smaller fragments, immunoprecipitation with antibodies against the histone modifications of interest, followed by PCR identification of associated DNA sequences. In this protocol, we describe a simplified and optimized version of ChIP assay by reducing the number of experimental steps and isolation solutions and shortening preparation times. We include a nuclear isolation step before chromatin shearing, which provides a good yield of high-quality DNA resulting in at least 15 mug of DNA from each immunoprecipitated sample (from 0.2 to 0.4 g of starting tissue material) sufficient to test > or =25 genes of interest. This simpler and cost-efficient protocol has been applied for histone-modification studies of various Arabidopsis thaliana tissues and is easy to adapt for other systems as well.
485 citations
TL;DR: The results suggest that transposon methylation may be guided by histone H3 methylation in plant genomes, which would account for the epigenetic inheritance of hypomethylated DNA once histone Lysine 4 methylation patterns are altered.
Abstract: The Arabidopsis gene DDM1 is required to maintain DNA methylation levels and is responsible for transposon and transgene silencing. However, rather than encoding a DNA methyltransferase, DDM1 has similarity to the SWI/SNF family of adenosine triphosphate-dependent chromatin remodeling genes, suggesting an indirect role in DNA methylation. Here we show that DDM1 is also required to maintain histone H3 methylation patterns. In wild-type heterochromatin, transposons and silent genes are associated with histone H3 methylated at lysine 9, whereas known genes are preferentially associated with methylated lysine 4. In ddm1 heterochromatin, DNA methylation is lost, and methylation of lysine 9 is largely replaced by methylation of lysine 4. Because DNA methylation has recently been shown to depend on histone H3 lysine 9 methylation, our results suggest that transposon methylation may be guided by histone H3 methylation in plant genomes. This would account for the epigenetic inheritance of hypomethylated DNA once histone H3 methylation patterns are altered.
467 citations
TL;DR: Both WRKY38 and WRKY62 are transcriptional activators in plant cells, but their activation activities are abolished by overexpressed HDA19, which has a role opposite from those of WR KY38 andWRKY62 in basal resistance to the bacterial pathogen.
Abstract: Arabidopsis thaliana WRKY38 and WRKY62, encoding two structurally similar type III WRKY transcription factors, are induced in a Nonexpressor of PR Gene1 (NPR1)-dependent manner by salicylic acid (SA) or by virulent Pseudomonas syringae. Disease resistance and SA-regulated Pathogenesis-Related1 (PR1) gene expression are enhanced in the wrky38 and wrky62 single mutants and, to a greater extent, in the double mutants. Overexpression of WRKY38 or WRKY62 reduces disease resistance and PR1 expression. Thus, WRKY38 and WRKY62 function additively as negative regulators of plant basal defense. WRKY38 and WRKY62 interact with Histone Deacetylase 19 (HDA19). Expression of HDA19 is also induced by P. syringae, and the stability of its induced transcripts depends on SA and NPR1 in infected plants. Disruption of HDA19 leads to compromised resistance, whereas its overexpression results in enhanced resistance to P. syringae. Thus, HDA19 has a role opposite from those of WRKY38 and WRKY62 in basal resistance to the bacterial pathogen. Both WRKY38 and WRKY62 are transcriptional activators in plant cells, but their activation activities are abolished by overexpressed HDA19. Interaction of WRKY38 and WRKY62 with HDA19 may act to fine-tune plant basal defense responses.
466 citations