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: There is such a diversity of DNA methylation profiling techniques that it can be challenging to select one, and this Review discusses the different approaches and their relative merits and introduces considerations for data analysis.
Abstract: Methylation of cytosine bases in DNA provides a layer of epigenetic control in many eukaryotes that has important implications for normal biology and disease. Therefore, profiling DNA methylation across the genome is vital to understanding the influence of epigenetics. There has been a revolution in DNA methylation analysis technology over the past decade: analyses that previously were restricted to specific loci can now be performed on a genome-scale and entire methylomes can be characterized at single-base-pair resolution. However, there is such a diversity of DNA methylation profiling techniques that it can be challenging to select one. This Review discusses the different approaches and their relative merits and introduces considerations for data analysis.
1,521 citations
TL;DR: The evolutionary relationship between Jumonji C (JmjC)-domain-containing proteins is analysed and their cellular functions in relation to their potential enzymatic activities are discussed.
Abstract: Histone methylation has important roles in regulating gene expression and forms part of the epigenetic memory system that regulates cell fate and identity. Enzymes that directly remove methyl marks from histones have recently been identified, revealing a new level of plasticity within this epigenetic modification system. Here we analyse the evolutionary relationship between Jumonji C (JmjC)-domain-containing proteins and discuss their cellular functions in relation to their potential enzymatic activities.
1,149 citations
TL;DR: Insight is provided into how modification of one residue can influence that of another, even when they are located on different histones, and how modifications at specific genomic locations might be perpetuated on newly assembled chromatin.
1,128 citations
TL;DR: The mechanisms of genome-wide erasure of DNA methylation, which involve modifications to 5-methylcytosine and DNA repair, are being unraveled.
Abstract: Epigenetic modifications of the genome are generally stable in somatic cells of multicellular organisms. In germ cells and early embryos, however, epigenetic reprogramming occurs on a genome-wide scale, which includes demethylation of DNA and remodeling of histones and their modifications. The mechanisms of genome-wide erasure of DNA methylation, which involve modifications to 5-methylcytosine and DNA repair, are being unraveled. Epigenetic reprogramming has important roles in imprinting, the natural as well as experimental acquisition of totipotency and pluripotency, control of transposons, and epigenetic inheritance across generations. Small RNAs and the inheritance of histone marks may also contribute to epigenetic inheritance and reprogramming. Reprogramming occurs in flowering plants and in mammals, and the similarities and differences illuminate developmental and reproductive strategies.
1,074 citations
TL;DR: Activation tagging using T-DNA vectors that contain multimerized transcriptional enhancers from the cauliflower mosaic virus (CaMV) 35S gene has been applied to Arabidopsis plants, and it is shown that overexpressed genes are almost always found immediately adjacent to the inserted CaMV 35S enhancers.
Abstract: Activation tagging using T-DNA vectors that contain multimerized transcriptional enhancers from the cauliflower mosaic virus (CaMV) 35S gene has been applied to Arabidopsis plants. New activation-tagging vectors that confer resistance to the antibiotic kanamycin or the herbicide glufosinate have been used to generate several tens of thousands of transformed plants. From these, over 30 dominant mutants with various phenotypes have been isolated. Analysis of a subset of mutants has shown that overexpressed genes are almost always found immediately adjacent to the inserted CaMV 35S enhancers, at distances ranging from 380 bp to 3.6 kb. In at least one case, the CaMV 35S enhancers led primarily to an enhancement of the endogenous expression pattern rather than to constitutive ectopic expression, suggesting that the CaMV 35S enhancers used here act differently than the complete CaMV 35S promoter. This has important implications for the spectrum of genes that will be discovered by this method.
1,023 citations