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.
Citations
More filters
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]....
[...]
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…...
[...]
...Transcriptomics will need to be complemented also by consideration of epigenetics and small RNA regulatory mechanisms (Humbeck, 2013; Ay et al., 2014a)....
[...]
...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)....
[...]
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)....
[...]
...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)....
[...]
References
More filters
TL;DR: A critical overview of different genome-wide techniques for DNA methylation analysis is provided and it is proposed that MeDIP assays may constitute a key method for elucidating the hypermethylome of cancer cells.
Abstract: One of the most challenging projects in the field of epigenetics is the generation of detailed functional maps of DNA methylation in different cell and tissue types in normal and disease-associated conditions. This information will help us not only understand the role of DNA methylation but also identify targets for therapeutic treatment. The completion of the various epigenome projects depends on the design of novel strategies to survey and generate detailed cartograms of the DNA methylome. Methyl-DNA immunoprecipitation (MeDIP) assays, in combination with hybridization on high-resolution microarrays or high-throughput sequencing (HTS) techniques, are excellent methods for identifying methylated CpG-rich sequences. We provide a critical overview of different genome-wide techniques for DNA methylation analysis and propose that MeDIP assays may constitute a key method for elucidating the hypermethylome of cancer cells.
219 citations
TL;DR: By analysing microarray expression data from 27 different treatments and comparing them with that from developmental leaf senescence, it is shown that at early stages of treatments, different hormones and stresses showed limited similarity in the induction of gene expression to that of developmental leafsenescence.
Abstract: In addition to age and developmental progress, leaf senescence and senescence-associated genes (SAGs) can be induced by other factors such as plant hormones, pathogen infection and environmental stresses. The relationship is not clear, however, between these induced senescence processes and developmental leaf senescence, and to what extent these senescence-promoting signals mimic age and developmental senescence in terms of gene expression profiles. By analysing microarray expression data from 27 different treatments (that are known to promote senescence) and comparing them with that from developmental leaf senescence, we were able to show that at early stages of treatments, different hormones and stresses showed limited similarity in the induction of gene expression to that of developmental leaf senescence. Once the senescence process is initiated, as evidenced by visible yellowing, generally after a prolonged period of treatments, a great proportion of SAGs of developmental leaf senescence are shared by gene expression profiles in response to different treatments. This indicates that although different signals that lead to initiation of senescence may do so through distinct signal transduction pathways, senescence processes induced either developmentally or by different senescence-promoting treatments may share common execution events.
214 citations
TL;DR: In this article, the ATP-dependent chromatin remodeling complex SWR1 was found to interact with PIE1 in Arabidopsis, but not canonical H2A histone.
Abstract: One of the mechanisms involved in chromatin remodelling is so-called 'histone replacement'. An example of such a mechanism is the substitution of canonical H2A histone by the histone variant H2A.Z. The ATP-dependent chromatin remodelling complex SWR1 is responsible for this action in yeast. We have previously proposed the existence of an SWR1-like complex in Arabidopsis by demonstrating genetic and physical interaction of the components SEF, ARP6 and PIE1, which are homologues of the yeast Swc6 and Arp6 proteins and the core ATPase Swr1, respectively. Here we show that histone variant H2A.Z, but not canonical H2A histone, interacts with PIE1. Plants mutated at loci HTA9 and HTA11 (two of the three Arabidopsis H2A.Z-coding genes) displayed developmental abnormalities similar to those found in pie1, sef and arp6 plants, exemplified by an early-flowering phenotype. Comparison of gene expression profiles revealed that 65% of the genes differentially regulated in hta9 hta11 plants were also mis-regulated in pie1 plants. Detailed examination of the expression data indicated that the majority of mis-regulated genes were related to salicylic acid-dependent immunity. RT-PCR and immunoblotting experiments confirmed constitutive expression of systemic acquired resistance (SAR) marker genes in pie1, hta9 hta11 and sef plants. Variations observed at the molecular level resulted in phenotypic alterations such as spontaneous cell death and enhanced resistance to the phytopathogenic bacteria Pseudomonas syringae pv. tomato. Thus, our results support the existence in Arabidopsis of an SWR1-like chromatin remodelling complex that is functionally related to that described in yeast and human, and attribute to this complex a role in maintaining a repressive state of the SAR response.
208 citations
TL;DR: Several chromatin-related proteins such as histone modification enzymes, linker histone H1 and components of chromatin remodeling complex influence the gene regulation in the stress responses.
Abstract: Plants respond and adapt to drought, cold and high-salinity stress in order to survive. Molecular and genomic studies have revealed that many stress-inducible genes with various functions and signalling factors, such as transcription factors, protein kinases and protein phosphatases, are involved in the stress responses. Recent studies have revealed the coordination of the gene expression and chromatin regulation in response to the environmental stresses. Several histone modifications are dramatically altered on the stress-responsive gene regions under drought stress conditions. Several chromatin-related proteins such as histone modification enzymes, linker histone H1 and components of chromatin remodeling complex influence the gene regulation in the stress responses. This review briefly describes chromatin regulation in response to drought, cold and high-salinity stress.
204 citations
TL;DR: The data indicate that AtWRKY70 functions downstream of defense-associated reactive oxygen intermediates and SA, and is required for RPP4-mediated resistance and basal defense against H. parasitica.
Abstract: AtWRKY70, encoding a WRKY transcription factor, is co-expressed with a set of Arabidopsis genes that share a pattern of RPP4- and RPP7-dependent late upregulation in response to Hyaloperonospora parasitica infection (LURP) genes. We show that AtWRKY70 is required for both full RPP4-mediated resistance and basal defense against H. parasitica. These two defense pathways are related to each other, because they require PAD4 and salicylic acid (SA). RPP7 function, which is independent from PAD4 and SA, is not affected by insertions in AtWRKY70. Although AtWRKY70 is required for RPP4-resistance, it appears not to contribute significantly to RPP4-triggered cell death. Furthermore, our data indicate that AtWRKY70 functions downstream of defense-associated reactive oxygen intermediates and SA. Constitutive and RPP4-induced transcript levels of two other LURP genes are reduced in AtWRKY70 T-DNA mutants, indicating a direct or indirect role for AtWRKY70 in their regulation. We propose that AtWRKY70 is a component of a basal defense mechanism that is boosted by engagement of either RPP4 or RPP7 and is required for RPP4-mediated resistance.
202 citations