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: This review summarizes recent molecular studies on the miRNAs involved in the regulation of drought-responsive genes, with emphasis on miRNA-associated regulatory networks involved in drought stress response.
Abstract: Drought is a major environmental stress factor that limits agricultural production worldwide. Plants employ complex mechanisms of gene regulation in response to drought stress. MicroRNAs (miRNAs) are a class of small RNAs that are increasingly being recognized as important modulators of gene expression at the post-transcriptional level. Many miRNAs have been shown to be involved in drought stress responses, including ABA response, auxin signalling, osmoprotection, and antioxidant defence, by downregulating the respective target genes encoding regulatory and functional proteins. This review summarizes recent molecular studies on the miRNAs involved in the regulation of drought-responsive genes, with emphasis on miRNA-associated regulatory networks involved in drought stress response.
239 citations
TL;DR: Results indicate that WRKY46, WRKY70, and WRKY53 positively regulate basal resistance to P. syringae; and that they play overlapping and synergetic roles in plant basal defense.
237 citations
Boston University1, University of Greifswald2, University of Alabama at Birmingham3, Johns Hopkins University4, University of Oxford5, Indiana University6, University of Texas Health Science Center at Houston7, King's College London8, Utrecht University9, University of California, Los Angeles10, University of Gothenburg11, National Institutes of Health12, Wake Forest University13, Harvard University14, University of Exeter15, University of Oulu16, University of Lübeck17, Imperial College London18, California Pacific Medical Center19, French Institute of Health and Medical Research20, University of Massachusetts Amherst21, Erasmus University Rotterdam22, Hannover Medical School23, Lund University24, University of Helsinki25, National Institute for Health and Welfare26, Fred Hutchinson Cancer Research Center27, Uppsala University28, University of Parma29, University of Pittsburgh30, Broad Institute31, Ludwig Maximilian University of Munich32, Cedars-Sinai Medical Center33, University of Washington34, Wellcome Trust Sanger Institute35, Memorial University of Newfoundland36, University of Turku37
TL;DR: Evidence of sex-differentiated genetic influences on sex steroid hormone-binding globulin is found and the importance of considering these features when estimating complex trait variance is highlighted.
Abstract: Sex hormone-binding globulin (SHBG) is a glycoprotein responsible for the transport and biologic availability of sex steroid hormones, primarily testosterone and estradiol. SHBG has been associated with chronic diseases including type 2 diabetes (T2D) and with hormone-sensitive cancers such as breast and prostate cancer. We performed a genome-wide association study (GWAS) meta-analysis of 21,791 individuals from 10 epidemiologic studies and validated these findings in 7,046 individuals in an additional six studies. We identified twelve genomic regions (SNPs) associated with circulating SHBG concentrations. Loci near the identified SNPs included SHBG (rs12150660, 17p13.1, p = 1.8x10(-106)), PRMT6 (rs17496332, 1p13.3, p=1.4x10(-11)), GCKR (rs780093, 2p23.3, p=2.2x10(-16)), ZBTB10 (rs440837, 8q21.13, p=3.4x10(-09)), JMJD1C (rs7910927, 10q21.3, p=6.1x10(-35)), SLCO1B1 (rs4149056, 12p12.1, p=1.9x10(-08)), NR2F2 (rs8023580, 15q26.2, p=8.3x10(-12)), ZNF652 (rs2411984, 17q21.32, p=3.5x10(-14)), TDGF3 (rs1573036, Xq22.3, p=4.1x10(-14)), LHCGR (rs10454142, 2p16.3, p=1.3x10(-07)), BAIAP2L1 (rs3779195, 7q21.3, p=2.7x10(-08)), and UGT2B15 (rs293428, 4q13.2, p=5.5x10(-06)). These genes encompass multiple biologic pathways, including hepatic function, lipid metabolism, carbohydrate metabolism and T2D, androgen and estrogen receptor function, epigenetic effects, and the biology of sex steroid hormone-responsive cancers including breast and prostate cancer. We found evidence of sex-differentiated genetic influences on SHBG. In a sex-specific GWAS, the loci 4q13.2-UGT2B15 was significant in men only (men p = 2.5x10(-08), women p=0.66, heterogeneity p=0.003). Additionally, three loci showed strong sex-differentiated effects: 17p13.1-SHBG and Xq22.3-TDGF3 were stronger in men, whereas 8q21.12-ZBTB10 was stronger in women. Conditional analyses identified additional signals at the SHBG gene that together almost double the proportion of variance explained at the locus. Using an independent study of 1,129 individuals, all SNPs identified in the overall or sex-differentiated or conditional analyses explained similar to 15.6% and similar to 8.4% of the genetic variation of SHBG concentrations in men and women, respectively. The evidence for sex-differentiated effects and allelic heterogeneity highlight the importance of considering these features when estimating complex trait variance.
231 citations
TL;DR: Results suggested that HD2C functionally associates with HDA6 and regulates gene expression through histone modifications, which support a role of HD 2C in the ABA and salt-stress response in Arabidopsis.
Abstract: HD2 proteins are plant specific histone deacetylases. Four HD2 proteins, HD2A, HD2B, HD2C, and HD2D, have been identified in Arabidopsis. It was found that the expression of HD2A, HD2B, HD2C, and HD2D was repressed by ABA and NaCl. To investigate the function of HD2 proteins further, two HD2C T-DNA insertion lines of Arabidopsis, hd2c-1 and hd2c-3 were identified. Compared with wild-type plants, hd2c-1 and hd2c-3 plants displayed increased sensitivity to ABA and NaCl during germination and decreased tolerance to salt stress. These observations support a role of HD2C in the ABA and salt-stress response in Arabidopsis. Moreover, it was demonstrated that HD2C interacted physically with a RPD3-type histone deacetylase, HDA6, and bound to histone H3. The expression of ABA-responsive genes, ABI1 and ABI2, was increased in hda6, hd2c, and hda6/hd2c-1 double mutant plants, which was associated with increased histone H3K9K14 acetylation and decreased histone H3K9 dimethylation. Taken together, our results suggested that HD2C functionally associates with HDA6 and regulates gene expression through histone modifications.
228 citations
TL;DR: It is shown that low-temperature treatments repress FLC in cells that are not mitotically active, but this repression is not fully maintained, suggesting that DNA replication is essential for maintenance of vernalization-induced repression of FLC.
225 citations