Epigenetic Mechanisms Regulating Plant Development

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Plant, Algae and Fungi Cell Biology".

Deadline for manuscript submissions: closed (1 August 2022) | Viewed by 28183

Special Issue Editor


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Guest Editor
Institute of Plant Biology, National Taiwan University, Taipei, Taiwan
Interests: plant epigenetics; plant development; plant responses to abiotic stresses

Special Issue Information

Dear Colleagues,

Epigenetic mechanisms such as DNA methylation and chromatin alterations have a decisive function in regulating plant development. The involvement of epigenetic mechanisms in the plant response to environmental cues has been documented. Understanding how epigenetic regulation is involved in plant development is highly desirable, not just for a better understanding of molecular mechanisms of plant response to environment but also for possible application in the genetic manipulation of plants. The proposed topic is focused on epigenetic regulation of plant development. We welcome all types of articles (original research and reviews) that provide new insight into different aspects of plant epigenetics, including its regulation, its function in plant development and plant responses to abiotic and biotic stresses.

Prof. Keqiang Wu
Guest Editor

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Keywords

  • Histone modification 
  • DNA methylation 
  • Chromatin remodeling 
  • Plant Development

Published Papers (8 papers)

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Research

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24 pages, 8838 KiB  
Article
HSP70 Gene Family in Brassica rapa: Genome-Wide Identification, Characterization, and Expression Patterns in Response to Heat and Cold Stress
by Javaria Tabusam, Qiling Shi, Daling Feng, Sumer Zulfiqar, Shuxing Shen, Wei Ma and Jianjun Zhao
Cells 2022, 11(15), 2316; https://doi.org/10.3390/cells11152316 - 27 Jul 2022
Cited by 8 | Viewed by 2227
Abstract
Heat shock proteins protect plants from abiotic stress, such as salt, drought, heat, and cold stress. HSP70 is one of the major members of the heat shock protein family. To explore the mechanism of HSP70 in Brassica rapa, we identified 28 putative [...] Read more.
Heat shock proteins protect plants from abiotic stress, such as salt, drought, heat, and cold stress. HSP70 is one of the major members of the heat shock protein family. To explore the mechanism of HSP70 in Brassica rapa, we identified 28 putative HSP70 gene family members using state-of-the-art bioinformatics-based tools and methods. Based on chromosomal mapping, HSP70 genes were the most differentially distributed on chromosome A03 and the least distributed on chromosome A05. Ka/Ks analysis revealed that B. rapa evolution was subjected to intense purifying selection of the HSP70 gene family. RNA-sequencing data and expression profiling showed that heat and cold stress induced HSP70 genes. The qRT-PCR results verified that the HSP70 genes in Chinese cabbage (Brassica rapa ssp. pekinensis) are stress-inducible under both cold and heat stress. The upregulated expression pattern of these genes indicated the potential of HSP70 to mitigate environmental stress. These findings further explain the molecular mechanism underlying the responses of HSP70 to heat and cold stress. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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16 pages, 2198 KiB  
Article
DNA Methylation as an Early Indicator of Aging in Stored Seeds of “Exceptional” Species Populus nigra L.
by Marcin Michalak, Beata Patrycja Plitta-Michalak, Mirosława Zofia Naskręt-Barciszewska, Jan Barciszewski and Paweł Chmielarz
Cells 2022, 11(13), 2080; https://doi.org/10.3390/cells11132080 - 30 Jun 2022
Cited by 7 | Viewed by 1742
Abstract
Ex situ preservation of genetic resources is an essential strategy for the conservation of plant biodiversity. In this regard, seed storage is the most convenient and efficient way of preserving germplasm for future plant breeding efforts. A better understanding of the molecular changes [...] Read more.
Ex situ preservation of genetic resources is an essential strategy for the conservation of plant biodiversity. In this regard, seed storage is the most convenient and efficient way of preserving germplasm for future plant breeding efforts. A better understanding of the molecular changes that occur during seed desiccation and aging is necessary to improve conservation protocols, as well as real-time methods for monitoring seed quality. In the present study, we assessed changes in the level of genomic 5-methylcytosine (5mC) in seeds of Populus nigra L. by 2D-TLC. Epigenetic changes were characterized in response to several seed storage regimes. Our results demonstrate that P. nigra seeds represent an intermediate type of post-harvest behavior, falling between recalcitrant and orthodox seeds. This was also true for the epigenetic response of P. nigra seeds to external factors. A crucial question is whether aging in seeds is initiated by a decline in the level of 5mC, or if epigenetic changes induce a process that leads to deterioration. In our study, we demonstrate for the first time that 5mC levels decrease during storage and that the decline can be detected before any changes in seed germination are evident. Once P. nigra seeds reached an 8–10% reduction in the level of 5mC, a substantial decrease in germination occurred. The decline in the level of 5mC appears to be a critical parameter underlying the rapid deterioration of intermediate seeds. Thus, the measurement of 5mC can be a fast, real-time method for assessing asymptomatic aging in stored seeds. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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27 pages, 5474 KiB  
Article
Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
by Joanna Morończyk, Agnieszka Brąszewska, Barbara Wójcikowska, Karolina Chwiałkowska, Katarzyna Nowak, Anna M. Wójcik, Mirosław Kwaśniewski and Małgorzata D. Gaj
Cells 2022, 11(5), 863; https://doi.org/10.3390/cells11050863 - 2 Mar 2022
Cited by 12 | Viewed by 4286
Abstract
Somatic embryogenesis (SE), which is a process that involves the in vitro-induced embryogenic reprogramming of plant somatic cells, requires dynamic changes in the cell transcriptome. These changes are fine-tuned by many genetic and epigenetic factors, including posttranslational histone modifications such as histone acetylation. [...] Read more.
Somatic embryogenesis (SE), which is a process that involves the in vitro-induced embryogenic reprogramming of plant somatic cells, requires dynamic changes in the cell transcriptome. These changes are fine-tuned by many genetic and epigenetic factors, including posttranslational histone modifications such as histone acetylation. Antagonistically acting enzymes, histone acetyltransferases (HATs) and deacetylases (HDACs), which control histone acetylation in many developmental processes, are believed to control SE. However, the function of specific HAT/HDACs and the genes that are subjected to histone acetylation-mediated regulation during SE have yet to be revealed. Here, we present the global and gene-specific changes in histone acetylation in Arabidopsis explants that are undergoing SE. In the TSA (trichostatin A)-induced SE, we demonstrate that H3 and H4 acetylation might control the expression of the critical transcription factor (TF) genes of a vital role in SE, including LEC1, LEC2 (LEAFY COTYLEDON 1; 2), FUS3 (FUSCA 3) and MYB118 (MYB DOMAIN PROTEIN 118). Within the HATs and HDACs, which mainly positively regulate SE, we identified HDA19 as negatively affecting SE by regulating LEC1, LEC2 and BBM. Finally, we provide some evidence on the role of HDA19 in the histone acetylation-mediated regulation of LEC2 during SE. Our results reveal an essential function of histone acetylation in the epigenetic mechanisms that control the TF genes that play critical roles in the embryogenic reprogramming of plant somatic cells. The results implicate the complexity of Hac-related gene regulation in embryogenic induction and point to differences in the regulatory mechanisms that are involved in auxin- and TSA-induced SE. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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22 pages, 5286 KiB  
Article
miR172 Regulates WUS during Somatic Embryogenesis in Arabidopsis via AP2
by Katarzyna Nowak, Joanna Morończyk, Małgorzata Grzyb, Aleksandra Szczygieł-Sommer and Małgorzata D. Gaj
Cells 2022, 11(4), 718; https://doi.org/10.3390/cells11040718 - 17 Feb 2022
Cited by 14 | Viewed by 3964
Abstract
In plants, the embryogenic transition of somatic cells requires the reprogramming of the cell transcriptome, which is under the control of genetic and epigenetic factors. Correspondingly, the extensive modulation of genes encoding transcription factors and miRNAs has been indicated as controlling the induction [...] Read more.
In plants, the embryogenic transition of somatic cells requires the reprogramming of the cell transcriptome, which is under the control of genetic and epigenetic factors. Correspondingly, the extensive modulation of genes encoding transcription factors and miRNAs has been indicated as controlling the induction of somatic embryogenesis in Arabidopsis and other plants. Among the MIRNAs that have a differential expression during somatic embryogenesis, members of the MIRNA172 gene family have been identified, which implies a role of miR172 in controlling the embryogenic transition in Arabidopsis. In the present study, we found a disturbed expression of both MIRNA172 and candidate miR172-target genes, including AP2, TOE1, TOE2, TOE3, SMZ and SNZ, that negatively affected the embryogenic response of transgenic explants. Next, we examined the role of AP2 in the miR172-mediated mechanism that controls the embryogenic response. We found some evidence that by controlling AP2, miR172 might repress the WUS that has an important function in embryogenic induction. We showed that the mechanism of the miR172-AP2-controlled repression of WUS involves histone acetylation. We observed the upregulation of the WUS transcripts in an embryogenic culture that was overexpressing AP2 and treated with trichostatin A (TSA), which is an inhibitor of HDAC histone deacetylases. The increased expression of the WUS gene in the embryogenic culture of the hdac mutants further confirmed the role of histone acetylation in WUS control during somatic embryogenesis. A chromatin-immunoprecipitation analysis provided evidence about the contribution of HDA6/19-mediated histone deacetylation to AP2-controlled WUS repression during embryogenic induction. The upstream regulatory elements of the miR172-AP2-WUS pathway might involve the miR156-controlled SPL9/SPL10, which control the level of mature miR172 in an embryogenic culture. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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15 pages, 14954 KiB  
Article
Arabidopsis SUMO E3 Ligase SIZ1 Interacts with HDA6 and Negatively Regulates HDA6 Function during Flowering
by Sujuan Gao, Xueqin Zeng, Jianhao Wang, Yingchao Xu, Chunwei Yu, Yishui Huang, Feng Wang, Keqiang Wu and Songguang Yang
Cells 2021, 10(11), 3001; https://doi.org/10.3390/cells10113001 - 3 Nov 2021
Cited by 2 | Viewed by 2984
Abstract
The changes in histone acetylation mediated by histone deacetylases (HDAC) play a crucial role in plant development and response to environmental changes. Mammalian HDACs are regulated by post-translational modifications (PTM), such as phosphorylation, acetylation, ubiquitination and small ubiquitin-like modifier (SUMO) modification (SUMOylation), which [...] Read more.
The changes in histone acetylation mediated by histone deacetylases (HDAC) play a crucial role in plant development and response to environmental changes. Mammalian HDACs are regulated by post-translational modifications (PTM), such as phosphorylation, acetylation, ubiquitination and small ubiquitin-like modifier (SUMO) modification (SUMOylation), which affect enzymatic activity and transcriptional repression. Whether PTMs of plant HDACs alter their functions are largely unknown. In this study, we demonstrated that the Arabidopsis SUMO E3 ligase SAP AND MIZ1 DOMAIN-CONTAINING LIGASE1 (SIZ1) interacts with HISTONE DEACETYLASE 6 (HDA6) both in vitro and in vivo. Biochemical analyses indicated that HDA6 is not modified by SUMO1. Overexpression of HDA6 in siz1-3 background results in a decreased level of histone H3 acetylation, indicating that the activity of HDA6 is increased in siz1-3 plants. Chromatin immunoprecipitation (ChIP) assays showed that SIZ1 represses HDA6 binding to its target genes FLOWERING LOCUS C (FLC) and MADS AFFECTING FLOWERING 4 (MAF4), resulting in the upregulation of FLC and MAF4 by increasing the level of histone H3 acetylation. Together, these findings indicate that the Arabidopsis SUMO E3 ligase SIZ1 interacts with HDA6 and negatively regulates HDA6 function. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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16 pages, 1327 KiB  
Article
Cauliflower mosaic virus P6 Dysfunctions Histone Deacetylase HD2C to Promote Virus Infection
by Shun Li, Shanwu Lyu, Yujuan Liu, Ming Luo, Suhua Shi and Shulin Deng
Cells 2021, 10(9), 2278; https://doi.org/10.3390/cells10092278 - 1 Sep 2021
Cited by 9 | Viewed by 2540
Abstract
Histone deacetylases (HDACs) are vital epigenetic modifiers not only in regulating plant development but also in abiotic- and biotic-stress responses. Though to date, the functions of HD2C—an HD2-type HDAC—In plant development and abiotic stress have been intensively explored, its function in biotic stress [...] Read more.
Histone deacetylases (HDACs) are vital epigenetic modifiers not only in regulating plant development but also in abiotic- and biotic-stress responses. Though to date, the functions of HD2C—an HD2-type HDAC—In plant development and abiotic stress have been intensively explored, its function in biotic stress remains unknown. In this study, we have identified HD2C as an interaction partner of the Cauliflower mosaic virus (CaMV) P6 protein. It functions as a positive regulator in defending against CaMV infection. The hd2c mutants show enhanced susceptibility to CaMV infection. In support, the accumulation of viral DNA, viral transcripts, and the deposition of histone acetylation on the viral minichromosomes are increased in hd2c mutants. P6 interferes with the interaction between HD2C and HDA6, and P6 overexpression lines have similar phenotypes with hd2c mutants. In further investigations, P6 overexpression lines, together with CaMV infection plants, are more sensitive to ABA and NaCl with a concomitant increasing expression of ABA/NaCl-regulated genes. Moreover, the global levels of histone acetylation are increased in P6 overexpression lines and CaMV infection plants. Collectively, our results suggest that P6 dysfunctions histone deacetylase HD2C by physical interaction to promote CaMV infection. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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17 pages, 5476 KiB  
Article
The Transcriptional Adaptor Protein ADA3a Modulates Flowering of Arabidopsis thaliana
by Stylianos Poulios, Despoina Dadarou, Maxim Gavriilidis, Niki Mougiou, Nestoras Kargios, Vasileia Maliori, Amy T. Hark, John H. Doonan and Konstantinos E. Vlachonasios
Cells 2021, 10(4), 904; https://doi.org/10.3390/cells10040904 - 14 Apr 2021
Cited by 3 | Viewed by 3019
Abstract
Histone acetylation is directly related to gene expression. In yeast, the acetyltransferase general control nonderepressible-5 (GCN5) targets histone H3 and associates with transcriptional co-activators alteration/deficiency in activation-2 (ADA2) and alteration/deficiency in activation-3 (ADA3) in complexes like SAGA. Arabidopsis thaliana has two genes encoding [...] Read more.
Histone acetylation is directly related to gene expression. In yeast, the acetyltransferase general control nonderepressible-5 (GCN5) targets histone H3 and associates with transcriptional co-activators alteration/deficiency in activation-2 (ADA2) and alteration/deficiency in activation-3 (ADA3) in complexes like SAGA. Arabidopsis thaliana has two genes encoding proteins, designated ADA3a and ADA3b, that correspond to yeast ADA3. We investigated the role of ADA3a and ADA3b in regulating gene expression during flowering time. Specifically, we found that knock out mutants ada3a-2 and the double mutant ada3a-2 ada3b-2 lead to early flowering compared to the wild type plants under long day (LD) conditions and after moving plants from short days to LD. Consistent with ADA3a being a repressor of floral initiation, FLOWERING LOCUS T (FT) expression was increased in ada3a mutants. In contrast, other genes involved in multiple pathways leading to floral transition, including FT repressors, players in GA signaling, and members of the SPL transcriptional factors, displayed reduced expression. Chromatin immunoprecipitation analysis revealed that ADA3a affects the histone H3K14 acetylation levels in SPL3, SPL5, RGA, GAI, and SMZ loci. In conclusion, ADA3a is involved in floral induction through a GCN5-containing complex that acetylates histone H3 in the chromatin of flowering related genes. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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Review

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21 pages, 2162 KiB  
Review
Updated Mechanisms of GCN5—The Monkey King of the Plant Kingdom in Plant Development and Resistance to Abiotic Stresses
by Lei Gan, Zhenzhen Wei, Zuoren Yang, Fuguang Li and Zhi Wang
Cells 2021, 10(5), 979; https://doi.org/10.3390/cells10050979 - 22 Apr 2021
Cited by 16 | Viewed by 6131
Abstract
Histone modifications are the main epigenetic mechanisms that regulate gene expression, chromatin structure, and plant development, among which histone acetylation is one of the most important and studied epigenetic modifications. Histone acetylation is believed to enhance DNA access and promote transcription. GENERAL CONTROL [...] Read more.
Histone modifications are the main epigenetic mechanisms that regulate gene expression, chromatin structure, and plant development, among which histone acetylation is one of the most important and studied epigenetic modifications. Histone acetylation is believed to enhance DNA access and promote transcription. GENERAL CONTROL NON-REPRESSIBLE 5 (GCN5), a well-known enzymatic protein responsible for the lysine acetylation of histone H3 and H4, is a universal and crucial histone acetyltransferase involved in gene transcription and plant development. Many studies have found that GCN5 plays important roles in the different development stages of Arabidopsis. In terms of exogenous stress conditions, GCN5 is also involved in the responses to heat stress, cold stress, and nutrient element deficiency by regulating the related gene expression to maintain the homeostasis of some key metabolites (e.g., cellulose) or ions (e.g., phosphate, iron); in addition, GCN5 is involved in the phytohormone pathways such as ethylene, auxin, and salicylic acid to play various roles during the plant lifecycle. Some of the pathways involved by GCN5 also interwind to regulate specific physiological processes or developmental stages. Here, interactions between various developmental events and stress-resistant pathways mediated by GCN5 are comprehensively addressed and the underlying mechanisms are discussed in the plant. Studies with some interacting factors such as ADA2b provided valuable information for the complicated histone acetylation mechanisms. We also suggest the future focuses for GCN5 functions and mechanisms such as functions in seed development/germination stages, exploration of novel interaction factors, identification of more protein substrates, and application of advanced biotechnology-CRISPR in crop genetic improvement, which would be helpful for the complete illumination of roles and mechanisms of GCN5. Full article
(This article belongs to the Special Issue Epigenetic Mechanisms Regulating Plant Development)
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