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Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice

Rice grassy stunt virus (RGSV), a typical negative single-stranded RNA virus, invades rice and generates several disease signs, including dwarfing, tillering, and sterility. Previous research has revealed that RGSV-encoded proteins can force the host’s ubiquitin-proteasome system to utilize them for...

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Autores principales: Wu, Xiaoqing, Liu, Hongfei, Lian, Bi, Jiang, Xue, Chen, Cheng, Tang, Tianxin, Ding, Xinlun, Hu, Jie, Zhao, Shanshan, Zhang, Shuai, Wu, Jianguo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9874293/
https://www.ncbi.nlm.nih.gov/pubmed/36714706
http://dx.doi.org/10.3389/fpls.2022.1090794
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author Wu, Xiaoqing
Liu, Hongfei
Lian, Bi
Jiang, Xue
Chen, Cheng
Tang, Tianxin
Ding, Xinlun
Hu, Jie
Zhao, Shanshan
Zhang, Shuai
Wu, Jianguo
author_facet Wu, Xiaoqing
Liu, Hongfei
Lian, Bi
Jiang, Xue
Chen, Cheng
Tang, Tianxin
Ding, Xinlun
Hu, Jie
Zhao, Shanshan
Zhang, Shuai
Wu, Jianguo
author_sort Wu, Xiaoqing
collection PubMed
description Rice grassy stunt virus (RGSV), a typical negative single-stranded RNA virus, invades rice and generates several disease signs, including dwarfing, tillering, and sterility. Previous research has revealed that RGSV-encoded proteins can force the host’s ubiquitin-proteasome system to utilize them for viral pathogenesis. However, most of the studies were limited to a single omics level and lacked multidimensional data collection and correlation analysis on the mechanisms of RGSV-rice interactions. Here, we performed a comprehensive association analysis of genome-wide methylation sequencing, transcriptome sequencing, and histone H3K9me3 modification in RGSV-infested as well as non-infested rice leaves, and the levels of all three cytosine contexts (CG, CHG and CHH) were found to be slightly lower in RGSV-infected rice leaves than in normal rice. Large proportions of DMRs were distributed in the promoter and intergenic regions, and most DMRs were enriched in the CHH context, where the number of CHH hypo-DMRs was almost twice as high as that of hyper-DMRs. Among the genes with down-regulated expression and hypermethylation, we analyzed and identified 11 transcripts involved in fertility, plant height and tillering, and among the transcribed up-regulated and hypermethylated genes, we excavated 7 transcripts related to fertility, plant height and tillering. By analyzing the changes of histone H3K9me3 modification before and after virus infestation, we found that the distribution of H3K9me3 modification in the whole rice genome was prevalent, mainly concentrated in the gene promoter and gene body regions, which was distinctly different from the characteristics of animals. Combined with transcriptomic data, H3K9me3 mark was found to favor targeting highly expressed genes. After RGSV infection, H3K9me3 modifications in several regions of CTK and BR hormone signaling-related genes were altered, providing important targets for subsequent studies.
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spelling pubmed-98742932023-01-26 Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice Wu, Xiaoqing Liu, Hongfei Lian, Bi Jiang, Xue Chen, Cheng Tang, Tianxin Ding, Xinlun Hu, Jie Zhao, Shanshan Zhang, Shuai Wu, Jianguo Front Plant Sci Plant Science Rice grassy stunt virus (RGSV), a typical negative single-stranded RNA virus, invades rice and generates several disease signs, including dwarfing, tillering, and sterility. Previous research has revealed that RGSV-encoded proteins can force the host’s ubiquitin-proteasome system to utilize them for viral pathogenesis. However, most of the studies were limited to a single omics level and lacked multidimensional data collection and correlation analysis on the mechanisms of RGSV-rice interactions. Here, we performed a comprehensive association analysis of genome-wide methylation sequencing, transcriptome sequencing, and histone H3K9me3 modification in RGSV-infested as well as non-infested rice leaves, and the levels of all three cytosine contexts (CG, CHG and CHH) were found to be slightly lower in RGSV-infected rice leaves than in normal rice. Large proportions of DMRs were distributed in the promoter and intergenic regions, and most DMRs were enriched in the CHH context, where the number of CHH hypo-DMRs was almost twice as high as that of hyper-DMRs. Among the genes with down-regulated expression and hypermethylation, we analyzed and identified 11 transcripts involved in fertility, plant height and tillering, and among the transcribed up-regulated and hypermethylated genes, we excavated 7 transcripts related to fertility, plant height and tillering. By analyzing the changes of histone H3K9me3 modification before and after virus infestation, we found that the distribution of H3K9me3 modification in the whole rice genome was prevalent, mainly concentrated in the gene promoter and gene body regions, which was distinctly different from the characteristics of animals. Combined with transcriptomic data, H3K9me3 mark was found to favor targeting highly expressed genes. After RGSV infection, H3K9me3 modifications in several regions of CTK and BR hormone signaling-related genes were altered, providing important targets for subsequent studies. Frontiers Media S.A. 2023-01-11 /pmc/articles/PMC9874293/ /pubmed/36714706 http://dx.doi.org/10.3389/fpls.2022.1090794 Text en Copyright © 2023 Wu, Liu, Lian, Jiang, Chen, Tang, Ding, Hu, Zhao, Zhang and Wu https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Wu, Xiaoqing
Liu, Hongfei
Lian, Bi
Jiang, Xue
Chen, Cheng
Tang, Tianxin
Ding, Xinlun
Hu, Jie
Zhao, Shanshan
Zhang, Shuai
Wu, Jianguo
Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice
title Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice
title_full Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice
title_fullStr Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice
title_full_unstemmed Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice
title_short Genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of RGSV in rice
title_sort genome-wide analysis of epigenetic and transcriptional changes in the pathogenesis of rgsv in rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9874293/
https://www.ncbi.nlm.nih.gov/pubmed/36714706
http://dx.doi.org/10.3389/fpls.2022.1090794
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