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

Xiaoqing Wu; Hongfei Liu; Bi Lian; Xue Jiang; Cheng Chen; Tianxin Tang; Xinlun Ding; Jie Hu; Shanshan Zhao; Shuai Zhang; Jianguo Wu

doi:10.3389/fpls.2022.1090794

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

Front Plant Sci. 2023 Jan 11:13:1090794. doi: 10.3389/fpls.2022.1090794. eCollection 2022.

Authors

Xiaoqing Wu¹, Hongfei Liu¹, Bi Lian², Xue Jiang¹, Cheng Chen¹, Tianxin Tang¹, Xinlun Ding¹, Jie Hu¹, Shanshan Zhao¹, Shuai Zhang¹, Jianguo Wu¹

Affiliations

¹ Vector-borne Virus Research Center, Key Laboratory of Plant Virology of Fujian Province, Institute of Plant Virology, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China.
² Center for Plant Biology, School of Life Sciences, Tsinghua University, Beijing, China.

Abstract

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.

Keywords: H3K9me3; RGSV; association analysis; methylation; transcriptome.

Grants and funding

This work was supported by grants from the National Natural Science Foundation of China (Nos. 32025031, U1905203, 32072381, 31901851), the Outstanding Youth Research Program of Fujian Agriculture and Forestry University (xjq202003), and Natural Science Foundation of Fujian Province of China (2019J01371, 2019J01370, 2019J01667).