Characterization of functional relationships of R-loops with gene transcription and epigenetic modifications in rice
- Yuan Fang1,6,
- Lifen Chen1,6,
- Kande Lin1,
- Yilong Feng1,
- Pengyue Zhang1,
- Xiucai Pan1,
- Jennifer Sanders2,
- Yufeng Wu1,
- Xiu-e Wang1,
- Zhen Su3,
- Caiyan Chen4,
- Hairong Wei2,5 and
- Wenli Zhang1
- 1State Key Laboratory for Crop Genetics and Germplasm Enhancement, JiangSu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China;
- 2School of Forest Resources and Environmental Science, Michigan Technological University, Houghton, Michigan 49931, USA;
- 3State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, P.R. China;
- 4Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan, 410125, P.R. China;
- 5Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing 100083, P.R. China
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↵6 These authors contributed equally to this work.
Abstract
We conducted genome-wide identification of R-loops followed by integrative analyses of R-loops with relation to gene expression and epigenetic signatures in the rice genome. We found that the correlation between gene expression levels and profiled R-loop peak levels was dependent on the positions of R-loops within gene structures (hereafter named “genic position”). Both antisense only (ASO)-R-loops and sense/antisense (S/AS)-R-loops sharply peaked around transcription start sites (TSSs), and these peak levels corresponded positively with transcript levels of overlapping genes. In contrast, sense only (SO)-R-loops were generally spread over the coding regions, and their peak levels corresponded inversely to transcript levels of overlapping genes. In addition, integrative analyses of R-loop data with existing RNA-seq, chromatin immunoprecipitation sequencing (ChIP-seq), DNase I hypersensitive sites sequencing (DNase-seq), and whole-genome bisulfite sequencing (WGBS or BS-seq) data revealed interrelationships and intricate connections among R-loops, gene expression, and epigenetic signatures. Experimental validation provided evidence that the demethylation of both DNA and histone marks can influence R-loop peak levels on a genome-wide scale. This is the first study in plants that reveals novel functional aspects of R-loops, their interrelations with epigenetic methylation, and roles in transcriptional regulation.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.246009.118.
- Received November 11, 2018.
- Accepted June 27, 2019.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
