In situ dissecting the evolution of gene duplication with different histone modification patterns based on high-throughput data analysis in Arabidopsis thaliana

Jingjing Wang; Yuriy L Orlov; Xue Li; Yincong Zhou; Yongjing Liu; Chunhui Yuan; Ming Chen

doi:10.7717/peerj.10426

In situ dissecting the evolution of gene duplication with different histone modification patterns based on high-throughput data analysis in Arabidopsis thaliana

PeerJ. 2021 Jan 5:9:e10426. doi: 10.7717/peerj.10426. eCollection 2021.

Authors

Jingjing Wang^#^{1

2

3

4}, Yuriy L Orlov^#^{5

6

7}, Xue Li^{3

8}, Yincong Zhou^{2

3}, Yongjing Liu^{2

3}, Chunhui Yuan^{4

9}, Ming Chen^{1

2

3}

Affiliations

¹ Center for Stem Cell and Regenerative Medicine, The First Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang University, Hangzhou, P. R. China.
² Department of Bioinformatics, The State Key Laboratory of Plant Physiology and Biochemistry, Institute of Plant Science, College of Life Sciences, Zhejiang University, Hangzhou, P. R. China.
³ James D. Watson Institute of Genome Sciences, Zhejiang University, Hangzhou, P. R. China.
⁴ Zhejiang Provincial Key Lab for Tissue Engineering and Regenerative Medicine, Dr. Li Dak Sum & Yip Yio Chin Center for Stem Cell and Regenerative Medicine, Zhejiang University, Hangzhou, P. R. China.
⁵ The Digital Health Institute, I.M Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia.
⁶ Novosibirsk State University, Novosibirsk, Russia.
⁷ Agrarian and Technological Institute, Peoples' Friendship University of Russia (RUDN), Moscow, Russia.
⁸ Institute of Hematology, Zhejiang University, Hangzhou, P. R. China.
⁹ Key Laboratory of Structural Biology of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou, Zhejiang Province, P. R. China.

^# Contributed equally.

Abstract

Background: Genetic regulation is known to contribute to the divergent expression of duplicate genes; however, little is known about how epigenetic modifications regulate the expression of duplicate genes in plants.

Methods: The histone modification (HM) profile patterns of different modes of gene duplication, including the whole genome duplication, proximal duplication, tandem duplication and transposed duplication were characterized based on ChIP-chip or ChIP-seq datasets. In this study, 10 distinct HM marks including H2Bub, H3K4me1, H3K4me2, H3K4me3, H3K9ac, H3K9me2, H3K27me1, H3K27me3, H3K36me3 and H3K14ac were analyzed. Moreover, the features of gene duplication with different HM patterns were characterized based on 88 RNA-seq datasets of Arabidopsis thaliana.

Results: This study showed that duplicate genes in Arabidopsis have a more similar HM pattern than single-copy genes in both their promoters and protein-coding regions. The evolution of HM marks is found to be coupled with coding sequence divergence and expression divergence after gene duplication. We found that functionally selective constraints may impose on epigenetic evolution after gene duplication. Furthermore, duplicate genes with distinct functions have more divergence in histone modification compared with the ones with the same function, while higher expression divergence is found with mutations of chromatin modifiers. This study shows the role of epigenetic marks in regulating gene expression and functional divergence after gene duplication in plants based on sequencing data.

Keywords: A. thaliana; Bioinformatics; ChIP-chip; Epigenetic pattern evolution; Gene duplication; Histone modifications; Plant genome; RNA-seq.

Grants and funding

This work was supported by the National Natural Sciences Foundation of China (Nos. 31371328, 31571366 and 31611130033), Science Technology Department of Zhejiang Province (No. 2015C32057), CSC & DAAD (PPP program No. 57136444), Jiangsu Collaborative Innovation Centre for Modern Crop Production, and the Fundamental Research Funds for the Central Universities (No. 2016FZA6001). This paper has been supported by the RUDN University Strategic Academic Leadership Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.