DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development

被引:158
作者
He, Li [1 ]
Huang, Huan [1 ]
Bradai, Mariem [1 ]
Zhao, Cheng [1 ,2 ]
You, Yin [1 ,3 ]
Ma, Jun [1 ]
Zhao, Lun [1 ]
Lozano-Duran, Rosa [1 ,4 ]
Zhu, Jian-Kang [1 ,5 ,6 ]
机构
[1] Chinese Acad Sci, Shanghai Ctr Plant Stress Biol, Ctr Excellence Mol Plant Sci, Shanghai 201602, Peoples R China
[2] Karolinska Inst, Dept Clin Sci Intervent & Technol, S-14186 Stockholm, Sweden
[3] Univ Chinese Acad Sci, Beijing 100049, Peoples R China
[4] Eberhard Karls Univ Tubingen, Ctr Plant Mol Biol ZMBP, Dept Plant Biochem, D-72076 Tubingen, Germany
[5] Southern Univ Sci & Technol, Inst Adv Biotechnol, Shenzhen 518055, Peoples R China
[6] Southern Univ Sci & Technol, Sch Life Sci, Shenzhen 518055, Peoples R China
基金
中国国家自然科学基金;
关键词
EPIGENETIC INHERITANCE; CYTOSINE METHYLTRANSFERASE; TRANSPOSABLE ELEMENTS; CG METHYLATION; NONCODING RNA; CELL-CYCLE; PLANT; BINDING; RETROTRANSPOSITION; HETEROCHROMATIN;
D O I
10.1038/s41467-022-28940-2
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Our understanding of the extent of involvement of DNA methylation in genome-wide gene regulation and plant developmental control is incomplete. Here, the authors knock out all five known DNA methyltransferases and show the developmental and gene expression changes in the DNA methylation-free Arabidopsis plants. A contribution of DNA methylation to defense against invading nucleic acids and maintenance of genome integrity is uncontested; however, our understanding of the extent of involvement of this epigenetic mark in genome-wide gene regulation and plant developmental control is incomplete. Here, we knock out all five known DNA methyltransferases in Arabidopsis, generating DNA methylation-free plants. This quintuple mutant exhibits a suite of developmental defects, unequivocally demonstrating that DNA methylation is essential for multiple aspects of plant development. We show that CG methylation and non-CG methylation are required for a plethora of biological processes, including pavement cell shape, endoreduplication, cell death, flowering, trichome morphology, vasculature and meristem development, and root cell fate determination. Moreover, we find that DNA methylation has a strong dose-dependent effect on gene expression and repression of transposable elements. Taken together, our results demonstrate that DNA methylation is dispensable for Arabidopsis survival but essential for the proper regulation of multiple biological processes.
引用
收藏
页数:16
相关论文
共 117 条
[1]   HTSeq-a Python']Python framework to work with high-throughput sequencing data [J].
Anders, Simon ;
Pyl, Paul Theodor ;
Huber, Wolfgang .
BIOINFORMATICS, 2015, 31 (02) :166-169
[2]   Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana [J].
Baduel, Pierre ;
Leduque, Basile ;
Ignace, Amandine ;
Gy, Isabelle ;
Gil, Jose ;
Loudet, Olivier ;
Colot, Vincent ;
Quadrana, Leandro .
GENOME BIOLOGY, 2021, 22 (01)
[3]   Repbase Update, a database of repetitive elements in eukaryotic genomes [J].
Bao, Weidong ;
Kojima, Kenji K. ;
Kohany, Oleksiy .
MOBILE DNA, 2015, 6
[4]   SHORT INTERNODES/STYLISH genes, regulators of auxin biosynthesis, are involved in leaf vein development in Arabidopsis thaliana [J].
Baylis, Tammy ;
Cierlik, Izabela ;
Sundberg, Eva ;
Mattsson, Jim .
NEW PHYTOLOGIST, 2013, 197 (03) :737-750
[5]   On the origin and evolutionary consequences of gene body DNA methylation [J].
Bewick, Adam J. ;
Ji, Lexiang ;
Niederhuth, Chad E. ;
Willing, Eva-Maria ;
Hofmeister, Brigitte T. ;
Shi, Xiuling ;
Wang, Li ;
Lu, Zefu ;
Rohr, Nicholas A. ;
Hartwig, Benjamin ;
Kiefer, Christiane ;
Deal, Roger B. ;
Schmutz, Jeremy ;
Grimwood, Jane ;
Stroud, Hume ;
Jacobsen, Steven E. ;
Schneeberger, Korbinian ;
Zhang, Xiaoyu ;
Schmitz, Robert J. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2016, 113 (32) :9111-9116
[6]   Trimmomatic: a flexible trimmer for Illumina sequence data [J].
Bolger, Anthony M. ;
Lohse, Marc ;
Usadel, Bjoern .
BIOINFORMATICS, 2014, 30 (15) :2114-2120
[7]   Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana [J].
Bond, Donna M. ;
Baulcombe, David C. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (03) :917-922
[8]   Small RNAs and heritable epigenetic variation in plants [J].
Bond, Donna M. ;
Baulcombe, David C. .
TRENDS IN CELL BIOLOGY, 2014, 24 (02) :100-107
[9]   The expanding world of small RNAs in plants [J].
Borges, Filipe ;
Martienssen, Robert A. .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2015, 16 (12) :727-741
[10]   DNA methylation dynamics during early plant life [J].
Bouyer, Daniel ;
Kramdi, Amira ;
Kassam, Mohamed ;
Heese, Maren ;
Schnittger, Arp ;
Roudier, Francois ;
Colot, Vincent .
GENOME BIOLOGY, 2017, 18