DRN facilitates WUS transcriptional regulatory activity by chromatin remodeling to regulate shoot stem cell homeostasis in Arabidopsis

Linjie Luo; Li Liu; Lili She; Haoran Zhang; Nannan Zhang; Yaqin Wang; Yuting Ni; Fugui Chen; Fengying Wan; Yuqiu Dai; Guoping Zhu; Zhong Zhao

doi:10.1371/journal.pbio.3002878

DRN facilitates WUS transcriptional regulatory activity by chromatin remodeling to regulate shoot stem cell homeostasis in Arabidopsis

PLoS Biol. 2024 Nov 8;22(11):e3002878. doi: 10.1371/journal.pbio.3002878. eCollection 2024 Nov.

Authors

Linjie Luo¹, Li Liu¹, Lili She¹, Haoran Zhang¹, Nannan Zhang¹, Yaqin Wang¹, Yuting Ni¹, Fugui Chen¹, Fengying Wan¹, Yuqiu Dai², Guoping Zhu¹, Zhong Zhao²

Affiliations

¹ Anhui Provincial Key Laboratory of Molecular Enzymology and Mechanism of Major Metabolic Diseases, Anhui Provincial Engineering Research Centre for Molecular Detection and Diagnostics, College of Life Sciences, Anhui Normal University, Wuhu, China.
² CAS Center for Excellence in Molecular Plant Sciences, MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, China.

Abstract

Shoot stem cells, harbored in the shoot apical meristem (SAM), play key roles during post-embryonic development of Arabidopsis and function as the origin of plant aerial tissues. Multiple transcription factors are involved in the sophisticated transcriptional regulation of stem cell homeostasis, with the WUSCHEL (WUS)/CLAVATA3 (CLV3) negative feedback loop playing a central role. WUS acts as a master regulator in maintaining stem cells through its transcriptional regulatory activity including repressive and activating abilities. Although the interaction between WUS and TOPLESS confers the repressive activity of WUS in transcriptional control, the mechanism by which WUS activates gene expression remains elusive. Here, we showed that DORNRÖSCHEN competitively interacts with WUS and disturbs the WUS homodimer, which recruits BRAHMA to activate CLV3 expression via nucleosome depletion for maintaining the stem cell pool.

Copyright: © 2024 Luo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

MeSH terms

Adenosine Triphosphatases
Arabidopsis Proteins* / genetics
Arabidopsis Proteins* / metabolism
Arabidopsis* / genetics
Arabidopsis* / metabolism
Chromatin Assembly and Disassembly*
Gene Expression Regulation, Plant*
Homeodomain Proteins* / genetics
Homeodomain Proteins* / metabolism
Homeostasis*
Meristem / genetics
Meristem / metabolism
Nucleosomes / metabolism
Plant Shoots / genetics
Plant Shoots / metabolism
Stem Cells* / metabolism
Transcription Factors* / genetics
Transcription Factors* / metabolism

Substances

Arabidopsis Proteins
WUSCHEL protein, Arabidopsis
Homeodomain Proteins
Transcription Factors
BRM protein, Arabidopsis
Nucleosomes
Adenosine Triphosphatases

Grants and funding

The study design, data collection, and analysis were funded by the National Natural Science Foundation of China (https://www.nsfc.gov.cn/) with grants 31900624 to L. Luo, 32071270 to G. Z., and 32130009 to Z. Z.. Additionally, the Natural Science Foundation of Anhui Province of China (http://kjt.ah.gov.cn/) provided support for study design, data collection, and analysis with grant 1908085QC91 to L. Luo. Data collection and analysis were also supported by the Major Science and Technology Projects in Anhui Province (http://kjt.ah.gov.cn/) with grant 202003a06020009 to G. Z.. The preparation and publication fees of the manuscript were supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (https://www.cas.cn/) with grant XDB27030105 to Z. Z., and by the Outstanding Innovative Research Team for Molecular Enzymology and Detection in Anhui Provincial Universities (https://www.ahnu.edu.cn/) with grant 2022AH010012 to G. Z.. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.