Genome-wide chromatin accessibility landscape and dynamics of transcription factor networks during ovule and fiber development in cotton

Yu Bao; Yangyang Wei; Yuling Liu; Jingjing Gao; Shuang Cheng; Guanqing Liu; Qi You; Peng Liu; Quanwei Lu; Pengtao Li; Shulin Zhang; Nan Hu; Yangshuo Han; Shuo Liu; Yuechao Wu; Qingqing Yang; Zhaoguo Li; Guowei Ao; Fang Liu; Kunbo Wang; Jiming Jiang; Tao Zhang; Wenli Zhang; Renhai Peng

doi:10.1186/s12915-023-01665-4

Genome-wide chromatin accessibility landscape and dynamics of transcription factor networks during ovule and fiber development in cotton

BMC Biol. 2023 Jul 31;21(1):165. doi: 10.1186/s12915-023-01665-4.

Authors

Yu Bao^#^{1

2

3}, Yangyang Wei^#^{2

4}, Yuling Liu^#^{2

4}, Jingjing Gao⁵, Shuang Cheng^{2

6}, Guanqing Liu^{1

3}, Qi You^{1

3}, Peng Liu⁷, Quanwei Lu^{2

4}, Pengtao Li^{2

4}, Shulin Zhang^{2

4}, Nan Hu^{2

4}, Yangshuo Han^{1

3}, Shuo Liu^{1

3}, Yuechao Wu^{1

3}, Qingqing Yang^{1

3}, Zhaoguo Li^{2

6}, Guowei Ao², Fang Liu⁴, Kunbo Wang⁴, Jiming Jiang^{8

9

10}, Tao Zhang^{11

12}, Wenli Zhang¹³, Renhai Peng^{14

15

16}

Affiliations

¹ Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Jiangsu Key Laboratory of Crop Genetics and Physiology/Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College of Yangzhou University, Yangzhou, 225009, China.
² Anyang Institute of Technology, Anyang, Henan, 455000, China.
³ Key Laboratory of Plant Functional Genomics of the Ministry of Education/Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China.
⁴ Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.
⁵ National Key Laboratory for Crop Genetics and Germplasm Enhancement and Utilization, Collaborative Innovation Center for Modern Crop Production Co-Sponsored By Province and Ministry (CIC-MCP), Nanjing Agricultural University, No.1 Weigang, Nanjing, 210095, Jiangsu, China.
⁶ Zhengzhou University, Zhengzhou, Henan, 450001, China.
⁷ Institutes of Agricultural Science and Technology Development, Joint International Research Laboratory of Agriculture and Agri-Product Safety, Yangzhou University, Yangzhou, 225009, China.
⁸ Department of Plant Biology, Michigan State University, East Lansing, MI, USA.
⁹ Department of Horticulture, Michigan State University, East Lansing, MI, USA.
¹⁰ Michigan State University AgBioResearch, East Lansing, MI, USA.
¹¹ Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Jiangsu Key Laboratory of Crop Genetics and Physiology/Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College of Yangzhou University, Yangzhou, 225009, China. zhangtao@yzu.edu.cn.
¹² Key Laboratory of Plant Functional Genomics of the Ministry of Education/Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education of China, Yangzhou University, Yangzhou, 225009, China. zhangtao@yzu.edu.cn.
¹³ National Key Laboratory for Crop Genetics and Germplasm Enhancement and Utilization, Collaborative Innovation Center for Modern Crop Production Co-Sponsored By Province and Ministry (CIC-MCP), Nanjing Agricultural University, No.1 Weigang, Nanjing, 210095, Jiangsu, China. wzhang25@njau.edu.cn.
¹⁴ Anyang Institute of Technology, Anyang, Henan, 455000, China. aydxprh@163.com.
¹⁵ Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China. aydxprh@163.com.
¹⁶ Zhengzhou University, Zhengzhou, Henan, 450001, China. aydxprh@163.com.

^# Contributed equally.

Abstract

Background: The development of cotton fiber is regulated by the orchestrated binding of regulatory proteins to cis-regulatory elements associated with developmental genes. The cis-trans regulatory dynamics occurred throughout the course of cotton fiber development are elusive. Here we generated genome-wide high-resolution DNase I hypersensitive sites (DHSs) maps to understand the regulatory mechanisms of cotton ovule and fiber development.

Results: We generated DNase I hypersensitive site (DHS) profiles from cotton ovules at 0 and 3 days post anthesis (DPA) and fibers at 8, 12, 15, and 18 DPA. We obtained a total of 1185 million reads and identified a total of 199,351 DHSs through ~ 30% unique mapping reads. It should be noted that more than half of DNase-seq reads mapped multiple genome locations and were not analyzed in order to achieve a high specificity of peak profile and to avoid bias from repetitive genomic regions. Distinct chromatin accessibilities were observed in the ovules (0 and 3 DPA) compared to the fiber elongation stages (8, 12, 15, and 18 DPA). Besides, the chromatin accessibility during ovules was particularly elevated in genomic regions enriched with transposable elements (TEs) and genes in TE-enriched regions were involved in ovule cell division. We analyzed cis-regulatory modules and revealed the influence of hormones on fiber development from the regulatory divergence of transcription factor (TF) motifs. Finally, we constructed a reliable regulatory network of TFs related to ovule and fiber development based on chromatin accessibility and gene co-expression network. From this network, we discovered a novel TF, WRKY46, which may shape fiber development by regulating the lignin content.

Conclusions: Our results not only reveal the contribution of TEs in fiber development, but also predict and validate the TFs related to fiber development, which will benefit the research of cotton fiber molecular breeding.

Keywords: Cis-regulatory DNA elements; Cotton fiber; DNase-seq; Network; Transcription factors.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Chromatin* / genetics
Deoxyribonuclease I / genetics
Gene Regulatory Networks
Ovule / genetics
Ovule / metabolism
Transcription Factors* / genetics
Transcription Factors* / metabolism

Substances

Chromatin
Transcription Factors
di-n-hexyl sulfosuccinate
Deoxyribonuclease I