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

Chromatin / genetics Transcription Factors / genetics Ovule / genetics Gene Regulatory Networks Deoxyribonuclease I / genetics
Cis-regulatory DNA elements Cotton fiber DNase-seq Network Transcription factors

Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
31 07 2023
Historique:
received: 24 11 2022
accepted: 18 07 2023
medline: 3 8 2023
pubmed: 1 8 2023
entrez: 31 7 2023
Statut: epublish

Résumé

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. 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. 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.

Sections du résumé

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.

Identifiants

DOI: 10.1186/s12915-023-01665-4 PMID: 37525156 PMC: PMC10391996
pubmed: 37525156
doi: 10.1186/s12915-023-01665-4
pii: 10.1186/s12915-023-01665-4
pmc: PMC10391996
doi:

Substances chimiques

Chromatin 0
Transcription Factors 0
di-n-hexyl sulfosuccinate 1CYC51DFL6
Deoxyribonuclease I EC 3.1.21.1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

165

Informations de copyright

© 2023. The Author(s).

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Auteurs

Yu Bao (Y)

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.
Anyang Institute of Technology, Anyang, Henan, 455000, China.
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.

Yangyang Wei (Y)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Yuling Liu (Y)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Jingjing Gao (J)

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.

Shuang Cheng (S)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Zhengzhou University, Zhengzhou, Henan, 450001, China.

Guanqing Liu (G)

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.
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.

Qi You (Q)

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.
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.

Peng Liu (P)

Institutes of Agricultural Science and Technology Development, Joint International Research Laboratory of Agriculture and Agri-Product Safety, Yangzhou University, Yangzhou, 225009, China.

Quanwei Lu (Q)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Pengtao Li (P)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Shulin Zhang (S)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Nan Hu (N)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Yangshuo Han (Y)

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.
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.

Shuo Liu (S)

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.
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.

Yuechao Wu (Y)

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.
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.

Qingqing Yang (Q)

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.
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.

Zhaoguo Li (Z)

Anyang Institute of Technology, Anyang, Henan, 455000, China.
Zhengzhou University, Zhengzhou, Henan, 450001, China.

Guowei Ao (G)

Anyang Institute of Technology, Anyang, Henan, 455000, China.

Fang Liu (F)

Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Kunbo Wang (K)

Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China.

Jiming Jiang (J)

Department of Plant Biology, Michigan State University, East Lansing, MI, USA.
Department of Horticulture, Michigan State University, East Lansing, MI, USA.
Michigan State University AgBioResearch, East Lansing, MI, USA.

Tao Zhang (T)

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.
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.
ORCID: 0000-0002-7897-0205

Wenli Zhang (W)

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.

Renhai Peng (R)

Anyang Institute of Technology, Anyang, Henan, 455000, China. aydxprh@163.com.
Research Base, Anyang Institute of Technology, State Key Laboratory of Cotton Biology, Anyang, Henan, 455000, China. aydxprh@163.com.
Zhengzhou University, Zhengzhou, Henan, 450001, China. aydxprh@163.com.

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Classifications MeSH

questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Structures de chromosome › Chromatine › Genome-wide chromatin accessibility landscape...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Genome-wide chromatin accessibility landscape...
questionsmedicales.fr › Structures de plante › Parties aériennes de plante › Sommités fleuries › Fleurs › Cellules germinales de plante › Ovule (botanique) › Genome-wide chromatin accessibility landscape...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Séquences d'acides nucléiques régulatrices › Réseaux de régulation génique › Genome-wide chromatin accessibility landscape...
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Esterases › Désoxyribonucléases › Deoxyribonuclease I › Genome-wide chromatin accessibility landscape...