Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis

Zhaoying Shi; Jinsheng Xu; Longjian Niu; Wei Shen; Shuting Yan; Yongjun Tan; Xuebo Quan; Edwin Cheung; Kai Huang; Yonglong Chen; Li Li; Chunhui Hou

doi:10.1016/j.celrep.2023.112151

Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis

Cell Rep. 2023 Mar 28;42(3):112151. doi: 10.1016/j.celrep.2023.112151. Epub 2023 Feb 22.

Authors

Zhaoying Shi¹, Jinsheng Xu², Longjian Niu³, Wei Shen², Shuting Yan⁴, Yongjun Tan⁵, Xuebo Quan⁴, Edwin Cheung⁶, Kai Huang⁷, Yonglong Chen⁸, Li Li⁹, Chunhui Hou¹⁰

Affiliations

¹ Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China.
² Department of Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China; Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China.
³ China State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; School of Public Health and Emergency Management, Southern University of Science and Technology, Shenzhen 518055, China; Shenzhen Key Laboratory of Cardiovascular Health and Precision Medicine, Southern University of Science and Technology, Shenzhen 518055, China.
⁴ Institute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen 518132, China.
⁵ Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China; China State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
⁶ Cancer Centre, Faculty of Health Sciences, University of Macau, Taipa, Macau 999078, China; Frontier Science Centre for Precision Oncology of Ministry of Education, University of Macau, Taipa, Macau 999078, China.
⁷ Institute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen 518132, China. Electronic address: huangkai@szbl.ac.cn.
⁸ Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China. Electronic address: chenyl@sustech.edu.cn.
⁹ Department of Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China; Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China. Electronic address: li.li@hzau.edu.cn.
¹⁰ China State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China. Electronic address: houchunhui@mail.kiz.ac.cn.

PMID: 36827186
DOI: 10.1016/j.celrep.2023.112151

Abstract

Transposable elements (TEs) are abundant in metazoan genomes and have multifaceted effects on host fitness. However, the mechanisms underlying the functions of TEs are still not fully understood. Here, we combine Hi-C, ATAC-seq, and ChIP-seq assays to report the existence of multimegabase supersized loop (SSL) clusters in the Xenopus tropicalis sperm. We show that SSL anchors are inaccessible and devoid of the architectural protein CTCF, RNA polymerase II, and modified histones. Nearly all SSL anchors are marked by Helitrons, a class II DNA transposon. Molecular dynamics simulations indicate that SSL clusters are likely formed via a molecular agent-mediated chromatin condensation process. However, only slightly more SSL anchor-associated genes are expressed at late embryo development stages, suggesting that SSL anchors might only function in sperm. Our work shows an evolutionarily distinct and sperm-specific genome structure marked by a subset of Helitrons, whose establishment and function remain to be explored.

Keywords: CP: Molecular biology; Helitrons; Xenopus tropicalis; gene repression; sperm; supersized loop cluster; three-dimensional genome organization; transposable element; transposition repression.

Publication types

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

MeSH terms

Animals
Chromatin / genetics
DNA Transposable Elements* / genetics
Histones / genetics
Male
Semen*
Xenopus / genetics

Substances

DNA Transposable Elements
Histones
Chromatin