Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison

IntroductionCompared to mammals and birds, sex-determining genes differ in most fish species. Largemouth bass (Micropterus Salmoides) is one of the most important cultured fish species in China, and there are growth differences between males and females. However, its sex-determining genes and mechan...

Full description

Saved in:
Bibliographic Details
Main Authors: Xinhui Zhang, Junjian Dong, Zhiqiang Ruan, Fengying Gao, Wenchuan Zhou, Xinxin You, Jieming Chen, Qiong Shi, Xing Ye, Chengfei Sun
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2025.1586534/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850185089959329792
author Xinhui Zhang
Xinhui Zhang
Xinhui Zhang
Junjian Dong
Zhiqiang Ruan
Fengying Gao
Wenchuan Zhou
Xinxin You
Jieming Chen
Qiong Shi
Qiong Shi
Xing Ye
Chengfei Sun
author_facet Xinhui Zhang
Xinhui Zhang
Xinhui Zhang
Junjian Dong
Zhiqiang Ruan
Fengying Gao
Wenchuan Zhou
Xinxin You
Jieming Chen
Qiong Shi
Qiong Shi
Xing Ye
Chengfei Sun
author_sort Xinhui Zhang
collection DOAJ
description IntroductionCompared to mammals and birds, sex-determining genes differ in most fish species. Largemouth bass (Micropterus Salmoides) is one of the most important cultured fish species in China, and there are growth differences between males and females. However, its sex-determining genes and mechanisms currently remain unknown.MethodsWe explored the sex-determination mechanism by integrating whole-genome sequencing, resequencing and comparative genomics approaches.ResultsIn this study, we employed HiFi and Hi-C sequencing technologies to construct a chromosome-level haplotypic genome assembly for male largemouth bass, with a genome size of 875.69 Mb. The assembled genome contains 23 chromosomes, covering 95.31% of the complete sequences with a high scaffold N50 of 35.93 Mb. A genome-wide association study (GWAS) of sex was performed with four populations consisting of 62 males and 58 females. For the sex trait, a total of 3,838 SNP loci were identified to be significantly associated with sexual discrepancy. Interestingly, almost all these significant SNPs (3,825) were clustered on chromosome 10 (Chr10), within a 3.5-Mb sex-determination region (SDR). They were homozygous in females while heterozygous in males. We therefore speculate that largemouth bass owns a XX/XY sex determination system. By comparing genomics data and examining coverage depth of resequencing reads, we revealed a ~51-kb male-specific region (MSR) on Chr10. Gene annotation discovered a coding sequence (msy) within MSR-1, which may contribute to sex determination of largemouth bass. By differential expression analysis, two candidate sex-determining genes (ccdc103 and jockey) were predicted within the target SDR. Moreover, we applied two male-specific non-coding fragments (within MSR-2 and MSR-3) to design specific sex markers, successfully obtaining universal gender identity in examined largemouth bass.DiscussionOverall, our findings improve our understanding of the molecular basis for sex determination in largemouth bass, which will thereby promote the mono-sexual breeding progress in the aquaculture industry.
format Article
id doaj-art-5bcc3c75700d4b1c8ba06e6448010378
institution OA Journals
issn 2296-7745
language English
publishDate 2025-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Marine Science
spelling doaj-art-5bcc3c75700d4b1c8ba06e64480103782025-08-20T02:16:50ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452025-05-011210.3389/fmars.2025.15865341586534Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparisonXinhui Zhang0Xinhui Zhang1Xinhui Zhang2Junjian Dong3Zhiqiang Ruan4Fengying Gao5Wenchuan Zhou6Xinxin You7Jieming Chen8Qiong Shi9Qiong Shi10Xing Ye11Chengfei Sun12Key Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaCollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaShenzhen Ocean Development Promotion Center, Shenzhen, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen, ChinaCollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen, ChinaShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI Marine, Shenzhen, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, ChinaIntroductionCompared to mammals and birds, sex-determining genes differ in most fish species. Largemouth bass (Micropterus Salmoides) is one of the most important cultured fish species in China, and there are growth differences between males and females. However, its sex-determining genes and mechanisms currently remain unknown.MethodsWe explored the sex-determination mechanism by integrating whole-genome sequencing, resequencing and comparative genomics approaches.ResultsIn this study, we employed HiFi and Hi-C sequencing technologies to construct a chromosome-level haplotypic genome assembly for male largemouth bass, with a genome size of 875.69 Mb. The assembled genome contains 23 chromosomes, covering 95.31% of the complete sequences with a high scaffold N50 of 35.93 Mb. A genome-wide association study (GWAS) of sex was performed with four populations consisting of 62 males and 58 females. For the sex trait, a total of 3,838 SNP loci were identified to be significantly associated with sexual discrepancy. Interestingly, almost all these significant SNPs (3,825) were clustered on chromosome 10 (Chr10), within a 3.5-Mb sex-determination region (SDR). They were homozygous in females while heterozygous in males. We therefore speculate that largemouth bass owns a XX/XY sex determination system. By comparing genomics data and examining coverage depth of resequencing reads, we revealed a ~51-kb male-specific region (MSR) on Chr10. Gene annotation discovered a coding sequence (msy) within MSR-1, which may contribute to sex determination of largemouth bass. By differential expression analysis, two candidate sex-determining genes (ccdc103 and jockey) were predicted within the target SDR. Moreover, we applied two male-specific non-coding fragments (within MSR-2 and MSR-3) to design specific sex markers, successfully obtaining universal gender identity in examined largemouth bass.DiscussionOverall, our findings improve our understanding of the molecular basis for sex determination in largemouth bass, which will thereby promote the mono-sexual breeding progress in the aquaculture industry.https://www.frontiersin.org/articles/10.3389/fmars.2025.1586534/fulllargemouth bass (Micropterus salmoides)chromosome-level genome assemblyGWASmale-specific regionsex markers
spellingShingle Xinhui Zhang
Xinhui Zhang
Xinhui Zhang
Junjian Dong
Zhiqiang Ruan
Fengying Gao
Wenchuan Zhou
Xinxin You
Jieming Chen
Qiong Shi
Qiong Shi
Xing Ye
Chengfei Sun
Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison
Frontiers in Marine Science
largemouth bass (Micropterus salmoides)
chromosome-level genome assembly
GWAS
male-specific region
sex markers
title Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison
title_full Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison
title_fullStr Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison
title_full_unstemmed Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison
title_short Identification and characterization of a male-specific region in largemouth bass (Micropterus Salmoides) by whole-genome sequencing, resequencing and genomics comparison
title_sort identification and characterization of a male specific region in largemouth bass micropterus salmoides by whole genome sequencing resequencing and genomics comparison
topic largemouth bass (Micropterus salmoides)
chromosome-level genome assembly
GWAS
male-specific region
sex markers
url https://www.frontiersin.org/articles/10.3389/fmars.2025.1586534/full
work_keys_str_mv AT xinhuizhang identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT xinhuizhang identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT xinhuizhang identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT junjiandong identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT zhiqiangruan identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT fengyinggao identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT wenchuanzhou identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT xinxinyou identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT jiemingchen identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT qiongshi identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT qiongshi identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT xingye identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison
AT chengfeisun identificationandcharacterizationofamalespecificregioninlargemouthbassmicropterussalmoidesbywholegenomesequencingresequencingandgenomicscomparison