Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)

Abstract Background Silver arowana (Osteoglossum bicirrhosum) is a basal fish species with sexual monomorphism, while its sex determination mechanism has been poorly understood, posing a significant challenge to its captive breeding efforts. Results We constructed two high-quality chromosome-level g...

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Main Authors: Yi Liu, Chao Bian, Ka Yan Ma, Yexin Yang, Yuanyuan Wang, Chao Liu, Guochang Ouyang, Meng Xu, Jinhui Sun, Changwei Shao, Jiehu Chen, Qiong Shi, Xidong Mu
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-025-02139-5
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author Yi Liu
Chao Bian
Ka Yan Ma
Yexin Yang
Yuanyuan Wang
Chao Liu
Guochang Ouyang
Meng Xu
Jinhui Sun
Changwei Shao
Jiehu Chen
Qiong Shi
Xidong Mu
author_facet Yi Liu
Chao Bian
Ka Yan Ma
Yexin Yang
Yuanyuan Wang
Chao Liu
Guochang Ouyang
Meng Xu
Jinhui Sun
Changwei Shao
Jiehu Chen
Qiong Shi
Xidong Mu
author_sort Yi Liu
collection DOAJ
description Abstract Background Silver arowana (Osteoglossum bicirrhosum) is a basal fish species with sexual monomorphism, while its sex determination mechanism has been poorly understood, posing a significant challenge to its captive breeding efforts. Results We constructed two high-quality chromosome-level genome assemblies for both female and male silver arowana, with scaffold N50 values over 10 Mb. Combining re-sequencing data of 109 individuals, we identified a female-specific region, which was localized in a non-coding region, i.e., around 26-kb upstream of foxl2 gene (encoding forkhead box L2). Its strong interaction with the neighboring foxl2 on the same chromosome suggests foxl2 as a candidate sex-related gene in silver arowana. We subsequently propose a complex gene network in the sex determination process of silver arowana, with foxl2 acting as the central contributor. Transcriptome sequencing of gonads support our hypothesis that the regulation of foxl2 can be influenced by the spatial proximity of the female-specific fragment, thereby promoting ovarian function or inhibiting testicular function to stimulate gonadal differentiation. Furthermore, we found the sex chromosomes to be homomorphic with a potentially recent origin, as a linkage disequilibrium analysis proved minor recombination suppression. Conclusions These results taken together serve as a crucial foundation for conducting extensive investigations on the evolution and differentiation of sex-determining mechanisms, as well as the emergence and development of sex chromosomes in various fishes.
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institution Kabale University
issn 1741-7007
language English
publishDate 2025-01-01
publisher BMC
record_format Article
series BMC Biology
spelling doaj-art-dc995a98cddd47858bd377106eeaeda12025-02-02T12:42:37ZengBMCBMC Biology1741-70072025-01-0123111710.1186/s12915-025-02139-5Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)Yi Liu0Chao Bian1Ka Yan Ma2Yexin Yang3Yuanyuan Wang4Chao Liu5Guochang Ouyang6Meng Xu7Jinhui Sun8Changwei Shao9Jiehu Chen10Qiong Shi11Xidong Mu12Key Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesLaboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen UniversityState Key Laboratory of Biocontrol, School of Ecology, Sun Yat-Sen UniversityKey Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesCollege of Fisheries, Tianjin Agricultural UniversityKey Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and TechnologyScience Corporation of Gene (SCGene)Laboratory of Aquatic Genomics, College of Life Sciences and Oceanography, Shenzhen UniversityKey Laboratory of Prevention and Control for Aquatic Invasive Alien Species, Ministry of Agriculture and Rural Affairs, Guangdong Modern Recreational Fisheries Engineering Technology Center, Pearl River Fisheries Research Institute, Chinese Academy of Fishery SciencesAbstract Background Silver arowana (Osteoglossum bicirrhosum) is a basal fish species with sexual monomorphism, while its sex determination mechanism has been poorly understood, posing a significant challenge to its captive breeding efforts. Results We constructed two high-quality chromosome-level genome assemblies for both female and male silver arowana, with scaffold N50 values over 10 Mb. Combining re-sequencing data of 109 individuals, we identified a female-specific region, which was localized in a non-coding region, i.e., around 26-kb upstream of foxl2 gene (encoding forkhead box L2). Its strong interaction with the neighboring foxl2 on the same chromosome suggests foxl2 as a candidate sex-related gene in silver arowana. We subsequently propose a complex gene network in the sex determination process of silver arowana, with foxl2 acting as the central contributor. Transcriptome sequencing of gonads support our hypothesis that the regulation of foxl2 can be influenced by the spatial proximity of the female-specific fragment, thereby promoting ovarian function or inhibiting testicular function to stimulate gonadal differentiation. Furthermore, we found the sex chromosomes to be homomorphic with a potentially recent origin, as a linkage disequilibrium analysis proved minor recombination suppression. Conclusions These results taken together serve as a crucial foundation for conducting extensive investigations on the evolution and differentiation of sex-determining mechanisms, as well as the emergence and development of sex chromosomes in various fishes.https://doi.org/10.1186/s12915-025-02139-5Silver arowanaWhole-genome sequencing and assemblyChromosome interactionTranscriptomeFemale-specific regionfoxl2
spellingShingle Yi Liu
Chao Bian
Ka Yan Ma
Yexin Yang
Yuanyuan Wang
Chao Liu
Guochang Ouyang
Meng Xu
Jinhui Sun
Changwei Shao
Jiehu Chen
Qiong Shi
Xidong Mu
Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)
BMC Biology
Silver arowana
Whole-genome sequencing and assembly
Chromosome interaction
Transcriptome
Female-specific region
foxl2
title Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)
title_full Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)
title_fullStr Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)
title_full_unstemmed Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)
title_short Reference genome provide insights into sex determination of silver aworana (Osteoglossum bicirrhosum)
title_sort reference genome provide insights into sex determination of silver aworana osteoglossum bicirrhosum
topic Silver arowana
Whole-genome sequencing and assembly
Chromosome interaction
Transcriptome
Female-specific region
foxl2
url https://doi.org/10.1186/s12915-025-02139-5
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