Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)

The increasing sea temperature caused by global warming has resulted in severe mortalities in maricultural scallops. Therefore, improving thermal tolerance has become an active research area in the scallop farming industry. Bay scallop (Argopecten irradians irradians) was introduced into China in 19...

Full description

Bibliographic Details
Main Authors: Xinghai Zhu, Pingping Liu, Xiujiang Hou, Junhao Zhang, Jia Lv, Wei Lu, Qifan Zeng, Xiaoting Huang, Qiang Xing, Zhenmin Bao
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2021.650045/full
_version_ 1818922345531703296
author Xinghai Zhu
Pingping Liu
Xiujiang Hou
Junhao Zhang
Jia Lv
Wei Lu
Qifan Zeng
Xiaoting Huang
Xiaoting Huang
Qiang Xing
Qiang Xing
Zhenmin Bao
Zhenmin Bao
author_facet Xinghai Zhu
Pingping Liu
Xiujiang Hou
Junhao Zhang
Jia Lv
Wei Lu
Qifan Zeng
Xiaoting Huang
Xiaoting Huang
Qiang Xing
Qiang Xing
Zhenmin Bao
Zhenmin Bao
author_sort Xinghai Zhu
collection DOAJ
description The increasing sea temperature caused by global warming has resulted in severe mortalities in maricultural scallops. Therefore, improving thermal tolerance has become an active research area in the scallop farming industry. Bay scallop (Argopecten irradians irradians) was introduced into China in 1982 and has developed into a vast aquaculture industry in northern China. To date, genetic studies on thermal tolerance in bay scallops are limited, and no systematic screening of thermal tolerance-related loci or genes has been conducted in this species. In the present study, we conducted a genome-wide association study (GWAS) for thermal tolerance using the Arrhenius break temperature (ABT) indicators of 435 bay scallops and 38,011 single nucleotide polymorphism (SNP) markers. The GWAS identified 1,906 significant thermal tolerance-associated SNPs located in 16 chromosomes of bay scallop. Gene ontology and Kyoto Encyclopedia of Genes and Genomes pathway analyses showed that 638 genes were enriched in 42 GO terms, while 549 annotated genes were enriched in aggregation pathways. Additionally, the SNP (15-5091-20379557-1) with the lowest P value was located in the transcriptional coactivator p15 (PC4) gene, which is involved in regulating DNA damage repair and stabilizing genome functions. Further analysis in another population identified two new thermal tolerance-associated SNPs in the first coding sequence of PC4 in bay scallops (AiPC4). Moreover, AiPC4 expression levels were significantly correlated (r = 0.675–0.962; P < 0.05) with the ABT values of the examined bay scallops. Our data suggest that AiPC4 might be a positive regulator of thermal tolerance and a potential candidate gene for molecular breeding in bay scallop aiming at thermal tolerance improvement.
first_indexed 2024-12-20T01:52:04Z
format Article
id doaj.art-e086218980894d13a4c21c3382b55baf
institution Directory Open Access Journal
issn 1664-8021
language English
last_indexed 2024-12-20T01:52:04Z
publishDate 2021-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Genetics
spelling doaj.art-e086218980894d13a4c21c3382b55baf2022-12-21T19:57:37ZengFrontiers Media S.A.Frontiers in Genetics1664-80212021-07-011210.3389/fgene.2021.650045650045Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)Xinghai Zhu0Pingping Liu1Xiujiang Hou2Junhao Zhang3Jia Lv4Wei Lu5Qifan Zeng6Xiaoting Huang7Xiaoting Huang8Qiang Xing9Qiang Xing10Zhenmin Bao11Zhenmin Bao12MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaMOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, ChinaLaboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaThe increasing sea temperature caused by global warming has resulted in severe mortalities in maricultural scallops. Therefore, improving thermal tolerance has become an active research area in the scallop farming industry. Bay scallop (Argopecten irradians irradians) was introduced into China in 1982 and has developed into a vast aquaculture industry in northern China. To date, genetic studies on thermal tolerance in bay scallops are limited, and no systematic screening of thermal tolerance-related loci or genes has been conducted in this species. In the present study, we conducted a genome-wide association study (GWAS) for thermal tolerance using the Arrhenius break temperature (ABT) indicators of 435 bay scallops and 38,011 single nucleotide polymorphism (SNP) markers. The GWAS identified 1,906 significant thermal tolerance-associated SNPs located in 16 chromosomes of bay scallop. Gene ontology and Kyoto Encyclopedia of Genes and Genomes pathway analyses showed that 638 genes were enriched in 42 GO terms, while 549 annotated genes were enriched in aggregation pathways. Additionally, the SNP (15-5091-20379557-1) with the lowest P value was located in the transcriptional coactivator p15 (PC4) gene, which is involved in regulating DNA damage repair and stabilizing genome functions. Further analysis in another population identified two new thermal tolerance-associated SNPs in the first coding sequence of PC4 in bay scallops (AiPC4). Moreover, AiPC4 expression levels were significantly correlated (r = 0.675–0.962; P < 0.05) with the ABT values of the examined bay scallops. Our data suggest that AiPC4 might be a positive regulator of thermal tolerance and a potential candidate gene for molecular breeding in bay scallop aiming at thermal tolerance improvement.https://www.frontiersin.org/articles/10.3389/fgene.2021.650045/fullgenome-wide association studyArgopecten irradians irradiansthermal tolerancesingle nucleotide polymorphismtranscriptional coactivator p15
spellingShingle Xinghai Zhu
Pingping Liu
Xiujiang Hou
Junhao Zhang
Jia Lv
Wei Lu
Qifan Zeng
Xiaoting Huang
Xiaoting Huang
Qiang Xing
Qiang Xing
Zhenmin Bao
Zhenmin Bao
Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)
Frontiers in Genetics
genome-wide association study
Argopecten irradians irradians
thermal tolerance
single nucleotide polymorphism
transcriptional coactivator p15
title Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)
title_full Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)
title_fullStr Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)
title_full_unstemmed Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)
title_short Genome-Wide Association Study Reveals PC4 as the Candidate Gene for Thermal Tolerance in Bay Scallop (Argopecten irradians irradians)
title_sort genome wide association study reveals pc4 as the candidate gene for thermal tolerance in bay scallop argopecten irradians irradians
topic genome-wide association study
Argopecten irradians irradians
thermal tolerance
single nucleotide polymorphism
transcriptional coactivator p15
url https://www.frontiersin.org/articles/10.3389/fgene.2021.650045/full
work_keys_str_mv AT xinghaizhu genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT pingpingliu genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT xiujianghou genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT junhaozhang genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT jialv genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT weilu genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT qifanzeng genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT xiaotinghuang genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT xiaotinghuang genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT qiangxing genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT qiangxing genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT zhenminbao genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians
AT zhenminbao genomewideassociationstudyrevealspc4asthecandidategeneforthermaltoleranceinbayscallopargopectenirradiansirradians