Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters

Many marine ectotherms, especially those inhabiting highly variable intertidal zones, develop high phenotypic plasticity in response to rapid climate change by modulating gene expression levels. Herein, we examined the regulatory architecture of heat-responsive gene expression plasticity in oysters...

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Main Authors: Kexin Zhang, Jinpeng Wang, Fangfang Ding, Ruihui Shi, Wei Wang, Guofan Zhang, Li Li
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/7/1040
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spelling doaj-bbd726e83c5447fdb7db1b5fc955f7d32021-07-23T13:41:54ZengMDPI AGGenes2073-44252021-07-01121040104010.3390/genes12071040Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in OystersKexin Zhang0Jinpeng Wang1Fangfang Ding2Ruihui Shi3Wei Wang4Guofan Zhang5Li Li6CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaCAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, ChinaMany marine ectotherms, especially those inhabiting highly variable intertidal zones, develop high phenotypic plasticity in response to rapid climate change by modulating gene expression levels. Herein, we examined the regulatory architecture of heat-responsive gene expression plasticity in oysters using expression quantitative trait loci (eQTL) analysis. Using a backcross family of <i>Crassostrea gigas</i> and its sister species <i>Crassostrea angulat</i><i>a</i> under acute stress, 56 distant regulatory regions accounting for 6–26.6% of the gene expression variation were identified for 19 heat-responsive genes. In total, 831 genes and 164 single nucleotide polymorphisms (SNPs) that could potentially regulate expression of the target genes were screened in the eQTL region. The association between three SNPs and the corresponding target genes was verified in an independent family. Specifically, Marker13973 was identified for heat shock protein (HSP) family A member 9 (<i>HspA9</i>). Ribosomal protein L10a (<i>RPL10A</i>) was detected approximately 2 kb downstream of the distant regulatory SNP. Further, Marker14346-48 and Marker14346-85 were in complete linkage disequilibrium and identified for autophagy-related gene 7 (<i>ATG7</i>). Nuclear respiratory factor 1 (<i>NRF1</i>) was detected approximately 3 kb upstream of the two SNPs. These results suggested regulatory relationships between <i>RPL10A</i> and <i>HSPA9</i> and between <i>NRF1</i> and <i>ATG7</i>. Our findings indicate that distant regulatory mutations play an important role in the regulation of gene expression plasticity by altering upstream regulatory factors in response to heat stress. The identified eQTLs provide candidate biomarkers for predicting the persistence of oysters under future climate change scenarios.https://www.mdpi.com/2073-4425/12/7/1040oysterthermal adaptionheat-responsive geneexpression quantitative trait loci (eQTL) mappingdistant regulatory locus
collection DOAJ
language English
format Article
sources DOAJ
author Kexin Zhang
Jinpeng Wang
Fangfang Ding
Ruihui Shi
Wei Wang
Guofan Zhang
Li Li
spellingShingle Kexin Zhang
Jinpeng Wang
Fangfang Ding
Ruihui Shi
Wei Wang
Guofan Zhang
Li Li
Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters
Genes
oyster
thermal adaption
heat-responsive gene
expression quantitative trait loci (eQTL) mapping
distant regulatory locus
author_facet Kexin Zhang
Jinpeng Wang
Fangfang Ding
Ruihui Shi
Wei Wang
Guofan Zhang
Li Li
author_sort Kexin Zhang
title Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters
title_short Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters
title_full Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters
title_fullStr Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters
title_full_unstemmed Identification of Distant Regulatory Elements Using Expression Quantitative Trait Loci Mapping for Heat-Responsive Genes in Oysters
title_sort identification of distant regulatory elements using expression quantitative trait loci mapping for heat-responsive genes in oysters
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2021-07-01
description Many marine ectotherms, especially those inhabiting highly variable intertidal zones, develop high phenotypic plasticity in response to rapid climate change by modulating gene expression levels. Herein, we examined the regulatory architecture of heat-responsive gene expression plasticity in oysters using expression quantitative trait loci (eQTL) analysis. Using a backcross family of <i>Crassostrea gigas</i> and its sister species <i>Crassostrea angulat</i><i>a</i> under acute stress, 56 distant regulatory regions accounting for 6–26.6% of the gene expression variation were identified for 19 heat-responsive genes. In total, 831 genes and 164 single nucleotide polymorphisms (SNPs) that could potentially regulate expression of the target genes were screened in the eQTL region. The association between three SNPs and the corresponding target genes was verified in an independent family. Specifically, Marker13973 was identified for heat shock protein (HSP) family A member 9 (<i>HspA9</i>). Ribosomal protein L10a (<i>RPL10A</i>) was detected approximately 2 kb downstream of the distant regulatory SNP. Further, Marker14346-48 and Marker14346-85 were in complete linkage disequilibrium and identified for autophagy-related gene 7 (<i>ATG7</i>). Nuclear respiratory factor 1 (<i>NRF1</i>) was detected approximately 3 kb upstream of the two SNPs. These results suggested regulatory relationships between <i>RPL10A</i> and <i>HSPA9</i> and between <i>NRF1</i> and <i>ATG7</i>. Our findings indicate that distant regulatory mutations play an important role in the regulation of gene expression plasticity by altering upstream regulatory factors in response to heat stress. The identified eQTLs provide candidate biomarkers for predicting the persistence of oysters under future climate change scenarios.
topic oyster
thermal adaption
heat-responsive gene
expression quantitative trait loci (eQTL) mapping
distant regulatory locus
url https://www.mdpi.com/2073-4425/12/7/1040
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