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

Kexin Zhang,Wei Wang,Jinpeng Wang,Li Li,Ruihui Shi,Fangfang Ding,Guofan Zhang

doi:10.3390/genes12071040

Abstract

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 Crassostrea gigas and its sister species Crassostrea angulata 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 (HspA9). Ribosomal protein L10a (RPL10A) 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 (ATG7). Nuclear respiratory factor 1 (NRF1) was detected approximately 3 kb upstream of the two SNPs. These results suggested regulatory relationships between RPL10A and HSPA9 and between NRF1 and ATG7. 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.

Highlights

Introduction distributed under the terms andClimate change has resulted in rapid global ocean warming [1], which threatens the survival and performance of marine ectotherms [2]
The phenotypic variation explanation (PVE) ranged from 6% to 26.6%. expression quantitative trait loci (eQTL) details and mapping results are shown in Table 2 and Supplementary Figure S2, respectively
The phenotypic variation of single regulatory loci at the transcript level was generally higher (6–26.6%) than growth-related traits (0.6–13.8%) using the same genetic map in Pacific oysters [42], which may due to the complexity of growth-related traits

Summary

Introduction

Introduction distributed under the terms andClimate change has resulted in rapid global ocean warming [1], which threatens the survival and performance of marine ectotherms [2]. High phenotypic plasticity, which at morphological and molecular levels allow them to adapt to highly variable intertidal zones. This ability makes them ideal representatives of intertidal organisms for the study of adaptive mechanisms in response to heat and other environmental stresses [8,9,10]. Gene expression variation accounts for much of the phenotypic variation among populations and individuals in response to rapid climate change [11,12,13,14]. Transcriptomic and proteomic analyses reveal changes in genes and proteins that are involved in cellular homeostasis, protein stability, metabolic adjustment, signaling transduction, and ion transportation and so on under heat stress in marine organisms. Heat shock proteins (HSP)s and genes related to metabolic adjustment and ion transport show differential expression in fish exposed to elevated temperatures [16,17]

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