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Regulatory variants in gene expression serve as bridges linking genetic variation and phenotypic plasticity. Environmental conditions typically influence the effects of regulatory variants on phenotypic plasticity; however, such genotype-by-environment interactions (G × E) are poorly understood. This study aimed to investigate the genetic basis of G × E in estuarine oyster (Crassostrea ariakensis), which is an important model animal for studying environmental adaption owing to its high plasticity and large intraspecific divergence. Genome-wide mapping of expression quantitative trait loci (eQTLs) for 23 environmental adaptive genes was performed for 256 estuarine oysters. We identified 1194 eQTL single nucleotide polymorphisms (eSNPs), including 433 cis -eSNPs in four genes and 722 trans -eSNPs in eight genes. The expression variation explanation of cis -eSNPs (9.95%) was significantly higher than that of trans -eSNPs (9.15%). We specifically showed cis- and trans-eSNPs with high linkage disequilibrium (LD) for Traf7 , Slc6a5 , Ggt , and Dap3. For example, we identified a cis -regulatory LD block containing 68 cis -eSNP and a trans -regulatory LD block, including 20 trans -eSNPs in Traf7. A high proportion (85%) of 40 vital eSNPs exhibited significant G × E effects. We identified crossing and nonparallel interactions of G × E, with the tag cis -eSNPs of Baat and Slc6a5 as representatives. Our results indicated that cis -eQTLs are highly conserved. This study provides insights into the understanding of adaptive evolutionary mechanisms and phenotypic response prediction to variable environments, as well as the genetic improvement for superior adaptive traits for genetic resource conservation and aquaculture. • We identified trans and cis regulatory variants and built potential regulatory networks. • Cis -eSNPs had larger contributions to gene expression plasticity and are conserved in different environments. • Trans -eSNPs are more abundant than cis -eSNPs and usually environment-specific. • A large proportion of eSNPs exhibited significant G × E effects. • Crossing and nonparallel G × E patterns were identified. [ABSTRACT FROM AUTHOR]

The estuarine oyster (Crassostrea ariakensis), a species native to Asia, is widespread throughout the estuarine region along the northern and southern coasts of China and has important ecological and economic values. Owing to runoff dropping and environmental threats caused by climate change and anthropogenic influences, the natural resources of C. ariakensis have persistently declined. Therefore, breeding oysters with high adaptability, which requires efficient and accurate genotyping tools, is beneficial to restore the germplasm resources and aquaculture. However, targeted genotyping tools are poorly developed for this species and even in other aquatic species. Previously, we have detected some selective regions and genes associated with temperature and salinity adaptation using selection signature analysis and found that the upstream regulatory regions of the environment-responsive genes exhibited higher differentiation. In this study, we developed a single nucleotide polymorphism (SNP) targeted genotyping tool for C. ariakensis , which includes 30 K SNPs located in previously identified target regions. The target genomic regions were enriched by hybridization capture using double-stranded DNA (dsDNA) biotin-labeled probes, and sequenced with high depth. A total of 24,541 (81.8%) high-quality SNPs were successfully genotyped in 655 samples. Compared to the genotypes obtained from previous genome-wide resequencing, 74.2% of the SNPs had a consistency rate of 1, with an average consistency rate for each sample of 97.8%. Population structure analysis showed three divergent populations (northern, southern, and middle) on the coast of China, consistent with those constructed using SNPs derived from whole-genome resequencing data. Most of the 30 K SNPs were located in the intergenic and regulatory regions, whereas 7% were located in the coding region. These high-quality SNPs were located in 953 genes, including 100 heat-response and 348 high-salinity-responsive genes. Therefore, this panel can be used to evaluate the adaptive divergence between populations, and causative SNPs related to temperature and salinity adaptation in the linkage and association analysis, providing robust support for the molecular breeding of estuarine oyster. To the best of our knowledge, this study proposes the first high-throughput SNP-targeted genotyping tool for studying the genetic basis of environmental adaptation in oyster, and providing insights into the development of targeted SNP genotyping tools for the adaptation study in other aquatic species under climate changes. • We developed a 30 K targeted genotyping tool for Crassostrea. Ariakensis. • 24,541 high-quality SNPs were successfully genotyped in 655 samples. • These high-quality SNPs were located in environment-responsive genes. • 74.2% of the SNPs had a consistency rate of 1 with resequencing. Population structure analysis showed three divergent populations on the coast of China • This study could be used to dissect the genetic basis of environmental adaptation. [ABSTRACT FROM AUTHOR]