| Summary: | Global warming drives adaptive evolution by influencing natural selection and exploiting temperature-related phenotypic plasticity. However, predicting how phenotypic plasticity will evolve under climate change remains a challenge, urging the need for understanding underlying genetic and molecular mechanisms. In this study, we focus on the expression plasticity divergence of heat shock protein 90 (Hsp90) which is heat responsive and exhibited strong selective sweep in the upstream noncoding region of two allopatric congeneric oyster species: cold-adapted Crassostrea gigas and warm-adapted Crassostrea angulata. Functional characterization confirmed Hsp90 expression is an ideal proxy for thermotolerance. The expression divergence in constitutive and plastic expressions, represents adaption to the mean and variance of habitat temperature changes, respectively. By combining forward and reverse genetic approaches, four causative loci with G+G×E effects in the promoter region (cis-variations) of Hsp90 between C. gigas and C. angulata were identified. Moreover, the allele g.-2291G of the causative loci in C.angulata specifically binds to the positive transcription factor Purine Rich Element Binding Protein B (PURB), explaining the higher constitutive expression of Hsp90. Meanwhile the response of Purb to thermal stress affects the magnitude of plastic expression in C. angulata. This integrative study revealed that cis-variation interacts with trans-variation induced by environmental changes underlying the G×E effect, thereby mediating the divergence of plastic expression. Furthermore, we established a paradigm for studying genetic variants and their G×E effects at an unprecedented resolution at the single nucleotide level in non-model organisms. This study will deepen our understanding of the significant role of phenotypic plasticity in adaptive responses and promote predictions of adaptive potential in marine organisms under climate change.
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