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DNA methylation mediates differentiation in thermal responses of Pacific oyster (Crassostrea gigas) derived from different tidal levels

Abstract

Epigenetic mechanisms such as DNA methylation have the potential to affect organism acclimatization and adaptation to environmental changes by influencing their phenotypic plasticity; however, little is known about the role of methylation in the adaptive phenotypic divergence of marine invertebrates. Therefore, in this study, a typical intertidal species, the Pacific oyster (Crassostrea gigas), was selected to investigate the epigenetic mechanism of phenotypic plasticity in marine invertebrates. Intertidal and subtidal oysters subjected to one-generation common garden experiments and exhibited phenotypic divergence were used. The methylation landscape of both groups of oysters was investigated under temperate and high temperature. The two tidal oysters exhibited divergent methylation patterns, regardless of the temperature, which was mainly original environment-induced. Intertidal samples exhibited significant hypomethylation and more plasticity of methylation in response to heat shock, while subtidal samples showed hypermethylation and less plasticity. Combined with RNA-seq data, a positive relationship between methylation and expression in gene bodies was detected on a genome-wide scale. In addition, approximately 11% and 7% of differentially expressed genes showed significant methylation variation under high temperatures in intertidal and subtidal samples, respectively. Genes related to apoptosis and organism development may be regulated by methylation in response to high temperature in intertidal oysters, whereas oxidation-reduction and ion homeostasis-related genes were involved in subtidal oysters. The results also suggest that DNA methylation mediates phenotypic divergence in oysters adapting to different environments. This study provides new insight into the epigenetic mechanisms underlying phenotypic plasticity in adaptation to rapid climate change in marine organisms.

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Fig. 1: Global methylation landscape.
Fig. 2: Assessment of genetic effect on DNA methylation.
Fig. 3: Relationship between DNA methylation and gene expression.
Fig. 4: Analysis of different genes in two tidal oysters.
Fig. 5: Comparative methylome analysis under heat shock.
Fig. 6: Analysis of gene response to heat shock.

Data availability

The methylome data have been deposited in the Sequence Read Archive database with the accession number PRJNA562805.

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Acknowledgements

LL is supported by the National Key R&D Program of China (No. 2018YFD09-00304) and Key Deployment Project of Centre for Ocean Mega-Research of Science, Chinese Academy of Sciences (COMS2019Q06). AL is supported by the Distinguished Young Scientists Research Fund of Key Laboratory of Experimental Marine Biology, Chinese Academy of Sciences (No. KLEMB-DYS04). LL is also supported by the National Natural Science Foundation of China (No. 31572620) and the Technology and the Modern Agro-industry Technology Research System (No. CARS-49). We thank professor Manuel Aranda for guidance on SNP calling and related analysis, and thank Dr. Yuxia Zou for advices with BSP experiment.

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Wang, X., Li, A., Wang, W. et al. DNA methylation mediates differentiation in thermal responses of Pacific oyster (Crassostrea gigas) derived from different tidal levels. Heredity 126, 10–22 (2021). https://doi.org/10.1038/s41437-020-0351-7

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