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Atgl启动子顺式变异的基因型×环境效应介导了两种同属牡蛎物种温度适应性表型可塑性的不同模式。

Genotype-by-Environment Effects of Cis-Variations in the Atgl Promoter Mediate the Divergent Pattern of Phenotypic Plasticity for Temperature Adaptation in Two Congeneric Oyster Species.

作者信息

Du Mingyang, Wang Chaogang, Jiang Zhuxiang, Cong Rihao, Li Ao, Wang Wei, Zhang Guofan, Li Li

机构信息

Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.

Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Qingdao, China.

出版信息

Mol Ecol. 2025 Feb;34(3):e17623. doi: 10.1111/mec.17623. Epub 2024 Dec 24.

DOI:10.1111/mec.17623
PMID:39718158
Abstract

Phenotypic plasticity plays an essential role in adaptive evolution. However, the molecular mechanisms of how genotype-by-environment interaction (G × E) effects shape phenotypic plasticity in marine organisms remain poorly understood. The crucial temperature-responsive trait triacylglycerol (TAG) content and its major gene adipose triglyceride lipase (Atgl) expression have divergent plastic patterns in two congeneric oyster species (Crassostrea gigas and Crassostrea angulata) to adapt to relative-cold/northern and relative-warm/southern habitats, respectively. In this study, eight putative loci were identified in the Atgl promoter region (cis-variations) between wild C. gigas and C. angulata that exhibited differential environmental responsiveness (G × E). The G and G × E effects of each locus were further dissected by measuring the Atgl gene expression of different genotypes in response to temperature changes at the cellular and organismal levels. Two transcription factors, non-environmentally responsive non-POU domain-containing octamer-binding protein (Nono) and environmentally responsive heterogeneous nuclear ribonucleoprotein K (Hnrnpk), were screened for binding to g.-1804 (G locus) and g.-1919 (G + G × E locus), respectively. The specificity of Nono binding to the C. angulata allele mediated the G effects of g.-1804, and the lower environmental sensitivity of Hnrnpk in C. angulata mediated the G × E effects of g.-1919, jointly regulating the trade-offs between higher constitutive and lower plastic expression of Atgl gene expression in C. angulata. This study served as an experimental case to reveal how the genetic variations with G and (or) G × E effects propagate into the divergent pattern of plasticity in environmental adaptive traits, which provides new insights into predicting the adaptability of marine organisms to future climate changes.

摘要

表型可塑性在适应性进化中起着至关重要的作用。然而,关于基因型与环境相互作用(G×E)效应如何塑造海洋生物表型可塑性的分子机制仍知之甚少。关键的温度响应性状三酰甘油(TAG)含量及其主要基因脂肪甘油三酯脂肪酶(Atgl)的表达在两种同属牡蛎物种(太平洋牡蛎和近江牡蛎)中具有不同的可塑性模式,分别适应相对寒冷/北方和相对温暖/南方的栖息地。在本研究中,在野生太平洋牡蛎和近江牡蛎的Atgl启动子区域(顺式变异)中鉴定出八个假定位点,这些位点表现出不同的环境响应性(G×E)。通过在细胞和生物体水平上测量不同基因型的Atgl基因表达对温度变化的响应,进一步剖析了每个位点的G和G×E效应。筛选出两个转录因子,即非环境响应性的含非POU结构域八聚体结合蛋白(Nono)和环境响应性的不均一核核糖核蛋白K(Hnrnpk),它们分别与g.-1804(G位点)和g.-1919(G + G×E位点)结合。Nono与近江牡蛎等位基因结合的特异性介导了g.-1804的G效应,而近江牡蛎中Hnrnpk较低的环境敏感性介导了g.-1919的G×E效应,共同调节了近江牡蛎中Atgl基因表达较高的组成型表达和较低的可塑性表达之间的权衡。本研究作为一个实验案例,揭示了具有G和(或)G×E效应的遗传变异如何传播到环境适应性性状的不同可塑性模式中,为预测海洋生物对未来气候变化的适应性提供了新的见解。

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