Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada.
Mol Ecol. 2019 Aug;28(16):3681-3697. doi: 10.1111/mec.15185. Epub 2019 Aug 5.
Understanding the plasticity, robustness and modularity of transcriptome expression to genetic and environmental conditions is crucial to deciphering how organisms adapt in nature. To test how genome architecture influences transcriptome profiles, we quantified expression responses for distinct temperature-adapted genotypes of the nematode Caenorhabditis briggsae when exposed to chronic temperature stresses throughout development. We found that 56% of the 8,795 differentially expressed genes show genotype-specific changes in expression in response to temperature (genotype-by-environment interactions, GxE). Most genotype-specific responses occur under heat stress, indicating that cold vs. heat stress responses involve distinct genomic architectures. The 22 co-expression modules that we identified differ in their enrichment of genes with genetic vs. environmental vs. interaction effects, as well as their genomic spatial distributions, functional attributes and rates of molecular evolution at the sequence level. Genes in modules enriched for simple effects of either genotype or temperature alone tend to evolve especially rapidly, consistent with disproportionate influence of adaptation or weaker constraint on these subsets of loci. Chromosome-scale heterogeneity in nucleotide polymorphism, however, rather than the scale of individual genes predominates as the source of genetic differences among expression profiles, and natural selection regimes are largely decoupled between coding sequences and noncoding flanking sequences that contain cis-regulatory elements. These results illustrate how the form of transcriptome modularity and genome structure contribute to predictable profiles of evolutionary change.
了解转录组表达对遗传和环境条件的可塑性、鲁棒性和模块性，对于破译生物在自然界中如何适应至关重要。为了测试基因组结构如何影响转录组谱，我们量化了在整个发育过程中暴露于慢性温度应激下不同温度适应基因型的秀丽隐杆线虫 Caenorhabditis briggsae 的表达响应。我们发现，8795 个差异表达基因中有 56%表现出对温度的基因型特异性表达变化（基因型-环境互作，GxE）。大多数基因型特异性反应发生在热应激下，表明冷应激与热应激反应涉及不同的基因组结构。我们鉴定的 22 个共表达模块在其具有遗传、环境和互作效应的基因富集程度、基因组空间分布、功能属性以及序列水平的分子进化率方面存在差异。在仅受基因型或温度单一因素影响的模块中富集的基因往往进化得特别快，这与这些基因座子集的适应或较弱约束的不成比例影响一致。然而，在表达谱中，核苷酸多态性的染色体规模异质性而不是单个基因的规模占主导地位，是遗传差异的来源，并且编码序列和包含顺式调控元件的非编码侧翼序列之间的自然选择机制在很大程度上是分离的。这些结果说明了转录组模块性和基因组结构的形式如何有助于可预测的进化变化模式。
