Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, CA.
Mol Biol Evol. 2018 Sep 1;35(9):2110-2119. doi: 10.1093/molbev/msy138.
Thermal tolerance is a key determinant of species distribution. Despite much study, the genetic basis of adaptive evolution of thermal tolerance, including the relative contributions of transcriptional regulation versus protein evolution, remains unclear. Populations of the intertidal copepod Tigriopus californicus are adapted to local thermal regimes across their broad geographic range. Upon thermal stress, adults from a heat tolerant southern population, San Diego (SD), upregulate several heat shock proteins (HSPs) to higher levels than those from a less tolerant northern population, Santa Cruz (SC). Suppression of a specific HSP, HSPB1, significantly reduces T. californicus survival following acute heat stress. Sequencing of HSPB1 revealed population specific nucleotide substitutions in both promoter and coding regions of the gene. HSPB1 promoters from heat tolerant populations contain two canonical heat shock elements (HSEs), the binding sites for heat shock transcription factor (HSF), whereas less tolerant populations have mutations in these conserved motifs. Allele specific expression of HSPB1 in F1 hybrids between tolerant and less tolerant populations showed significantly biased expression favoring alleles from tolerant populations and supporting the adaptive divergence in these cis-regulatory variants. The functional impact of population-specific nonsynonymous substitutions in HSPB1 coding sequences was tested by assessing the thermal stabilization properties of SD versus SC HSPB1 protein variants. Recombinant HSPB1 from the southern SD population showed greater capacity for protecting protein structure under elevated temperature. Our results indicate that both regulatory and protein coding sequence evolution within a single gene appear to contribute to thermal tolerance phenotypes and local adaptation among conspecific populations.
耐热性是物种分布的关键决定因素。尽管进行了大量研究，但耐热性适应性进化的遗传基础，包括转录调控与蛋白质进化的相对贡献，仍不清楚。潮间带桡足类动物加利福尼亚 T. californicus 的种群分布广泛，适应其所在地区的热环境。在受到热胁迫时，来自耐热南部种群圣地亚哥（SD）的成年个体比来自较不耐热的北部种群圣克鲁兹（SC）的个体上调更多的热休克蛋白（HSPs）到更高的水平。抑制特定的 HSP，HSPB1，会显著降低 T. californicus 在急性热应激后的存活率。对 HSPB1 的测序揭示了该基因的启动子和编码区都存在种群特异性核苷酸取代。耐热种群的 HSPB1 启动子包含两个典型的热休克元件（HSEs），是热休克转录因子（HSF）的结合位点，而较不耐热的种群在这些保守基序中发生了突变。在耐受和不耐热种群之间的 F1 杂种中，HSPB1 的等位基因特异性表达显示出明显的偏向表达，有利于耐受种群的等位基因，并支持这些顺式调控变异的适应性分化。通过评估 SD 与 SC HSPB1 蛋白变异体的热稳定性特性，测试了 HSPB1 编码序列中种群特异性非同义取代的功能影响。来自南部 SD 种群的重组 HSPB1 表现出在高温下保护蛋白质结构的更大能力。我们的结果表明，单个基因内的调控和蛋白质编码序列进化似乎都有助于耐热性表型和同种群之间的局部适应。
