Department of Botany, Charles University, Prague, 128 01, Czech Republic.
Institute of Botany, The Czech Academy of Sciences, Průhonice, 252 43, Czech Republic.
Plant J. 2021 Mar;105(5):1211-1224. doi: 10.1111/tpj.15105. Epub 2021 Jan 4.
Parallel adaptation results from the independent evolution of similar traits between closely related lineages and allows us to test to what extent evolution is repeatable. Similar gene expression changes are often detected but the identity of genes shaped by parallel selection and the causes of expression parallelism remain largely unknown. By comparing genomes and transcriptomes of four distinct foothill-alpine population pairs across four treatments, we addressed the genetic underpinnings, plasticity and functional consequences of gene expression parallelism in alpine adaptation. Seeds of eight populations of Arabidopsis arenosa were raised under four treatments that differed in temperature and irradiance, factors varying strongly with elevation. Parallelism in differential gene expression between the foothill and alpine ecotypes was quantified by RNA-seq in leaves of young plants. By manipulating temperature and irradiance, we also tested for parallelism in plasticity (i.e., gene-environment interaction, GEI). In spite of global non-parallel patterns transcriptome wide, we found significant parallelism in gene expression at the level of individual loci with an over-representation of genes involved in biotic stress response. In addition, we demonstrated significant parallelism in GEI, indicating a shared differential response of the originally foothill versus alpine populations to environmental variation across mountain regions. A fraction of genes showing expression parallelism also encompassed parallel outliers for genomic differentiation, with greater enrichment of such variants in cis-regulatory elements in some mountain regions. In summary, our results suggest frequent evolutionary repeatability in gene expression changes associated with the colonization of a challenging environment that combines constitutive expression differences and plastic interaction with the surrounding environment.
平行适应是由密切相关的谱系中相似特征的独立进化产生的，它使我们能够检验进化在多大程度上是可重复的。虽然经常检测到相似的基因表达变化，但由平行选择塑造的基因的身份和表达平行的原因在很大程度上仍然未知。通过比较四个不同的山麓-高山种群对的基因组和转录组，我们研究了基因表达平行在高山适应中的遗传基础、可塑性和功能后果。我们在四个不同的温度和光照处理下，对 8 个 Arabidopsis arenosa 种群的种子进行了培养，这些因素随海拔高度的变化而强烈变化。在幼苗叶片中通过 RNA-seq 量化了山麓和高山生态型之间差异表达的基因的平行性。通过操纵温度和光照，我们还测试了可塑性（即基因-环境互作，GEI）的平行性。尽管在转录组范围内存在整体非平行模式，但我们在个体基因座的基因表达水平上发现了显著的平行性，其中涉及生物胁迫反应的基因过度表达。此外，我们还证明了 GEI 的显著平行性，表明最初的山麓和高山种群对山区环境变化的差异反应具有共享性。表现出表达平行性的一部分基因也包含了基因组分化的平行离群值，在一些山区，这种变体在顺式调控元件中的富集程度更大。总之，我们的研究结果表明，与挑战性环境的殖民化相关的基因表达变化中存在频繁的进化可重复性，这种变化结合了组成型表达差异和与周围环境的可塑性相互作用。
