Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Munich, Germany.
Department of Insect Symbiosis, Max-Planck-Institute for Chemical Ecology, Jena, Germany.
PLoS Genet. 2024 Aug 23;20(8):e1011257. doi: 10.1371/journal.pgen.1011257. eCollection 2024 Aug.
The pervasiveness of gene expression variation and its contribution to phenotypic variation and evolution is well known. This gene expression variation is context dependent, with differences in regulatory architecture often associated with intrinsic and environmental factors, and is modulated by regulatory elements that can act in cis (linked) or in trans (unlinked) relative to the genes they affect. So far, little is known about how this genetic variation affects the evolution of regulatory architecture among closely related tissues during population divergence. To address this question, we analyzed gene expression in the midgut, hindgut, and Malpighian tubule as well as microbiome composition in the two gut tissues in four Drosophila melanogaster strains and their F1 hybrids from two divergent populations: one from the derived, European range and one from the ancestral, African range. In both the transcriptome and microbiome data, we detected extensive tissue- and genetic background-specific effects, including effects of genetic background on overall tissue specificity. Tissue-specific effects were typically stronger than genetic background-specific effects, although the two gut tissues were not more similar to each other than to the Malpighian tubules. An examination of allele specific expression revealed that, while both cis and trans effects were more tissue-specific in genes expressed differentially between populations than genes with conserved expression, trans effects were more tissue-specific than cis effects. Despite there being highly variable regulatory architecture, this observation was robust across tissues and genetic backgrounds, suggesting that the expression of trans variation can be spatially fine-tuned as well as or better than cis variation during population divergence and yielding new insights into cis and trans regulatory evolution.
基因表达变异的普遍性及其对表型变异和进化的贡献是众所周知的。这种基因表达变异是上下文相关的，其调控结构的差异通常与内在和环境因素有关，并受到调节元件的调节，这些调节元件可以在顺式（连锁）或反式（非连锁）相对于它们影响的基因起作用。到目前为止，对于这种遗传变异如何影响群体分歧过程中近亲组织的调控结构进化，我们知之甚少。为了解决这个问题，我们分析了来自两个不同种群的四个黑腹果蝇（Drosophila melanogaster）品系及其 F1 杂种在中肠、后肠和马氏管中的基因表达，以及在这两个肠道组织中的微生物组组成：一个来自衍生的欧洲范围，一个来自祖先的非洲范围。在转录组和微生物组数据中，我们检测到广泛的组织和遗传背景特异性效应，包括遗传背景对整体组织特异性的影响。组织特异性效应通常强于遗传背景特异性效应，尽管两个肠道组织彼此之间的相似性并不高于与马氏管的相似性。对等位基因特异性表达的研究表明，虽然 cis 和 trans 效应在群体间表达差异的基因中比在表达保守的基因中更具组织特异性，但 trans 效应比 cis 效应更具组织特异性。尽管存在高度可变的调控结构，但这一观察结果在组织和遗传背景上都是稳健的，这表明在群体分歧过程中，trans 变异的表达可以像 cis 变异一样或更好地进行空间微调，并为 cis 和 trans 调控进化提供了新的见解。
