Department of Genetics, University of Georgia, Athens, GA.
Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI.
Mol Biol Evol. 2020 Jul 1;37(7):2084-2098. doi: 10.1093/molbev/msaa071.
Divergence in gene expression regulation is common between closely related species and may give rise to incompatibilities in their hybrid progeny. In this study, we investigated the relationship between regulatory evolution within species and reproductive isolation between species. We focused on a well-studied case of hybrid sterility between two closely related yellow monkeyflower species, Mimulus guttatus and Mimulus nasutus, that is caused by two epistatic loci, hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2). We compared genome-wide transcript abundance across male and female reproductive tissues (i.e., stamens and carpels) from four genotypes: M. guttatus, M. nasutus, and sterile and fertile progeny from an advanced M. nasutus-M. guttatus introgression line carrying the hms1-hms2 incompatibility. We observed substantial variation in transcript abundance between M. guttatus and M. nasutus, including distinct but overlapping patterns of tissue-biased expression, providing evidence for regulatory divergence between these species. We also found rampant genome-wide misexpression, but only in the affected tissues (i.e., stamens) of sterile introgression hybrids carrying incompatible alleles at hms1 and hms2. Examining patterns of allele-specific expression in sterile and fertile introgression hybrids, we found evidence for interspecific divergence in cis- and trans-regulation, including compensatory cis-trans mutations likely to be driven by stabilizing selection. Nevertheless, species divergence in gene regulatory networks cannot explain the vast majority of the gene misexpression we observe in Mimulus introgression hybrids, which instead likely manifests as a downstream consequence of sterility itself.
基因表达调控的分歧在密切相关的物种中很常见，可能导致它们的杂交后代之间存在不兼容性。在这项研究中，我们研究了物种内调控进化与物种间生殖隔离之间的关系。我们专注于两个密切相关的黄花狸藻物种之间杂种不育的一个研究充分的案例，即黄花狸藻和北美黄花狸藻，这是由两个上位性基因位点杂种雄性不育 1（hms1）和杂种雄性不育 2（hms2）引起的。我们比较了来自四个基因型的雄性和雌性生殖组织（即雄蕊和雌蕊）的全基因组转录丰度：黄花狸藻、北美黄花狸藻以及携带 hms1-hms2 不兼容性的先进北美黄花狸藻-黄花狸藻渐渗系的不育和可育后代。我们观察到黄花狸藻和北美黄花狸藻之间的转录丰度存在很大差异，包括明显但重叠的组织偏表达模式，为这些物种之间的调控分歧提供了证据。我们还发现了广泛的全基因组基因表达错误，但仅在携带 hms1 和 hms2 不相容等位基因的不育渐渗杂种的受影响组织（即雄蕊）中。在对不育和可育渐渗杂种的等位基因特异性表达模式进行研究时，我们发现了种间 cis-和 trans-调控的分歧证据，包括可能由稳定选择驱动的补偿性 cis-trans 突变。尽管如此，基因调控网络中的物种分歧并不能解释我们在黄花狸藻渐渗杂种中观察到的绝大多数基因表达错误，这些错误更可能是不育本身的下游结果。
