The degree of selfing has major impacts on adaptability and is often controlled by molecular mechanisms determining mating compatibility. Changes in compatibility systems are therefore important evolutionary events, but their underlying genomic mechanisms are often poorly understood. Fungi display frequent shifts in compatibility systems, and their small genomes facilitate elucidation of the mechanisms involved. In particular, linkage between the pre- and postmating compatibility loci has evolved repeatedly, increasing the odds of gamete compatibility under selfing. Here, we studied the mating-type chromosomes of two anther-smut fungi with unlinked mating-type loci despite a self-fertilization mating system. Segregation analyses and comparisons of high-quality genome assemblies revealed that these two species displayed linkage between mating-type loci and their respective centromeres. This arrangement renders the same improved odds of gamete compatibility as direct linkage of the two mating-type loci under the automictic mating (intratetrad selfing) of anther-smut fungi. Recombination cessation was found associated with a large inversion in only one of the four linkage events. The lack of trans-specific polymorphism at genes located in nonrecombining regions and linkage date estimates indicated that the events of recombination cessation occurred independently in the two sister species. Our study shows that natural selection can repeatedly lead to similar genomic patterns and phenotypes, and that different evolutionary paths can lead to distinct yet equally beneficial responses to selection. Our study further highlights that automixis and gene linkage to centromeres have important genetic and evolutionary consequences, while being poorly recognized despite being present in a broad range of taxa.

中文翻译：

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自交花药黑穗病真菌中交配型基因和着丝粒之间的趋同重组终止。


自交程度对适应性有重大影响，并且通常由决定交配兼容性的分子机制控制。因此，相容性系统的变化是重要的进化事件，但人们对其潜在的基因组机制往往知之甚少。真菌在相容性系统中表现出频繁的变化，它们的小基因组有助于阐明所涉及的机制。特别是，交配前和交配后相容性基因座之间的联系反复进化，增加了自交下配子相容性的几率。在这里，我们研究了两种花药黑粉菌真菌的交配型染色体，尽管它们具有自体受精交配系统，但它们的交配型基因座不相连。高质量基因组组装的分离分析和比较表明，这两个物种在交配型基因座与其各自的着丝粒之间显示出连锁。这种排列使得配子相容性的改善几率与花药黑粉菌真菌的自交配（内分体自交）下两个交配型基因座的直接连锁相同。发现重组停止仅与四个连锁事件之一中的大倒位相关。位于非重组区域的基因缺乏反式特异性多态性和连锁日期估计表明重组停止事件在两个姐妹物种中独立发生。我们的研究表明，自然选择可以反复导致相似的基因组模式和表型，并且不同的进化路径可以导致对选择的不同但同样有益的反应。 我们的研究进一步强调，自混合和与着丝粒的基因连锁具有重要的遗传和进化后果，尽管存在于广泛的分类群中，但人们对它的认识却很少。