Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa.
Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa.
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PRDM9物种形成基因在多种后生分类单元中加速了进化。
DOI：
10.1371/journal.pgen.1000753
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发表时间：
2009-12
期刊：
影响因子：
4.5
通讯作者：
Ponting CP
中科院分区：
文献类型：
--
作者：
Oliver PL;Goodstadt L;Bayes JJ;Birtle Z;Roach KC;Phadnis N;Beatson SA;Lunter G;Malik HS;Ponting CP
种群间基因流动的合子前和合子后障碍的出现是物种形成的标志。早期物种之间最早出现的合子后隔离障碍之一是种间杂种中异配子性别的不育。已经在动物中鉴定了四种导致杂种不育的基因：果蝇中的Odysseus、JYalpha和Overdrive以及小鼠中的Prdm9（Meisetz）。小鼠Prdm 9编码具有KRAB基序、组蛋白甲基转移酶结构域和几个锌指的蛋白质。单个锌指的差异将导致杂种不育的Prdm9等位基因与不导致杂种不育的Prdm9等位基因区分开。我们发现协同进化和正选择已经迅速改变了13个啮齿动物基因组中Prdm 9锌指的数量和序列。Prdm9锌指中的正选择模式意味着快速进化作用于Prdm9蛋白与其结合的DNA序列之间的界面。对于包括灵长类动物在内的多种后生动物，Prdm9锌指也有类似的模式。事实上，人类PRDM9锌指的DNA结合位置的等位基因变异显示出与不育风险降低的显著相关性。因此，Prdm 9在决定物种之间（小鼠）和物种内（人）的雄性不育性方面发挥作用。作用于Prdm9的正选择周期性事件表明，它所结合的DNA序列也必须迅速进化。我们的研究结果没有确定潜在的DNA序列的性质，但反对Prdm 9作为小鼠减数分裂中的重要转录因子的作用。我们提出了一个假设模型，其中Prdm9结合特异性和卫星DNA之间的不相容性提供了Prdm9介导的杂交不育的分子基础。我们建议，Prdm9应调查作为一个候选基因在其他情况下的杂种不育后生动物。物种形成是一个物种分裂成两个物种的过程，涉及到先前杂交种群之间的生殖障碍。早在达尔文的《物种起源》之前，物种形成是如何发生的问题就一直吸引着生物学家的注意力。对最近分化的物种的研究揭示了杂种不育基因（俗称“物种形成基因”）的存在，其等位基因与种间杂种的不育性有关。小鼠Prdm 9是脊椎动物中唯一已知的此类基因。在这里，我们报告说，Prdm9蛋白在其DNA结合结构域，包括一系列的“锌指”进化非常迅速。这表明，杂种不育性可能是由Prdm9的DNA结合特异性和快速进化的DNA之间的错配引起的。我们认为Prdm9与不同物种内部和之间快速进化的卫星DNA重复序列相结合。Prdm9的进化是不寻常的，因为其他杂交不育基因似乎只在孤立的爆发中迅速进化，而Prdm9在许多啮齿动物物种，不同的灵长类动物和其他后生动物中已经进化了7亿多年。这导致了一种诱人的可能性，即Prdm9可能在后生动物进化的其他场合充当了“物种形成基因”，这种可能性现在需要进行调查。
The onset of prezygotic and postzygotic barriers to gene flow between populations is a hallmark of speciation. One of the earliest postzygotic isolating barriers to arise between incipient species is the sterility of the heterogametic sex in interspecies' hybrids. Four genes that underlie hybrid sterility have been identified in animals: Odysseus, JYalpha, and Overdrive in Drosophila and Prdm9 (Meisetz) in mice. Mouse Prdm9 encodes a protein with a KRAB motif, a histone methyltransferase domain and several zinc fingers. The difference of a single zinc finger distinguishes Prdm9 alleles that cause hybrid sterility from those that do not. We find that concerted evolution and positive selection have rapidly altered the number and sequence of Prdm9 zinc fingers across 13 rodent genomes. The patterns of positive selection in Prdm9 zinc fingers imply that rapid evolution has acted on the interface between the Prdm9 protein and the DNA sequences to which it binds. Similar patterns are apparent for Prdm9 zinc fingers for diverse metazoans, including primates. Indeed, allelic variation at the DNA–binding positions of human PRDM9 zinc fingers show significant association with decreased risk of infertility. Prdm9 thus plays a role in determining male sterility both between species (mouse) and within species (human). The recurrent episodes of positive selection acting on Prdm9 suggest that the DNA sequences to which it binds must also be evolving rapidly. Our findings do not identify the nature of the underlying DNA sequences, but argue against the proposed role of Prdm9 as an essential transcription factor in mouse meiosis. We propose a hypothetical model in which incompatibilities between Prdm9-binding specificity and satellite DNAs provide the molecular basis for Prdm9-mediated hybrid sterility. We suggest that Prdm9 should be investigated as a candidate gene in other instances of hybrid sterility in metazoans. Speciation, the process by which one species splits into two, involves reproductive barriers between previously interbreeding populations. The question of how speciation occurs has rightly occupied the attention of biologists since before Darwin's “On the Origin of Species.” Studies of recently diverged species have revealed the presence of hybrid sterility genes (colloquially referred to as “speciation genes”), alleles of which are associated with sterility of interspecies hybrids. Mouse Prdm9 is the only known such gene in vertebrate animals. Here we report that the Prdm9 protein has evolved extremely rapidly in its DNA-binding domain, comprising an array of “zinc fingers.” This suggests that hybrid sterility may arise from a mismatch between the DNA-binding specificity of Prdm9 and rapidly evolving DNA. We propose that Prdm9 binds to satellite-DNA repeats evolving rapidly within and between different species. Prdm9 evolution is unusual because other hybrid sterility genes appear only to evolve rapidly in isolated bursts, whereas Prdm9 has evolved rapidly over 700 million years, in many rodent species, diverse primates and other metazoans. This leads to the tantalizing possibility that Prdm9 may have served as a “speciation gene” on other occasions in metazoan evolution, a possibility that will now need to be investigated.
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