Data from: Izumo1 and Juno: the evolutionary origins and coevolution of essential sperm-egg binding partners

Reproductive proteins are among the most rapidly evolving classes of proteins. For a subset of these, rapid evolution is driven by positive Darwinian selection despite vital, well-conserved, reproductive functions. Izumo1 is the only essential sperm–egg fusion protein currently known on mammalian sperm, and its egg receptor (Juno; formerly Folr4) was recently discovered. Male knockout mice for Izumo1 and female knockout mice for Juno are both healthy but sterile. Here, both sperm–egg binding proteins are shown to be evolving under positive selection. Within mammals, coevolution of Izumo1 and Juno is also uncovered, suggesting that similar forces have shaped the evolutionary histories of these binding partners within Mammalia. Additionally, genomic analyses reveal an ancient origin for the Izumo gene family, initially reported as conserved exclusively in mammals. Newly identified Izumo1 orthologues could serve reproductive functions in birds, fish and reptiles. Surprisingly, these same analyses support Juno's presence in mammals alone, suggesting a recent mammalian-specific duplication and neofunctionalization of the ancestral folate receptor. Despite the indispensability of their reproductive interaction, and their apparent coevolution within Mammalia, this binding pair arose through strikingly different evolutionary forces.

生殖蛋白是进化速率最快的蛋白类群之一。其中部分子类群尽管执行着至关重要且高度保守的生殖功能，但其快速进化却由达尔文正选择（positive Darwinian selection）驱动。Izumo1是目前已知的唯一一种定位于哺乳动物精子表面的必需精卵融合蛋白，其卵子受体（Juno；旧称Folr4）已于近期被发现。Izumo1基因敲除雄性小鼠与Juno基因敲除雌性小鼠均表现为健康但不育。本研究证实，这两种精卵结合蛋白均处于达尔文正选择的进化压力之下。在哺乳纲（Mammalia）中，研究同时揭示了Izumo1与Juno的协同进化（coevolution）现象，表明相似的进化力量塑造了这对结合伴侣在哺乳纲中的进化历程。此外，基因组分析显示Izumo基因家族拥有古老起源——该家族最初被认为仅在哺乳动物中保守存在。新鉴定出的Izumo1直系同源基因（orthologue）在鸟类、鱼类与爬行动物中可能执行生殖功能。令人意外的是，上述分析结果表明Juno仅存在于哺乳动物中，这提示祖先叶酸受体（folate receptor）在近期发生了哺乳纲特异性的基因复制与新功能化（neofunctionalization）。尽管二者的生殖结合作用不可或缺，且在哺乳纲中呈现明显的协同进化，但这对结合伴侣的起源却受到了截然不同的进化力量驱动。