Endogenous retroviruses drive species-specific germline transcriptomes in mammals.

Gene regulation in the germline ensures the production of high-quality gametes, long-term maintenance of the species, and speciation. Male germline transcriptomes undergo dynamic changes after the mitosis-to-meiosis transition and have been subject to evolutionary divergence among mammals. However, the mechanisms underlying germline regulatory divergence remain undetermined. Here, we show that endogenous retroviruses (ERVs) influence species-specific germline transcriptomes. After the mitosis-to-meiosis transition in male mice, specific ERVs function as active enhancers to drive germline genes, including a mouse-specific gene set, and bear binding motifs for critical regulators of spermatogenesis such as A-MYB. This raises the possibility that a genome-wide transposition of ERVs rewired germline gene expression in a species-specific manner. Of note, independently evolved ERVs are associated with the expression of human-specific germline genes, demonstrating the prevalence of ERV-driven mechanisms in mammals. Together, we propose that ERVs fine-tune species-specific transcriptomes in the mammalian germline.

生殖系中的基因调控确保了高质量配子的产生、物种的长期维持以及物种形成。雄性生殖系转录组在有丝分裂向减数分裂转变后会发生动态变化，并且在哺乳动物中已经发生了进化上的分化。然而，生殖系调控分化的潜在机制仍未确定。在此，我们表明内源性逆转录病毒（ERVs）影响物种特异性的生殖系转录组。在雄性小鼠有丝分裂向减数分裂转变后，特定的ERVs作为活性增强子来驱动生殖系基因，包括一组小鼠特异性基因，并且具有精子发生的关键调控因子（如A - MYB）的结合基序。这增加了一种可能性，即ERVs在全基因组范围内的转座以物种特异性的方式重新连接了生殖系基因的表达。值得注意的是，独立进化的ERVs与人类特异性生殖系基因的表达相关，这表明ERV驱动的机制在哺乳动物中普遍存在。总之，我们提出ERVs在哺乳动物生殖系中微调物种特异性转录组。