A newly evolved gene is essential for efficient sperm entry into eggs in Drosophila melanogaster

Sara Y Guay, Prajal H Patel, Jonathon M Thomalla, Kerry L McDermott, Jillian M O'Toole, Sarah E Arnold, Sarah J Obrycki, Mariana F Wolfner, Geoffrey D Findlay
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Abstract

New genes arise through a variety of evolutionary processes and provide raw material for adaptation in the face of both natural and sexual selection. De novo evolved genes emerge from previously non-protein-coding DNA sequences, and many such genes are expressed in male reproductive structures. In Drosophila melanogaster, several putative de novo genes have evolved essential roles in spermatogenesis, but whether such genes can also impact sperm function beyond the male has not been investigated. We identified a putative de novo gene, katherine johnson (kj), that is required for high levels of male fertility. Males that do not express kj produce and transfer sperm that are stored normally in females, but sperm from these males enter eggs with severely reduced efficiency. Using a tagged transgenic rescue construct, we observed that KJ protein localizes to the nuclear periphery in various stages of spermatogenesis, but is not detectable in mature sperm. These data suggest that kj exerts an effect on sperm development, the loss of which results in reduced fertilization ability. While previous bioinformatic analyses suggested the kj gene was restricted to the melanogaster group of Drosophila, we identified putative orthologs with conserved synteny, male-biased expression, and predicted protein features across the genus, as well as instances of gene loss in some lineages. Thus, kj potentially arose in the Drosophila common ancestor and subsequently evolved an essential role in D. melanogaster. Our results demonstrate a new aspect of male reproduction that has been shaped by new gene evolution and provide a molecular foothold for further investigating the mechanism of sperm entry into eggs in Drosophila.
一个新进化的基因对黑腹果蝇精子有效进入卵子至关重要
新基因通过各种进化过程产生,并在自然选择和性选择的作用下为适应性提供原材料。新进化基因来自以前的非蛋白编码DNA序列,许多这类基因在雄性生殖结构中表达。在黑腹果蝇中,几个推定的新基因在精子发生过程中发挥了重要作用,但这些基因是否也能影响雄性以外的精子功能,目前还没有研究。我们发现了一个推定的新基因凯瑟琳-约翰逊(kj),它是雄性高水平生育能力所必需的。不表达 kj 的雄性能产生和转移正常储存在雌性体内的精子,但这些雄性的精子进入卵子的效率严重下降。利用标记转基因拯救构建体,我们观察到 KJ 蛋白在精子发生的不同阶段定位于核外围,但在成熟精子中检测不到。这些数据表明,KJ对精子的发育有影响,失去它就会导致受精能力下降。虽然之前的生物信息学分析表明 kj 基因仅限于黑腹果蝇,但我们在整个果蝇属中发现了具有保守同源关系、雄性偏向表达和预测蛋白特征的推定直向同源物,并在一些品系中发现了基因缺失的情况。因此,kj 有可能产生于果蝇的共同祖先,随后在黑腹果蝇中演化出重要作用。我们的研究结果展示了新基因进化所形成的雄性生殖的一个新方面,并为进一步研究果蝇精子进入卵子的机制提供了分子基础。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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