Abstract

Divergence of gene function and expression during development can give rise to phenotypic differences at the level of cells, tissues, organs, and ultimately whole organisms. To gain insights into the evolution of gene expression and novel genes at spatial resolution, we compared the spatially resolved transcriptomes of two distantly related nematodes, Caenorhabditis elegans and Pristionchus pacificus, that diverged 60–90 Ma. The spatial transcriptomes of adult worms show little evidence for strong conservation at the level of single genes. Instead, regional expression is largely driven by recent duplication and emergence of novel genes. Estimation of gene ages across anatomical structures revealed an enrichment of novel genes in sperm-related regions. This provides first evidence in nematodes for the “out of testis” hypothesis that has been previously postulated based on studies in Drosophila and mammals. “Out of testis” genes represent a mix of products of pervasive transcription as well as fast evolving members of ancient gene families. Strikingly, numerous novel genes have known functions during meiosis in Caenorhabditis elegans indicating that even universal processes such as meiosis may be targets of rapid evolution. Our study highlights the importance of novel genes in generating phenotypic diversity and explicitly characterizes gene origination in sperm-related regions. Furthermore, it proposes new functions for previously uncharacterized genes and establishes the spatial transcriptome of Pristionchus pacificus as a catalog for future studies on the evolution of gene expression and function.

中文翻译：

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线虫的空间转录组学将精子细胞鉴定为基因组新颖性和快速进化的来源。

摘要

发育过程中基因功能和表达的差异会导致细胞、组织、器官乃至整个生物体水平上的表型差异。为了以空间分辨率深入了解基因表达和新基因的进化，我们比较了两种远缘线虫，秀丽隐杆线虫和太平洋刺毛虫的空间分辨转录组，分歧了 60-90 Ma。成虫的空间转录组几乎没有证据表明在单基因水平上有很强的保守性。相反，区域表达主要是由最近的重复和新基因的出现驱动的。跨解剖结构的基因年龄估计揭示了精子相关区域中新基因的富集。这为线虫中的“睾丸外”假说提供了第一个证据，该假说先前是基于对果蝇和哺乳动物的研究而提出的。“睾丸外”基因代表了普遍转录的产物以及古老基因家族的快速进化成员的混合。引人注目的是，许多新基因在秀丽隐杆线虫减数分裂过程中具有已知功能这表明即使是减数分裂这样的普遍过程也可能成为快速进化的目标。我们的研究强调了新基因在产生表型多样性方面的重要性，并明确描述了精子相关区域的基因起源。此外，它为以前未表征的基因提出了新的功能，并建立了Pristionchus pacificus的空间转录组，作为未来基因表达和功能进化研究的目录。