Rödelsperger Christian, Ebbing Annabel, Sharma Devansh Raj, Okumura Misako, Sommer Ralf J, Korswagen Hendrik C
Department for Integrative Evolutionary Biology, Max Planck Institute for Developmental Biology, Tübingen, Germany.
Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center Utrecht, Utrecht, The Netherlands.
Mol Biol Evol. 2021 Jan 4;38(1):229-243. doi: 10.1093/molbev/msaa207.
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.
在发育过程中，基因功能和表达的差异会在细胞、组织、器官乃至整个生物体水平上产生表型差异。为了在空间分辨率上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小杆线虫——的空间分辨转录组，它们在6000万至9000万年前发生了分化。成年线虫的空间转录组几乎没有证据表明单个基因水平上存在强烈的保守性。相反，区域表达在很大程度上是由新基因的近期复制和出现驱动的。对跨解剖结构的基因年龄估计显示，与精子相关的区域中富集了新基因。这为线虫中的“睾丸外”假说提供了首个证据，该假说此前是基于对果蝇和哺乳动物的研究提出的。“睾丸外”基因代表了广泛转录产物以及古老基因家族中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的减数分裂过程中具有已知功能，这表明即使是像减数分裂这样的普遍过程也可能是快速进化的目标。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，并明确表征了与精子相关区域中的基因起源。此外，它为以前未表征的基因提出了新功能，并将太平洋小杆线虫的空间转录组确立为未来基因表达和功能进化研究的目录。
