Department for Integrative Evolutionary Biology, Max Planck Institute for Biology, Tübingen, Germany.
PLoS Genet. 2023 Jul 3;19(7):e1010832. doi: 10.1371/journal.pgen.1010832. eCollection 2023 Jul.
Adaptation of organisms to environmental change may be facilitated by the creation of new genes. New genes without homologs in other lineages are known as taxonomically-restricted orphan genes and may result from divergence or de novo formation. Previously, we have extensively characterized the evolution and origin of such orphan genes in the nematode model organism Pristionchus pacificus. Here, we employ large-scale transcriptomics to establish potential functional associations and to measure the degree of transcriptional plasticity among orphan genes. Specifically, we analyzed 24 RNA-seq samples from adult P. pacificus worms raised on 24 different monoxenic bacterial cultures. Based on coexpression analysis, we identified 28 large modules that harbor 3,727 diplogastrid-specific orphan genes and that respond dynamically to different bacteria. These coexpression modules have distinct regulatory architecture and also exhibit differential expression patterns across development suggesting a link between bacterial response networks and development. Phylostratigraphy revealed a considerably high number of family- and even species-specific orphan genes in certain coexpression modules. This suggests that new genes are not attached randomly to existing cellular networks and that integration can happen very fast. Integrative analysis of protein domains, gene expression and ortholog data facilitated the assignments of biological labels for 22 coexpression modules with one of the largest, fast-evolving module being associated with spermatogenesis. In summary, this work presents the first functional annotation for thousands of P. pacificus orphan genes and reveals insights into their integration into environmentally responsive gene networks.
生物体对环境变化的适应可能通过创造新基因来促进。没有其他谱系同源物的新基因被称为分类限制的孤儿基因，可能是由分歧或从头形成的。以前，我们已经广泛研究了线虫模式生物 Pristionchus pacificus 中此类孤儿基因的进化和起源。在这里，我们采用大规模转录组学来建立潜在的功能关联，并测量孤儿基因的转录可塑性程度。具体来说，我们分析了 24 个来自成年 P. pacificus 蠕虫的 RNA-seq 样本，这些蠕虫是在 24 种不同的单养细菌培养物上培养的。基于共表达分析，我们确定了 28 个大型模块，这些模块包含 3727 个双鞭毛虫特异性孤儿基因，并对不同的细菌表现出动态响应。这些共表达模块具有独特的调控结构，并且在发育过程中表现出不同的表达模式，这表明细菌反应网络与发育之间存在联系。系统发生分析显示，在某些共表达模块中，存在相当数量的家族甚至种特异性孤儿基因。这表明新基因不是随机附着在现有的细胞网络上的，并且整合可以非常迅速地发生。对蛋白质结构域、基因表达和同源数据的综合分析有助于为 22 个共表达模块分配生物学标签，其中最大的、快速进化的模块与精子发生有关。总之，这项工作首次对数千个 P. pacificus 孤儿基因进行了功能注释，并揭示了它们整合到对环境有反应的基因网络中的见解。
