Coexpression modules.

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.

生物体应对环境变化的适应性，可通过新基因的生成而得到促进。在其他演化支中无同源基因的新基因，被称为分类限制型孤儿基因（taxonomically-restricted orphan genes），这类基因可由趋异演化或从头起源产生。此前，我们已对模式线虫物种太平洋小杆线虫（Pristionchus pacificus）中的这类孤儿基因的演化与起源进行了全面解析。本研究借助大规模转录组学（transcriptomics）技术，明确孤儿基因间潜在的功能关联，并量化其转录可塑性程度。具体而言，我们分析了24份RNA测序（RNA-seq）样本，这些样本取自以24种不同单菌培养物饲养的成年太平洋小杆线虫。基于共表达分析，我们鉴定出28个大型共表达模块，其中包含3727个双胃线虫科特异性孤儿基因，且这些模块可随不同细菌环境呈现动态响应。这些共表达模块具有独特的调控架构，且在不同发育阶段呈现差异表达模式，这提示细菌响应网络与发育过程之间存在关联。系统发生地层分析法（phylostratigraphy）结果显示，在部分共表达模块中，存在数量可观的科特异性甚至种特异性孤儿基因。这表明新基因并非随机整合至现有的细胞网络中，且其整合过程可快速完成。通过对蛋白质结构域、基因表达及直系同源数据的整合分析，我们为22个共表达模块赋予了生物学功能注释；其中体量最大、演化最快的模块之一与精子发生过程相关。综上，本研究首次为数千个太平洋小杆线虫孤儿基因提供了功能注释，并揭示了其整合至环境响应基因网络的相关机制。