Pers Daniel, Buchta Thomas, Özüak Orhan, Wolff Selma, Pietsch Jessica M, Memon Mohammad Bilal, Roth Siegfried, Lynch Jeremy A
Department of Biological Sciences, University of Illinois at Chicago, MBRB 4020, 900 S. Ashland Avenue, Chicago, IL, 60402, USA.
Institute for Developmental Biology, University at Cologne, Cologne, Germany.
BMC Biol. 2016 Aug 1;14:63. doi: 10.1186/s12915-016-0285-y.
Gene regulatory networks (GRNs) underlie developmental patterning and morphogenetic processes, and changes in the interactions within the underlying GRNs are a major driver of evolutionary processes. In order to make meaningful comparisons that can provide significant insights into the evolution of regulatory networks, homologous networks from multiple taxa must be deeply characterized. One of the most thoroughly characterized GRNs is the dorsoventral (DV) patterning system of the Drosophila melanogaster embryo. We have developed the wasp Nasonia as a comparative DV patterning model because it has shown the convergent evolution of a mode of early embryonic patterning very similar to that of the fly, and it is of interest to know whether the similarity at the gross level also extends to the molecular level.
We used RNAi to dorsalize and ventralize Nasonia embryos, RNAseq to quantify transcriptome-wide expression levels, and differential expression analysis to identify genes whose expression levels change in either RNAi case. This led to the identification of >100 genes differentially expressed and regulated along the DV axis. Only a handful of these genes are shared DV components in both fly and wasp. Many of those unique to Nasonia are cytoskeletal and adhesion molecules, which may be related to the divergent cell and tissue behavior observed at gastrulation. In addition, many transcription factors and signaling components are only DV regulated in Nasonia, likely reflecting the divergent upstream patterning mechanisms involved in producing the conserved pattern of cell fates observed at gastrulation. Finally, several genes that lack Drosophila orthologs show robust and distinct expression patterns. These include genes with vertebrate homologs that have been lost in the fly lineage, genes that are found only among Hymenoptera, and several genes that entered the Nasonia genome through lateral transfer from endosymbiotic bacteria.
Altogether, our results provide insights into how GRNs respond to new functional demands and how they can incorporate novel components.
基因调控网络（GRNs）是发育模式形成和形态发生过程的基础，潜在GRNs内相互作用的变化是进化过程的主要驱动力。为了进行有意义的比较，从而深入了解调控网络的进化，必须深入刻画多个分类群的同源网络。最全面刻画的GRNs之一是黑腹果蝇胚胎的背腹（DV）模式形成系统。我们已将黄蜂丽蝇蛹集金小蜂开发为一个用于比较DV模式形成的模型，因为它已显示出一种与果蝇非常相似的早期胚胎模式形成方式的趋同进化，并且了解总体水平上的相似性是否也延伸到分子水平很有意义。
我们使用RNA干扰使丽蝇蛹集金小蜂胚胎背化和腹化，用RNA测序来定量全转录组范围的表达水平，并通过差异表达分析来鉴定在任何一种RNA干扰情况下表达水平发生变化的基因。这导致鉴定出100多个沿DV轴差异表达和调控的基因。这些基因中只有少数是果蝇和黄蜂共有的DV组分。丽蝇蛹集金小蜂特有的许多基因是细胞骨架和粘附分子，这可能与原肠胚形成时观察到的不同细胞和组织行为有关。此外，许多转录因子和信号传导组分仅在丽蝇蛹集金小蜂中受DV调控，这可能反映了在产生原肠胚形成时观察到的保守细胞命运模式中涉及的不同上游模式形成机制。最后，几个没有果蝇直系同源基因的基因表现出强大且独特的表达模式。这些基因包括在果蝇谱系中已丢失的具有脊椎动物同源物的基因、仅在膜翅目中发现的基因，以及通过从内共生细菌横向转移进入丽蝇蛹集金小蜂基因组的几个基因。
总之，我们的结果为GRNs如何响应新的功能需求以及它们如何纳入新组分提供了见解。
