Integrated network analysis identifies fight-club nodes as a class of hubs encompassing key putative switch genes that induce major transcriptome reprogramming during grapevine development

We developed an approach that integrates different network-based methods to analyze the correlation network arising from large-scale gene expression data. By studying grapevine (Vitis vinifera) and tomato (Solanum lycopersicum) gene expression atlases and a grapevine berry transcriptomic data set during the transition from immature to mature growth, we identified a category named “fight-club hubs” characterized by a marked negative correlation with the expression profiles of neighboring genes in the network. A special subset named “switch genes” was identified, with the additional property of many significant negative correlations outside their own group in the network. Switch genes are involved in multiple processes and include transcription factors that may be considered master regulators of the previously reported transcriptome remodeling that marks the developmental shift from immature to mature growth. All switch genes, expressed at low levels in vegetative/green tissues, showed a significant increase in mature/woody organs, suggesting a potential regulatory role during the developmental transition. Finally, our analysis of tomato gene expression data sets showed that wild-type switch genes are downregulated in ripening-deficient mutants. The identification of known master regulators of tomato fruit maturation suggests our method is suitable for the detection of key regulators of organ development in different fleshy fruit crops.

本研究开发了一种整合多种基于网络分析方法的研究策略，用于解析源自大规模基因表达数据的共表达相关网络。通过分析葡萄（Vitis vinifera）与番茄（Solanum lycopersicum）的基因表达图谱，以及葡萄浆果从不成熟生长向成熟生长转变过程中的转录组数据集，研究团队鉴定出一类被命名为“搏击俱乐部枢纽（fight-club hubs）”的基因，其核心特征为与网络中相邻基因的表达谱呈现显著负相关。本研究进一步鉴定出一类特殊亚组，命名为“开关基因（switch genes）”，该亚组具备另一项特征：其与网络中自身所属群组之外的众多基因均呈现显著负相关。开关基因参与多种生物学过程，其中包含的转录因子可被视作此前报道的、标志着从不成熟到成熟发育转变的转录组重塑过程的核心调控因子。所有开关基因在营养组织/绿色组织中均呈低表达水平，而在成熟/木质化器官中其表达量显著上调，这提示其在发育转变过程中具备潜在的调控功能。最后，针对番茄基因表达数据集的分析结果显示，野生型植株中的开关基因在果实成熟缺陷突变体中呈现表达下调。本次研究成功鉴定出已知的番茄果实成熟核心调控因子，这表明本研究开发的方法可用于检测多种肉质果实作物的器官发育关键调控因子。