Topological clustering of regulatory genes confers pathogenic tolerance to cassava brown streak virus (CBSV) in cassava

Abstract

Robustness, a naïve property of biological systems, enables organisms to maintain functions during perturbation and is crucial for improving the resilience of crops to prevailing stress conditions and diseases, guaranteeing food security. Most studies of robustness in crops have focused on genetic superiority based upon individual genes, overlooking the collaborative actions of multiple responsive genes and the regulatory network topology. This research aims to uncover patterns of gene cooperation leading to organismal robustness by studying the topology of gene co-expression networks (GCNs) of both CBSV virus resistant and susceptible cassava cultivars. The resulting GCNs show higher topological clustering of cooperative genes in the resistant cultivar, suggesting that the network architecture is central to attaining robustness. Despite a reduction in the number of hub genes in the resistant cultivar following the perturbation, essential biological functions contained in the network were maintained through neighboring genes that withstood the shock. The susceptible cultivar seemingly coped by inducing more gene actions in the network but could not maintain the functions required for plant growth. These findings underscore the importance of regulatory network architecture in ensuring phenotypic robustness and deepen our understanding of transcriptional regulation.