Neighbours matter: Effects of genomic organization on gene expression plasticity in response to environmental stresses during biological invasions

Abstract

Gene expression regulation has been widely recognized as an important molecular mechanism underlying phenotypic plasticity in environmental adaptation. However, it remains largely unexplored on the effects of genomic organization on gene expression plasticity under environmental stresses during biological invasions. Here, we use an invasive model ascidian, Ciona robusta, to investigate how genomic organization affects gene expression in response to salinity stresses during range expansions. Our study showed that neighboring genes were co-expressed and approximately 30% of stress responsive genes were physically clustered on chromosomes. Such coordinated expression was substantially affected by the physical distance and orientation of genes. Interestingly, the overall expression correlation of neighboring genes was significantly decreased under high salinity stresses, illustrating that the co-expression regulation could be disrupted by salinity challenges. Furthermore, the clustering of genes was associated with their function constraints and expression patterns - operon genes enriched in gene expression machinery had the highest transcriptional activity and expression stability. Notably, our analyses showed that the tail-to-tail genes, mainly involved in biological functions related to phosphorylation, homeostatic process, and ion transport, exhibited higher intrinsic expression variability and greater response to salinity challenges. Altogether, the results obtained here provide new insights into the effects of gene organization on gene expression plasticity under environmental challenges, hence improving our knowledge on mechanisms of rapid environmental adaptation during biological invasions.

Keywords: Biological invasion; Environmental challenge; Gene co-expression; Neighboring gene; Operon.