Genetic diversity in gene regulatory interactions underlies the response to soil drying in the model grass Brachypodium distachyon

Abstract

Gene expression is a quantitative trait under the control of genetic and environmental factors and their interaction, so-called GxE. Understanding the mechanisms driving GxE is fundamental for ensuring stable crop performance across environments and for predicting the response of natural populations to climate change. Gene expression is regulated through complex molecular networks, yet the interactions between genotype and environment on genome-wide regulatory networks are rarely considered. In this study, we model genome-scale gene expression variation between two natural accessions of the model grass Brachypodium distachyon and their response to soil drying. We identified genotypic, environmental, and GxE responses in physiological, metabolic, and gene expression traits. We then identified gene regulation conservation and variation among conditions and genotypes, simplified as co-expression clusters in each combination of genotype and environmental treatment. Putative gene regulatory interactions are inferred as network edges with a graphical modelling approach, resulting in hypotheses about gene-gene interactions specific to -- or with higher affinity in -- one genotype, one treatment, or in one genotype under treatment. We further find that some gene-gene interactions are conserved across conditions such that differential expression of one gene is apparently transmitted to a target gene. These variably detected edges cluster together in co-expression modules, suggestive of different constraints or selection strength acting on specific pathways. These variable features of gene regulatory networks may represent candidates modulate environmental response via genome editing, and suggest possible targets of evolutionary change in gene regulatory networks associated with phenotypic plasticity.