Cis-regulatory variation and transcription factor binding contribute to allelic genotype-by-environment interactions for gene expression in maize

Abstract

Genotype-by-environment interactions (GxE), or differences in how genotypes perform across varying environments, are a pervasive source of phenotypic variation and underlie differences in local adaptation. Though GxE is well characterized across kingdoms of life, less is known about what causes GxE interactions, particularly at the molecular level. In this study, we use allele-specific gene expression estimates in a maize (Zea mays L.) B73 x Mo17 hybrid to isolate cis-regulatory effects on gene expression for each of the two parental alleles. The hybrid was grown in two environments, and expression differences between the parental alleles were used to characterize allele-by-environment (AxE) interactions and study the influence of gene-proximal sequence variation on transcript abundance AxE. We tested the hypothesis that gene-proximal sequence variation can cause GxE in gene expression by modifying transcription factor binding. Our results show that sequence variation in gene promoter regions has a small but consistent enrichment in genes that show transcriptional AxE. Further, we demonstrate that differential transcription factor binding potential caused by sequence variation is also enriched in AxE genes. Predictive models trained on sequence and transcription factor binding variation show that while these features contain some information about whether a gene will show transcriptional AxE, they alone are not sufficient to reliably distinguish AxE genes. These findings support the hypothesis that gene expression GxE can be caused by sequence variation that modifies transcription factor binding, while also reinforcing the complex and context-specific nature of GxE interactions.