Gene regulatory effects of a large chromosomal inversion in highland maize

Chromosomal inversions play an important role in local adaptation. Inversions can capture multiple locally adaptive functional variants in a linked block by repressing recombination. However, this recombination suppression makes it difficult to identify the genetic mechanisms underlying an inversion's role in adaptation. In this study, we used large-scale transcriptomic data to dissect the functional importance of a 13 Mb inversion locus (Inv4m) found almost exclusively in highland populations of maize (Zea mays ssp. mays). Inv4m was introgressed into highland maize from the wild relative Zea mays ssp. mexicana, also present in the highlands of Mexico, and is thought to be important for the adaptation of these populations to cultivation in highland environments. However, the specific genetic variants and traits that underlie this adaptation are not known. We created two families segregating for the standard and inverted haplotypes of Inv4m in a common genetic background and measured gene expression effects associated with the inversion across 9 tissues in two experimental conditions. With these data, we quantified both the global transcriptomic effects of the highland Inv4m haplotype, and the local cis-regulatory variation present within the locus. We found diverse physiological effects of Inv4m across the 9 tissues, including a strong effect on the expression of genes involved in photosynthesis and chloroplast physiology. Although we could not confidently identify the causal alleles within Inv4m, this research accelerates progress towards understanding this inversion and will guide future research on these important genomic features. Author summary Chromosomal inversions are a type of structural variant commonly found to underlie local adaptation and speciation. However, in most cases we do not know what genes or genetic variants inside an inversion are important, and how any such variants regulate the associated adaptive traits. Fine-mapping genetic variants using forward genetics inside inversions is difficult because recombination between heterokayotypes are suppressed. In this study, we used gene expression as a tool to study the genetics of a large chromosomal inversion found in highland maize populations in Mexico called Inv4m. Gene expression analyses in 9 tissues across two environmental conditions identified a large number of seemingly independent developmental and physiological processes regulated by Inv4m, suggesting that this locus contributes to local adaptation of maize to highland environments in multiple ways.