Abstract
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.
Highlights
Chromosomal inversions are structural rearrangements that form when a portion of a chromosome breaks in two places and reinserts in the opposite orientation
To assess evidence of local adaptation, we modeled the association of Inv4m genotype with elevation among the 1757 Mexican plants
One key question is whether inversions generally contain only two important functional variants, or if they capture many, perhaps because they act as a sieve for new mutations [51,52,53,54], and whether these variants contribute to the same trait, or independently regulate multiple traits that may all be adaptive
Summary
Chromosomal inversions are structural rearrangements that form when a portion of a chromosome breaks in two places and reinserts in the opposite orientation. The reversed order of loci inside an inversion greatly reduces recombination in heterozygous individuals because the crossover products are imbalanced in gene content and often non-viable [1] This newlyformed genetic linkage can be important for speciation and local adaptation when haplotypes with alternative orientations carry multiple adaptive and potentially interacting loci in a linked block [2,3,4]. Chromosomal inversions were first discovered nearly a century ago in Drosophila [3, 15] by visualizing karyotypes, and can be identified based on their effects on recombination rates among nearby markers Both techniques are labor intensive and difficult to apply to large-scale population-level surveys within or among species. Modern genome-wide sequencing technologies have recently been used to rapidly discover inversion loci, measure their frequencies across populations, and test for associations with adaptation and speciation, leading to the discovery of large numbers of inversions across a wide range of species [1, 16,17,18]
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