Allele-specific expression reveals multiple paths to highland adaptation in maize

Authors: HU, HAIXIAO - University Of California, Davis; CROW, TAYLOR - University Of California, Davis; NOJOOMI, SAGHI - University Of California, Davis; SCHULZ, AIMEE - Iowa State University; ESTEVEZ-PALMAS, JUAN - National Laboratory Of Genomics And Biodiversity; HUFFORD, MATTHEW - Iowa State University; Flint-Garcia, Sherry; SAWERS, RUAIRIDH - Pennsylvania State University; RELLAN-ALVAREZ, RUBEN - North Carolina State University; ROSS-IBARRA, JEFFREY - University Of California, Davis; RUNICE, DANIEL - University Of California, Davis

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2022
Publication Date: 11/3/2022
Citation: Hu, H., Crow, T., Nojoomi, S., Schulz, A.J., Estevez-Palmas, J.M., Hufford, M., Flint Garcia, S.A., Sawers, R., Rellan-Alvarez, R., Ross-Ibarra, J., Runice, D. 2022. Allele-specific expression reveals multiple paths to highland adaptation in maize. Molecular Biology and Evolution. 39(11). Article msac239. https://doi.org/10.1093/molbev/msac239.
DOI: https://doi.org/10.1093/molbev/msac239

Interpretive Summary: Corn is adapted to a wide range of growing environments around the world including high elevations, some of which are greater than two miles above sea level. In many regions, this highland-adapted corn is a major component of human and animal diets, and a major source of income for smallholder farmers. Temperate-adapted and low elevation corn does not grow or produce well in highland sites, and the corn from highland regions is low yielding. In order to understand this specialized adaptation, we evaluated gene activity of corn hybrids originating from both highland or lowland regions of Mexico and South America when they are grown in highland and lowland field sites. We found that thousands of genes belonging to different gene networks are active in distinguishing adaptation to highland and lowland sites. We also found that different gene networks were active depending on the broader geographic origin of the corn (e.g. Mexico versus South America). These results suggest that adaptation is very location specific. Many of the genes active in highland-adapted corn are involved in cold stress (highland field sites are much cooler and have shorter growing seasons), photosynthesis (corn adapted to the different light quality and temperatures in highland versus lowland sites are able to capture light energy more or less efficiently), or plant hormones (one mechanism by which plants grow and respond to their environment). This information can be used to develop higher yielding corn varieties for highland field sites. In addition, understanding how plants have historically adapted to a broad range of environments is valuable as breeders and geneticists continue to adapt crops to new environments in the future.

Technical Abstract: Maize is a staple food of smallholder farmers living in highland regions up to 4,000 m above sea level worldwide. Mexican and South American highlands are two major highland maize growing regions, and population genetic data suggest the maize's adaptation to these regions occurred largely independently, providing a case study for convergent evolution. To better understand the mechanistic basis of highland adaptation, we crossed maize landraces from 108 highland and lowland sites of Mexico and South America with the inbred line B73 to produce F1 hybrids and grew them in both highland and lowland sites in Mexico. We identified thousands of genes with divergent expression between highland and lowland populations. Hundreds of these genes show patterns of convergent evolution between Mexico and South America. To dissect the genetic architecture of the divergent gene expression, we developed a novel allele–specific expression analysis pipeline to detect genes with divergent functional cis-regulatory variation between highland and lowland populations. We identified hundreds of genes with divergent cis-regulation between highland and lowland landrace alleles, with 20 in common between regions, further suggesting convergence in the genes underlying highland adaptation. Further analyses suggest multiple mechanisms contribute to this convergence in gene regulation. Although the vast majority of evolutionary changes associated with highland adaptation were region specific, our findings highlight an important role for convergence at the gene expression and gene regulation levels as well.