The maize recombination landscape evolved during domestication

Authors: EPSTEIN, RUTH - Cornell University; WHEELER, JJ - Cornell University; HUBISZ, MELISSA - Cornell University; SUN, QI - Cornell University; BUKOWSKI, ROBERT - Cornell University; ZHAI, JINGJING - Cornell University; LAI, WEI-YUN - Cornell University; Buckler Iv, Edward; PAWLOWSKI, WOJTEK - Cornell University

Submitted to: bioRxiv
Publication Type: Other
Publication Acceptance Date: 11/6/2024
Publication Date: N/A
Citation: N/A
DOI: https://doi.org/10.1101/2024.11.04.621928

Interpretive Summary: ARS scientists investigated how the recombination landscape in maize evolved during its domestication from teosinte, its wild ancestor. They found that maize has a 12% higher genome-wide recombination rate, especially in gene-rich regions in the middle of chromosomes. This shift was likely driven by reduced interference between chromosome crossover events and selection on genes that regulate recombination. The increase in recombination in key genomic regions helped reduce harmful mutations and allowed beneficial traits tied to domestication to evolve more efficiently. These findings show that changes in recombination patterns were an important part of maize’s adaptation and success as a crop.

Technical Abstract: Meiotic recombination is an important evolutionary process because it can increase the amount of genetic variation within populations through the breakage of unfavorable linkages and creation of novel allelic combinations. Despite the plethora of knowledge about population-level benefits of recombination and numerous theoretical studies examining how recombination rates can evolve over time, there is a lack of empirical evidence for any hypotheses that have been put forward. To alleviate this gap in knowledge, we characterized the evolution of the recombination landscape in Zea mays ssp. mays (maize) during its domestication from Zea mays ssp. parviglumis (teosinte), explored hypotheses that permitted the evolution of the maize recombination landscape and tied these alterations to changes in the genetic basis of recombination. Using experimental populations and the population genomics approach of ancestral recombination graph (ARG) inference, our data demonstrated that maize had a 12% increase in its genome-wide recombination rate during domestication. Although the maize and teosinte recombination landscapes are highly correlated, r = 0.85 at 1Mb resolution, maize has evolved to have higher recombining regions in interstitial chromosome regions, compared to teosinte which only harbors high recombining regions sub-telomerically. Our data show that the re-patterning of COs towards interstitial chromosome regions came from reduced CO interference levels within maize. Supporting the idea that CO interference is reduced within maize, we found evidence for selection acting on trans-acting recombination-modifiers that participate in the class I CO pathway or CO interference directly. Lastly, we showed that the re-patterning of COs was beneficial to maize evolution because regions that significantly increased in recombination were targeted to gene-rich regions harboring domestication related loci. Because we found regions with significant increases in recombination had a lower deleterious mutation load, compared to regions with decreases in recombination, we concluded that the domestication-related variation in these regions, in which selection acted upon during domestication, was shielded from the Hill-Robertson effect. In conclusion, the re-patterning of CO events during domestication allowed maize to adapt and evolve at a faster rate than previously understood.