The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication

Authors: CHEN, QIUYUE - University Of Wisconsin; SAMAYOA, LUIS FERNANDO - North Carolina State University; YANG, C - University Of Wisconsin; Bradbury, Peter; OLUKOLU, BODE - University Of Tennessee; NEUMEYER, MICHAEL - University Of Wisconsin; TOMAY, MARIA CINTA - Cornell University; SUN, QI - Cornell University; LORANT, ANNE - University Of California; Buckler, Edward - Ed; ROSS-IBARRA, J - University Of California; Holland, Jim - Jim; DOEBLEY, JOHN - University Of Wisconsin

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/6/2020
Publication Date: 5/14/2020
Citation: Chen, Q., Samayoa, L., Yang, C.J., Bradbury, P., Olukolu, B., Neumeyer, M.A., Tomay, M., Sun, Q., Lorant, A., Buckler IV, E.S., Ross-Ibarra, J., Holland, J.B., Doebley, J.F. 2020. The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication. PLoS Genetics. 16(5):e1008791.

Interpretive Summary: Corn (maize) was domesticated about 5000 years ago from the wild grass teosinte in Mexico. The dramatic change in seed, ear, and plant morphology that occurred under domestication was primarily the result of selection for a few mutations with large effect. Nevertheless, variation still exists within both maize and teosinte for some of the traits that dramatically changed under selection. We asked in this paper what the difference in the genetic control of these important agronomic (for corn) or fitness (for teosinte) traits is. Such traits include flowering time, plant height, number of seeds produced per plant. Our results show that many genes affect all of these traits, with a small handful of genes having large effects, and many other genes with quite small effects. The variants with large effects occur at low population frequency, suggestion that they are mutations that are generally unfavorable and are being selected against either naturally (in teosinte) or by humans (in corn). We found more evidence for selection reducing the number of large effect variants and overall genetic variation in corn compared to its wild relative.

Technical Abstract: The genetics of domestication has been extensively studied ever since the rediscovery of Mendel’s law of inheritance and much has been learned about the genetic control of trait differences between crops and their ancestors. Here, we ask how domestication has altered genetic architecture by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. We observed a strongly reduced number of QTL for domestication traits in maize relative to teosinte, which is consistent with the previously reported depletion of additive variance by selection during domestication. We also observed more dominance in maize than teosinte, likely a consequence of selective removal of additive variants. We observed that large effect QTL have low minor allele frequency (MAF) in both maize and teosinte. Regions of the genome that are strongly differentiated between teosinte and maize (high FST) explain less quantitative variation in maize than teosinte, suggesting that, in these regions, allelic variants were brought to (or near) fixation during domestication. We also observed that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of the additive variance in both teosinte and maize is “missing” in the sense that it cannot be ascribed to detectable QTL and only 25% of variance maps to specific QTL. This latter result suggests that morphological evolution during domestication is largely attributable to very large numbers of QTL of very small effect.