Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte

Authors

Luis Fernando Samayoa, North Carolina State University
Bode A. Olukolu, University of Tennessee
Chin Jian Yang, University of Wisconsin–Madison
Qiuyue Chen, University of Wisconsin–Madison
Markus G. Stetter, University of Cologne
Alessandra M. York, University of Wisconsin–Madison
Jose de Jesus Sanchez-Gonzalez, Universidad de Guadalajara
Jeffrey C. Glaubitz, Cornell University
Peter J. Bradbury, Cornell University
Maria Cinta Romay, Cornell University
Qi Sun, Cornell University
Jinliang Yang, University of Nebraska - LincolnFollow
Jeffrey Ross-Ibarra, University of California, Davis
Edward S. Buckler, Cornell University
John F. Doebley, University of Wisconsin–Madison
James B. Holland, North Carolina State University, United States Department of Agriculture– Agriculture Research Service

Date of this Version

12-20-2021

Citation

Samayoa LF, Olukolu BA, Yang CJ, Chen Q, Stetter MG, York AM, et al. (2021) Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte. PLoS Genet 17(12): e1009797. https://doi.org/10.1371/journal. pgen.1009797

Comments

This is an open access article

Abstract

Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to large-effect mutations versus variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load in the maize population that we predicted from sequence data. Parental breeding values were highly consistent between outcross and selfed offspring, indicating that additive effects determine most of the genetic value even in the presence of strong inbreeding depression. We developed a novel linkage scan to identify quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, smalleffect partially recessive effects in linkage disequilibrium underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against some large effect variants, but polygenic load is harder to purge and overall segregating mutational burden increased in maize compared to teosinte.