Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize

Authors: YANG, JINLIANG - University Of California, Davis; MEZMOUK, SOFIANE - Kws Saat Ag; BAUMGARTEN, ANDY - Dupont Pioneer Hi-Bred; Buckler, Edward - Ed; Guill, Katherine; MCMULLEN, MICHAEL - University Of Missouri; MUMM, RITA - University Of Illinois; ROSS-IBARRA, JEFFREY - University Of California, Davis

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/13/2017
Publication Date: 9/27/2017
Citation: Yang, J., Mezmouk, S., Baumgarten, A., Buckler IV, E.S., Guill, K.E., McMullen, M., Mumm, R., Ross-Ibarra, J. 2017. Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize. PLoS Genetics. https://doi.org/10.1371/journal.pgen.1007019.
DOI: https://doi.org/10.1371/journal.pgen.1007019

Interpretive Summary: The scientific application of hybrid vigor has been central to the productivity of US agriculture starting over a century ago. However, the molecular basis of this vigor is now being cataloged. Every generation a plant reproduces novel mutations occur, and some of these mutations cause disease or reduce the vigor of the plant - deleterious mutations. Plant breeders can select against these deleterious mutations, but frequently there are too many of them to remove them all. Using extensive DNA sequencing of elite corn varieties, this study was able to use evolutionary approaches to catalog deleterious mutations, and successfully used the catalog of mutations to predict hybrid corn yield. Many of the deleterious mutations had their effects partially masked when they were in hybrids, which is why hybrids are so productive.

Technical Abstract: Deleterious alleles have long been proposed to play an important role in patterning phenotypic variation and are central to commonly held ideas explaining the hybrid vigor observed in the offspring by crossing two inbred parents. We test these ideas using evolutionary measures of sequence conservation to ask whether incorporating information about putatively deleterious alleles can inform genomic selection (GS) models and improve phenotypic prediction. We measured a number of agronomic traits in both the inbred parents and hybrids of an elite maize partial diallel population and re-sequenced the parents of the population. Inbred elite maize lines vary for more than 350,000 putatively deleterious sites, but show a lower burden of such sites than a comparable set of traditional landraces. Our modeling reveals widespread evidence for incomplete dominance at these loci, and supports theoretical models that more damaging variants are usually more recessive. We identify haplotype blocks using an identity-by-descent (IBD) analysis and perform genomic prediction analyses in which we weigh blocks on the basis of segregating putatively deleterious variants. Cross-validation results show that incorporating sequence conservation in genomic selection improves prediction accuracy for grain yield and other fitness-related traits as well as heterosis for those traits. Our results provide empirical support for an important role for incomplete dominance of deleterious alleles in explaining heterosis and demonstrate the utility of incorporating functional annotation in phenotypic prediction and plant breeding.