The Genetic Architecture of Complex Traits in Teosinte (Zea maysssp.parviglumis): New Evidence From Association Mapping

Abstract

Previous association analyses showed that variation at major regulatory genes contributes to standing variation for complex traits in Balsas teosinte, the progenitor of maize. This study expands our previous association mapping effort in teosinte by testing 123 markers in 52 candidate genes for association with 31 traits in a population of 817 individuals. Thirty-three significant associations for markers from 15 candidate genes and 10 traits survive correction for multiple testing. Our analyses suggest several new putative causative relationships between specific genes and trait variation in teosinte. For example, two ramosa genes (ra1 and ra2) associate with ear structure, and the MADS-box gene, zagl1, associates with ear shattering. Since zagl1 was previously shown to be a target of selection during maize domestication, we suggest that this gene was under selection for its effect on the loss of ear shattering, a key domestication trait. All observed effects were relatively small in terms of the percentage of phenotypic variation explained (,10%). We also detected several epistatic interactions between markers in the same gene that associate with the same trait. Candidategene-based association mapping appears to be a promising method for investigating the inheritance of complex traits in teosinte.T HROUGH the characterization of major loss-offunction mutants, geneticists have determined the function of a vast number of genes. Despite a general knowledge of how these genes control developmental and physiological processes, very little is known about how (or if) they contribute to natural variation for complex traits. Association mapping with its high mapping resolution, its potential to sample multiple alleles, and its use of preexisting populations provides a powerful tool to investigate the role of these genes in the genetic architecture of complex traits ( Previously, we detected significant associations between polymorphisms in nine candidate genes and phenotypic variation in the maize ancestor, Balsas teosinte (Zea mays ssp. parviglumis) (Weber et al. 2007). Our study builds upon our prior analyses in several ways, including an increase in the numbers of individuals, candidate genes, and traits. We also selected our association mapping panel to decrease the amount of population structure as compared to our prior study. With this strategy, we detected 33 associations between complex traits in teosinte and our candidate genes that survive a correction for multiple testing. These include associations between indeterminate spikelet1 and inflorescence branching, ramosa1 and ramosa2 and ear structure, sugary1 and seed oil content, and terminal ear1 and ear length. We also observed an association between zea agamous-like1 (zagl1) and ear shattering. Since zagl1 was a target of selection during domestication, we propose that it was selected for its role in ear disarticulation. Several epistatic 1

Genetic Architecture of Domestication-Related Traits in Maize

“…Variants in zap1 were associated with ear length in teosinte (Weber et al 2008); our results suggest some functional variation at this locus passed through the domestication bottleneck and remains in maize or new functional variants have arisen within maize. Haplotypes at candidate gene gt1 were also associated with a small amount of shank length variation in maize.…”

“…Furthermore, teosinte "ears" are small, with kernels arranged in a distichous (two-ranked) pattern on the ear axis, compared to large ears of maize that typically have from 8 to .20 rows of kernels in four or more ranks. Several major QTL and in some cases, the specific genes, controlling these differences between maize and teosinte have been identified (Clark et al 2003;Doebley 2004;Briggs et al 2007;Weber et al 2008).The strong directional selection that occurred during the domestication of maize from teosinte reduced genetic diversity most strongly at key genes controlling domesticationrelated traits. Despite the severe bottleneck that occurred during domestication and strong selection for the maize plant type, standing variability in cob length, kernel row number, and shank length can be observed among maize breeding lines.…”

“…Furthermore, teosinte "ears" are small, with kernels arranged in a distichous (two-ranked) pattern on the ear axis, compared to large ears of maize that typically have from 8 to .20 rows of kernels in four or more ranks. Several major QTL and in some cases, the specific genes, controlling these differences between maize and teosinte have been identified (Clark et al 2003;Doebley 2004;Briggs et al 2007;Weber et al 2008).…”

Do Transcription Factors Play Special Roles in Adaptive Variation?

“…The strongest evidence for this comes from study of the gene encoding the teosinte branched TCP TF whose activity has influenced (negatively) the degree of branching in the transition during domestication from teosinte to maize, largely through changes in its expression pattern (Doebley et al, 1997;Wang et al, 1999;Lukens and Doebley, 2001;Doebley, 2004). Some studies, such as those of Weber et al (2007), have subsequently shown strong association of major traits distinguishing species to be associated with regulatory genes (although the definition of a regulatory gene in this case was not restricted to TFs), with three out of the five genes showing strong associations between regulatory genes and major trait variation in standing populations of teosinte, encoding TFs.…”

“…Consequently, what started as a relatively robust proposal has more recently been watered down, such that the definition of regulatory genes includes genes involved in signal transduction (Weber et al, 2007). Originally Doebley and Lukens suggested that evolution was more likely to occur through changes in the expression of genes involved in transcriptional regulation than those involved in sig-naling pathways; an argument based on the idea that signaling components operate upstream of transcriptional regulators, so that changes in the expression of signaling components were more likely to cause pleiotropic effects (and therefore had many more ways of being severely deleterious).…”