Distinct Genetic Architectures for Male and Female Inflorescence Traits of Maize

Abstract

We compared the genetic architecture of thirteen maize morphological traits in a large population of recombinant inbred lines. Four traits from the male inflorescence (tassel) and three traits from the female inflorescence (ear) were measured and studied using linkage and genome-wide association analyses and compared to three flowering and three leaf traits previously studied in the same population. Inflorescence loci have larger effects than flowering and leaf loci, and ear effects are larger than tassel effects. Ear trait models also have lower predictive ability than tassel, flowering, or leaf trait models. Pleiotropic loci were identified that control elongation of ear and tassel, consistent with their common developmental origin. For these pleiotropic loci, the ear effects are larger than tassel effects even though the same causal polymorphisms are likely involved. This implies that the observed differences in genetic architecture are not due to distinct features of the underlying polymorphisms. Our results support the hypothesis that genetic architecture is a function of trait stability over evolutionary time, since the traits that changed most during the relatively recent domestication of maize have the largest effects.

Author Summary

Genetic architecture is of broad interest in evolutionary biology, plant and animal breeding, and medicine, because it influences both the response to selection and the success of trait mapping. Results from the most rigorously studied genetic systems suggest a similar genetic architecture across all species and traits studied, with many loci of small effect. A few strongly selected traits in domesticated organisms show unusual genetic architecture, for reasons that are unclear. We compare maize inflorescence, flowering, and leaf traits and show that inflorescence traits have distinct genetic architectures characterized by larger effects. Female inflorescences (ears) have larger effects than male inflorescences (tassels) even though the two structures have similar developmental origins. Analysis of pleiotropic loci shows that these larger effects are not inherent features of the underlying polymorphisms. Rather, maize inflorescences appear to be exceptionally labile, with female inflorescences more labile than male inflorescences. These results support the canalization hypothesis, which predicts that rapidly changing traits will have larger effects. We suggest that maize inflorescence traits, and ear traits in particular, have larger effects than flowering or leaf traits as a result of strong directional selection during maize domestication.