The Ga1 locus of the genus Zea is associated with novel genome structures derived from multiple, independent nonhomologous recombination events

Abstract

Abstract The Ga1 locus controls cross-incompatibility between field corn and popcorn. The Ga1-S haplotype contains 2 types of pectin methylesterase (PME) genes, ZmPme3 and several copies of ZmGa1P that are expressed in silk and pollen, respectively. The ga1 haplotype contains nonfunctional tandem repeat sequences related to ZmPme3 and ZmGa1P. This haplotype can cross-pollinate freely and is widely present in field corn. The primary objective of this study is to characterize the repeat sequences from a diverse collection of maize and teosinte lines and use this information to understand the evolution of the Ga1 locus. First, we characterized the complexity of the Ga1 genome region in high-quality maize genome assemblies that led to their categorization into 5 groups based on the number and type of PME-like sequences found at this region. Second, we studied duplication events that led to the ga1 and Ga1-S repeats using maximum likelihood phylogenetic reconstruction. Divergence estimates of the ga1 haplotype suggest that the duplication events occurred more than 600 KYA whereas those in Ga1-S occurred at 3 time points, i.e. >600, ∼260, and ∼100 KYA. These estimates suggest that the ga1 and Ga1-S tandem duplication events occurred independently. Finally, analysis of ZmPme3 and ZmGa1P homologs in Zea and Tripsacum genomes suggests that ga1 and Ga1-S repeats originated from an ancestral pair of PME genes that duplicated and diverged through 2 evolutionary branches prior to the domestication of maize.