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

Authors: BAPAT, AMRUTA - Iowa State University; Moran Lauter, Adrienne; HUFFORD, MATTHEW - Iowa State University; Boerman, Nicholas; Scott, Marvin

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/16/2023
Publication Date: 8/31/2023
Citation: Bapat, A.R., Moran Lauter, A., Hufford, M.B., Boerman, N.A., Scott, M.P. 2023. The Ga1 locus of the genus Zea is associated with novel genome structures derived from multiple, independent nonhomologous recombination events. G3, Genes/Genomes/Genetics. Article jkad196. https://doi.org/10.1093/g3journal/jkad196.
DOI: https://doi.org/10.1093/g3journal/jkad196

Interpretive Summary: The maize Ga1 gene controls cross pollination between field corn and popcorn varieties. The DNA sequence surrounding Ga1 has an usual structure, composed of repeated sequences similar to the Ga1 sequence. We wanted to understand the molecular events that gave rise to this complex structure. Analysis of these repeated sequences allowed us to develop a model for how the current genome structure arose. By comparing to sequences of maize wild relatives, we were able to assign dates to key events in the model. This region of the genome seems to be a "hotspot" for duplications because independent arrays of repeated sequences arose at least twice in evolutionary history. This information is valuable as a case study to researchers who seek to understand how modern genetic regions evolved from their progenitors.

Technical Abstract: The maize Ga1 locus controls cross incompatibility between field corn and popcorn varieties. The Ga1-S haplotype mediates its effect through pollen- and silk-specific factors that interact genetically to enable correct pollen tube growth and fertilization. This haplotype contains two pectin methylesterase (PME) genes, ZmPme3 and several copies of ZmGa1P that are expressed in silk and pollen, respectively. A haplotype called ga1 contains non-functional tandem repeat sequences derived from both ZmPme3 and ZmGa1P through non-homologous recombination. 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 and use this information to better understand the evolution of the Ga1 locus. To do this, we first examined the complexity of the genomic region at this locus in all field corn and popcorn lines for which high-quality genome assemblies are currently available. DNA sequence analysis of the genome region of Ga1 locus led to the categorization of the genomes into 5 groups based on the number and type of PME-like sequences found at this region. Second, we studied the duplication events that led to the tandemly repeated sequence arrays. Phylogenetic reconstruction using a maximum-likelihood approach was used to infer a duplication history for the ga1 and Ga1-S repeat regions. The ga1 phylogeny suggests that at least two separate duplication events occurred very close to each other in time, while the Ga1-S phylogeny suggests a series of duplications occurred during the evolution of the haplotype. Divergence estimates of the duplicates of the ga1 haplotype suggest the event occurred more than 600 kya whereas those in Ga1-S occurred at three time points of > 600 kya, ~ 260 kya and ~ 100 kya. These estimates suggest that the ga1 and Ga1-S duplication events occurred independently of each other, however, both likely involved a non-homologous recombination mechanism, suggesting that this region of the genome may be a hot-spot for non-homologous recombination events. Finally, we also identified and studied ZmPme3 and ZmGa1P homologs in Zea and Tripsacum genomes. The results suggest that ga1 and Ga1-S repeats originated from an ancestral pair of PME genes that duplicated and diverged through two evolutionary branches prior to the domestication of maize. In conclusion, the Ga1 locus is a hotspot for non-homologous recombination events that may provide insights into the evolution of repeated regions of genomes.