Rapid evolution of alpha-gliadin gene family revealed by analyzing Gli-2 locus regions of wild emmer wheat

Authors: HUO, NAXIN - University Of California, Davis; ZHU, TINGTING - University Of California, Davis; ZHANG, SHENGLI - Henan Institute Of Science And Technology; Mohr, Toni; LUO, MING-CHENG - University Of California, Davis; LEE, JONG-YEOL - National Institute For Agricultural Science & Technology; DISTELFELD, ASSAF - Tel Aviv University; Altenbach, Susan; Gu, Yong

Submitted to: Functional and Integrative Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/30/2019
Publication Date: 6/13/2019
Citation: Huo, N., Zhu, T., Zhang, S., Mohr, T.J., Luo, M., Lee, J., Distelfeld, A., Altenbach, S.B., Gu, Y.Q. 2019. Rapid evolution of alpha-gliadin gene family revealed by analyzing Gli-2 locus regions of wild emmer wheat. Functional and Integrative Genomics. https://doi.org/10.1007/s10142-019-00686-z.
DOI: https://doi.org/10.1007/s10142-019-00686-z

Interpretive Summary: Domestication of wheat occurred about 10,000 years ago and played an important role in human civilization. Wild emmer wheat is the direct progenitor of both cultivated tetraploid pasta wheat and hexaploid bread wheat, contributing the AABB genomes to both cultivated wheat types. The composition of prolamins, the major seed storage proteins of wheat, is an important trait in wheat breeding and production since it determines the end-use quality of wheat flour. Prolamine composition is also a critical determinant of wheat’s allergenicity potential and individual sensitivity to wheat through food allergies or celiac disease (CD). The analysis of gluten complements in ancestral wheat species has shown that different types of prolamin genes from diploid, tetraploid, and polyploid wheats differ considerably in the frequencies and in the presence and abundance of CD immunogenic peptides. In this study, we employed a comprehensive approach to analyze the alpha-gliadin genomic regions in wild emmer wheat. The results in this study could enhance the breeding effort by unraveling the genetic diversity in wild emmer and reintroducing valuable traits from wild ancestral species into cultivated wheat.

Technical Abstract: alpha-gliadins are a major group of gluten proteins in wheat flour that contribute to the end-use properties for food processing and contain major immunogenic epitopes that can cause serious health-related issues including celiac disease (CD). alpha-gliadins are also the youngest group of gluten proteins and are encoded by a large gene family. The majority of the gene family members evolved independently in the A, B and D genomes of different wheat species after their separation from a common ancestral species. To gain insights into the origin and evolution of these complex genes, the genomic regions of the Gli-2 loci encoding alpha-gliadins were characterized from the tetraploid wild emmer, a direct progenitor of hexaploid bread wheat that contributed the AABB genomes. Genomic sequences of Gli-2 locus regions for the wild emmer A and B genomes were first reconstructed using the genome sequence scaffolds along with optical genome maps. A total of 25 and 16 alpha-gliadin genes were identified for the A and B genome regions, respectively. Alpha-gliadin pseudogene frequencies of 86% for the A genome and 69% for the B genome were primarily caused by C to T substitutions in the highly abundant glutamine codons, resulting in the generation of premature stop codons. Comparison with the homologous regions from the hexaploid wheat cv Chinese Spring indicated considerable sequence divergence of the two A genomes at the genomic level. In comparison, conserved regions between the two B genomes were identified that included alpha-gliadin pseudogenes containing shared nested TE insertions. Analyses of the genomic organization and phylogenetic tree reconstruction indicate that although orthologous gene pairs derived from speciation were present, large portions of alpha-gliadin genes were likely derived from differential gene duplications or deletions after the separation of the homologous wheat genomes ~0.5 MYA. The higher number of full-length intact alpha-gliadin genes in hexaploid wheat than that in wild emmer suggests that human selection through domestication might have an impact on alpha-gliadin evolution.