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

Naxin Huo, Tingting Zhu, Shengli Zhang, Toni Mohr, Ming Cheng Luo, Jong Yeol Lee, Assaf Distelfeld, Susan Altenbach, Yong Q. Gu

Research output: Contribution to journalArticlepeer-review

Abstract

α-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). α-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 α-gliadins were characterized from the tetraploid wild emmer, a 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 24 and 16 α-gliadin genes were identified for the A and B genome regions, respectively. α-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 α-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 α-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 α-gliadin genes in hexaploid wheat than that in wild emmer suggests that human selection through domestication might have an impact on α-gliadin evolution. Our study provides insights into the rapid and dynamic evolution of genomic regions harboring the α-gliadin genes in wheat.

Original languageEnglish
Pages (from-to)993-1005
Number of pages13
JournalFunctional and Integrative Genomics
Volume19
Issue number6
DOIs
StatePublished - 1 Nov 2019
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported from grants from the National Science Foundation (IOS 1238231), Next-Generation BioGreen 21 Program (RDA PJ013149), South Korea, National Natural Science Foundation of China (Grants 31571667 and U1204315), and USDA-Agricultural Research Service CRIS project (2030-21430-014). Mention of trade names or commercial project is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. USDA is an equal opportunity provider and employer.

Publisher Copyright:
© 2019, The Author(s).

Keywords

  • Celiac disease
  • Gene duplication
  • Genome evolution
  • Phylogeny
  • Wheat gluten proteins
  • α-Gliadin gene family

ASJC Scopus subject areas

  • Genetics

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