New insights into structural organization and gene duplication in a 1.75‐Mb genomic region harboring the α‐gliadin gene family in Aegilops tauschii, the source of wheat D genome

Abstract

Among the wheat prolamins important for its end-use traits, α-gliadins are the most abundant, and are also a major cause of food-related allergies and intolerances. Previous studies of various wheat species estimated that between 25 and 150 α-gliadin genes reside in the Gli-2 locus regions. To better understand the evolution of this complex gene family, the DNA sequence of a 1.75-Mb genomic region spanning the Gli-2 locus was analyzed in the diploid grass, Aegilops tauschii, the ancestral source of D genome in hexaploid bread wheat. Comparison with orthologous regions from rice, sorghum, and Brachypodium revealed rapid and dynamic changes only occurring to the Ae. tauschii Gli-2 region, including insertions of high numbers of non-syntenic genes and a high rate of tandem gene duplications, the latter of which have given rise to 12 copies of α-gliadin genes clustered within a 550-kb region. Among them, five copies have undergone pseudogenization by various mutation events. Insights into the evolutionary relationship of the duplicated α-gliadin genes were obtained from their genomic organization, transcription patterns, transposable element insertions and phylogenetic analyses. An ancestral glutamate-like receptor (GLR) gene encoding putative amino acid sensor in all four grass species has duplicated only in Ae. tauschii and generated three more copies that are interspersed with the α-gliadin genes. Phylogenetic inference and different gene expression patterns support functional divergence of the Ae. tauschii GLR copies after duplication. Our results suggest that the duplicates of α-gliadin and GLR genes have likely taken different evolutionary paths; conservation for the former and neofunctionalization for the latter.

Gene Duplication and Evolution Dynamics in the Homeologous Regions Harboring Multiple Prolamin and Resistance Gene Families in Hexaploid Wheat

“…The identification of a full complement of prolamin genes allowed us to map transcriptome reads to individual prolamin genes, providing a more accurate view of their expression. Mapping the transcriptome reads to the annotated gene set is also useful in validating the prolamin gene assembly manually ( Huo et al, 2017 ). Through this process, all 27 prolamin pseudogene sequences were confirmed, indicating that the high rate of pseudogenes (49%) is likely associated with the dynamic sequence evolution in the analyzed regions.…”

“…Therefore, one can speculate that the prolamin genes in Glu-3 and Gli-1 loci might originate from an ancestral gene related to HMW-GS. We exclude α-gliadins from the origin of Glu-3 and Gli-1 loci because they are the youngest group of wheat prolamin that evolved after the divergence of wheat and rye ∼7–8 million years ago ( Huo et al, 2017 ). On the contrary, R genes are present in many genetic loci.…”

Dynamic Evolution of α-Gliadin Prolamin Gene Family in Homeologous Genomes of Hexaploid Wheat

“…Of the three major genomic regions harboring wheat prolamin genes, the Gli-2 loci encoding α-gliadins are the youngest by evolution, as closely related species in Triticeae tribe such as barley and rye do not carry α-gliadin genes 24 . The α-gliadin gene family is also the most complex with estimates of copy numbers ranging from 25 to 150 in different wheat cultivars and ancestral species 25 , 26 .…”

Analysis of the Gli‐D2 locus identifies a genetic target for simultaneously improving the breadmaking and health‐related traits of common wheat

“…The physical relationships among the four contigs were deduced based on comparison with the Gli-D t 2 locus of Ae. tauschii (Huo et al, 2017) (Figure 1). D2ctg1, -2 and -4 each exhibited >95% identity with their corresponding segments in Gli-D t 2.…”