Rapid evolutionary dynamics in a 2.8‐Mb chromosomal region containing multiple prolamin and resistance gene families in Aegilops tauschii

Abstract

Prolamin and resistance gene families are important in wheat food use and in defense against pathogen attacks, respectively. To better understand the evolution of these multi-gene families, the DNA sequence of a 2.8-Mb genomic region, representing an 8.8 cM genetic interval and harboring multiple prolamin and resistance-like gene families, was analyzed in the diploid grass Aegilops tauschii, the D-genome donor of bread wheat. Comparison with orthologous regions from rice, Brachypodium, and sorghum showed that the Ae. tauschii region has undergone dramatic changes; it has acquired more than 80 non-syntenic genes and only 13 ancestral genes are shared among these grass species. These non-syntenic genes, including prolamin and resistance-like genes, originated from various genomic regions and likely moved to their present locations via sequence evolution processes involving gene duplication and translocation. Local duplication of non-syntenic genes contributed significantly to the expansion of gene families. Our analysis indicates that the insertion of prolamin-related genes occurred prior to the separation of the Brachypodieae and Triticeae lineages. Unlike in Brachypodium, inserted prolamin genes have rapidly evolved and expanded to encode different classes of major seed storage proteins in Triticeae species. Phylogenetic analyses also showed that the multiple insertions of resistance-like genes and subsequent differential expansion of each R gene family. The high frequency of non-syntenic genes and rapid local gene evolution correlate with the high recombination rate in the 2.8-Mb region with nine-fold higher than the genome-wide average. Our results demonstrate complex evolutionary dynamics in this agronomically important region of Triticeae species.

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

“…The short arms of the same chromosomes carry the Glu‐3 loci encoding the LMW glutenins and the Gli‐1 loci encoding γ‐, δ‐ and ω‐gliadins (Anderson et al ., ; Dong et al ., ). The Glu‐3 and Gli‐1 loci are more complex than the Glu‐1 loci because they are tightly linked and each contains multiple prolamin genes.…”

“…Because the sequenced BACs were identified by hybridization to prolamin gene‐derived probes, and thus did not span the entire Glu‐3/Gli‐1 loci, the knowledge gained from these studies was useful, but not complete. Recently, a large BAC‐based physical contig covering a 2.8‐Mb genomic region and spanning both the Glu‐3 and Gli‐1 loci was identified and completely sequenced from a diploid Aegilops tauschii species, the D‐genome donor of hexaploid wheat (Dong et al ., ). The study delineated the genomic structural organization of genes encoding LMW glutenins and γ‐, δ‐ and ω‐gliadins.…”

“…These non‐syntenic genes originated from independent gene insertions followed by local/tandem duplications. The observation that the prolamin and disease resistance genes are often interspersed with each other supports the hypothesis that they co‐evolved in the region (Dong et al ., ).…”

Genome-wide analysis of complex wheat gliadins, the dominant carriers of celiac disease epitopes

“…A partial sequencing of bread wheat Gli-A2, -B2 and -D2 loci, approximately 200 kb for each locus, has been reported, with 12 active and four inactive α-gliadin genes identified15. A recent study has sequenced a chromosomal region harboring the entire Gli-D t 1 locus of Aegilops tauschii , which is orthologous to Gli-D1 16. In Gli-D t 1 , six ω-gliadin, four γ-gliadin and two δ-gliadin genes are found in a genomic DNA segment of about 888.5 kb, and for all three types of gliadin genes, there are both active and pseudogene members.…”

Highly Genotype- and Tissue-specific Single-Parent Expression Drives Dynamic Gene Expression Complementation in Maize Hybrids

“…Non-syntenic genes have been proposed to contribute to the adaptation of plants to fluctuating environments. For example, disease resistance genes were found to be enriched in the non-syntenic portion of the Arabidopsis thaliana (Freeling et al, 2008), Oryza sativa (Xu et al, 2011), and Aegilops tauschii (Dong et al, 2016) genomes.…”