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

item DONG, L - University Of California
item HUO, NAXIN - University Of California
item WANG, Y - University Of California
item DEAL, K - University Of California
item WANG, D - Chinese Academy Of Sciences
item HU, D - Henan Institute Of Science And Technology
item DVORAK, J - University Of California
item Anderson, Olin
item LUO, M-C - University Of California
item Gu, Yong

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2016
Publication Date: 5/26/2016
Citation: Dong, L., Huo, N., Wang, Y., Deal, K., Wang, D., Hu, D., Dvorak, J., Anderson, O.D., Luo, M., Gu, Y.Q. 2016. Rapid evolutionary dynamics in a 2.8-Mb chromosomal region containing multiple prolamin and resistance gene families in Aegilops tauschii. Plant Journal. doi: 10.111/tpi.13214.

Interpretive Summary: Wheat (Triticum aestivum) accounts for approximately 30% of the global cereal consumption. Prolamins, the major seed storage proteins of wheat, provide nitrogen to build proteins during the early phase of seed germination, are an important cereal protein source for human beings, and determine the bread-making quality of wheat flour. Disease resistance is another important trait that protects the wheat plants against pathogen attacks. Both these traits are the products of the combined activities of large gene families. To better understand the evolution, structure and functions of wheat prolamin and resistance genes, we employed the available genomics resources from Aegilops tauschii (Tausch’s goatgrass), one of the three ancestors of modern bread wheat. In this study, we identified, sequenced, and analyzed a 2.8 million base pair segment of Aegilops tauschii genomic DNA. We compared that sequence to the comparable regions of rice, sorghum and the wild grass Brachypodium. We found that Aegilops tauschii contains many more members of both the prolamin and resistance gene families than the other grasses. The new genes were added to this region by rapid and dynamic evolution after the separation of the Brachypodia and Triticeae lineages and before wheat domestication. These results show that multi-gene families can expand rapidly during evolution, providing new variants on which natural and human selection can act.

Technical Abstract: The prolamin (seed storage proteins high in glutamine and proline) and resistance gene families are important in domesticated bread wheat (Triticum aestivum) food uses 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 wheat Ae. tauschii, the D genome donor of bread wheat. Comparisons of the Ae. tauschii genome sequence with orthologous regions from rice, Brachypodium, and sorghum showed that it has undergone dramatic changes by acquiring more than 80 non-syntenic genes in this DNA region. Only 13 ancestral genes are shared among these grass species. A large number of non-syntenic genes including these prolamin and resistance-like genes originated from various genomic regions and likely moved to their present locations via mechanisms involving gene duplication and translocation. However, local duplication of non-syntenic genes also contributed significantly to the expansion of gene families. In addition, we found the insertion of prolamin-like genes occurred prior to the separation of the Brachypodieae and Triticeae lineages. Unlike in Brachypodium, these inserted prolamin genes have rapidly evolved and expanded to encode different classes of the major seed storage proteins in Triticeae species. Phylogenetic analyses also indicated that multiple insertions of resistance-like genes occurred in this 2.8 Mb region and subsequently experienced different evolutionary paths, resulting in differential expansion of each R gene family. The high frequency of non-syntenic genes, compared to other grasses, and rapid local gene evolution rates correlate with the high recombination rate in this region. Our results provide better understanding of the evolution of two agronomically important gene families in Triticeae species.