Sixty million years in evolution of soft grain trait in grasses: emergence of the softness locus in the common ancestor of Pooideae and Ehrhartoideae, after their divergence from Panicoideae

Mathieu Charles, Haibao Tang, Harry Belcram, Andrew Paterson, Piotr Gornicki, Boulos Chalhoub
Molecular Biology and Evolution 2009, 26 (7): 1651-61
Together maize, Sorghum, rice, and wheat grass (Poaceae) species are the most important cereal crops in the world and exhibit different "grain endosperm texture." This trait has been studied extensively in wheat because of its pivotal role in determining quality of products obtained from wheat grain. Grain softness protein-1 and Puroindolines A and B (grain storage proteins), encoded by Ha-like genes: Gsp-1, Pina, and Pinb, of the Hardness (Ha) locus, are the main determinants of the grain softness/hardness trait in wheat. The origin and evolution of grain endosperm texture in grasses was addressed by comparing genomic sequences of the Ha orthologous region of wheat, Brachypodium, rice, and Sorghum. Results show that the Ha-like genes are present in wheat and Brachypodium but are absent from Sorghum bicolor. A truncated remnant of an Ha-like gene is present in rice. Synteny analysis of the genomes of these grass species shows that only one of the paralogous Ha regions, created 70 My by whole-genome duplication, contained Ha-like genes. The comparative genome analysis and evolutionary comparison with genes encoding grain reserve proteins of grasses suggest that an ancestral Ha-like gene emerged, as a new member of the prolamin gene family, in a common ancestor of the Pooideae (Triticeae and Brachypoidieae tribes) and Ehrhartoideae (rice), between 60 and 50 My, after their divergence from Panicoideae (Sorghum). It was subsequently lost in Ehrhartoideae. Recurring duplications, deletions, and/or truncations occurred independently and appear to characterize Ha-like gene evolution in the grass species. The Ha-like genes gained a new function in Triticeae, such as wheat, underlying the soft grain phenotype. Loss of these genes in some wheat species leads, in turn, to hard endosperm seeds.

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