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Location: Cereal Crops Research

Title: Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat

item Zhang, Zengcui
item Belcram, Harry
item Gornicki, Piotr
item Charles, Mathieu
item Just, Jérémy
item Huneau, Cécile
item Magdelenat, Ghislaine
item Couloux, Arnaud
item Samain, Sylvie
item Gill, Bikram
item Rasmussen, Jack
item Barbe, Valérie
item Faris, Justin
item Chalhoub, Boulos

Submitted to: Proceedings of the National Academy of Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2011
Publication Date: 11/15/2011
Citation: Zhang, Z., Belcram, H., Gornicki, P., Charles, M., Just, J., Huneau, C., Magdelenat, G., Couloux, A., Samain, S., Gill, B.S., Rasmussen, J.B., Barbe, V., Faris, J.D., Chalhoub, B. 2011. Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proceedings of the National Academy of Sciences. 108:18737-18742.

Interpretive Summary: The Q gene of wheat is an important domestication gene because it confers the free-threshing character, i.e. it allows the grain to easily be separated from the chaff by mechanical means. A mutation that occurred approximately 10,000 years ago in the primitive form of the gene, known as q, gave rise to Q resulting in the acquisition of this and other domestication traits. The Q gene on wheat chromosome 5A (5AQ) has been studied extensively for the past century, but the related forms of the gene known as 5Bq and 5Dq that exist on homoeologous chromosomes 5B and 5D of polyploid wheat have not been analyzed. Here, we studied the structure and function of the Q/q genes in wheat and some of its relatives to determine their evolutionary fates and contributions to wheat domestication. Our analysis revealed that a duplication of the primitive 5Aq gene occurred 5.8 million years ago, and was likely followed by selective loss of one of the copies from the A-genome progenitor of modern wheat and the other copy from the B and D genome progenitors. The 5Bq gene underwent pseudogenization, or non-functionalization fairly recently, but still influences domestication traits through the regulation of expression of the other Q/q genes. The 5Dq gene is fully intact and functional, and contributes to domestication traits directly. Therefore, whereas the mutation that occurred in 5Aq to give rise to 5AQ resulted in profound effects on domestication traits and led to the rapid spread of agriculture around the world, the 5Bq and 5Dq genes are also necessary for full expression of the wheat domestication syndrome.

Technical Abstract: The Q gene encodes an AP2-like transcription factor that played an important role in domestication of polyploid wheat. The chromosome 5A Q alleles (5AQ and 5Aq) have been well studied, but much less is known about the q alleles on wheat homoeologous chromosomes 5B (5Bq) and 5D (5Dq). We investigated the organization, evolution, and function of the Q/q homoeoalleles in hexaploid wheat (Triticum aestivum L.). Q/q gene sequences are highly conserved within and among the A, B, and D genomes of hexaploid wheat, the A and B genomes of tetraploid wheat, and the A, S, and D genomes of the diploid progenitors, but the intergenic regions of the Q/q locus are highly divergent among homoeologous genomes. Duplication of the q gene 5.8 MYA was likely followed by selective loss of one of the copies from the A-genome progenitor and the other copy from the B, D, and S genomes. A recent V329 to I mutation in the A lineage is correlated with the Q phenotype. The 5Bq homoeoallele became a pseudogene after allotetraploidization. Expression analysis indicated that the homoeoalleles are co-regulated in a complex manner. Combined phenotypic and expression analysis indicated that, whereas 5AQ plays a major role in conferring domestication-related traits, 5Dq contributes to suppression of the speltoid phenotype directly and 5Bq indirectly, especially in the absence of 5AQ. The evolution of the Q/q loci in polyploid wheat resulted in the hyper-functionalization of 5AQ, pseudogenization of 5Bq, and sub-functionalization of 5Dq, all contributing to the domestication traits.