Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome

Authors: ZHAO, KEYAN - Cornell University; WRIGHT, MARK - Cornell University; KIMBALL, JENNIFER - Cornell University; Eizenga, Georgia; McClung, Anna; KOVACH, MICHAEL - Cornell University; TYAGI, WRICHA - Cornell University; ALI, M. LIAKAT - Arkansas Agricultural Experiment Station; TUNG, CHIH-WEI - Cornell University; REYNOLDS, ANDY - Cornell University; BUSTAMANTE, CARLOS - Cornell University; MCCOUCH, SUSAN - Cornell University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2010
Publication Date: 5/10/2010
Citation: Zhao, K., Wright, M.K., Kimball, J.A., Eizenga, G.C., McClung, A.M., Kovach, M.J., Tyagi, W., Ali, M., Tung, C., Reynolds, A., Bustamante, C.D., McCouch, S.R. 2010. Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS One. 5(5):e10780. doi: 10.1371/journal.pone.0010780..

Interpretive Summary: Two different varietal groups of cultivated rice, Indica and Japonica, have been recognized since ancient times, suggesting rice was domesticated by man two different times from wild ancestral species. In general, indica rice and japonica rice have different plant and seed characteristics, and are adapted to different regions of the world. In 1982, a report suggested the two varietal groups could be further divided into five different groups identified as indica, aus, temperate japonica, tropical japonica, and aromatic. This study was conducted to look at the genotypic differences between a diverse collection of 395 rice cultivars (accessions) from the world’s rice-growing regions using a set of new DNA markers, called SNP (single nucleotide polymorphism) markers. Data analysis validated that the previously reported five major varietal groups were present in this collection and revealed that desirable traits were moved from one varietal group to another through crossing between the different groups, especially between the indica and japonica groups. Specifically, we identified chromosomal regions where a short plant height gene and a blast resistance gene from selected indica rice cultivars were recently incorporated into some tropical japonica rice cultivars; a desirable starch (amylose) gene from temperate japonica rice was incorporated into some indica rice cultivars; and the gene for longer grain length found in tropical japonica was incorporated into some indica rice cultivars. These results highlight how the new SNP markers can be used to genetically fingerprint important agronomic traits in individual rice cultivars. Ultimately, this information can be used by rice breeders to move desirable traits found in selected rice cultivars across varietal groups and develop improved rice cultivars.

Technical Abstract: The domestication of Asian rice (Oryza sativa) was a complex process and substantial ambiguity remains regarding the timing, number, and locations of domestication events. Deep genetic divergence between the two main varietal groups (Indica and Japonica) suggests at least two independent domestications from distinct wild populations. However, genetic uniformity surrounding key domestication genes across divergent subpopulations suggests cultural exchange of genetic material among ancient farmers and breeders. In this study, we utilize a novel 1,536 SNP panel genotyped across 395 diverse accessions of O. sativa to study genome-wide patterns of polymorphism, characterize population structure, and infer the introgression history of domesticated Asian rice. Our population structure analyses support the existence of five major subpopulations (indica, aus, tropical japonica, temperate japonica and aromatic/GroupV) consistent with previous analyses. Our introgression analysis shows that most accessions exhibit some degree of admixture, with many individuals within a population sharing the same introgressed segment due to artificial selection. Genes in these regions control a myriad of traits including plant stature, blast resistance, and amylose content. Admixture mapping and association analysis of amylose content and grain length illustrate the potential for dissecting the genetic basis of complex traits in domesticated plant populations. These analyses highlight the power of population genomics in agricultural systems to identify functionally important regions of the genome and to decipher the role of human-directed breeding in refashioning the genomes and population structure of a domesticated species.