Genetic Architecture of Aluminum Tolerance in Rice (Oryza sativa) Determined through Genome-Wide Association Analysis and QTL Mapping
Top Cited Papers
Open Access
- 4 August 2011
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Genetics
- Vol. 7 (8), e1002221
- https://doi.org/10.1371/journal.pgen.1002221
Abstract
Aluminum (Al) toxicity is a primary limitation to crop productivity on acid soils, and rice has been demonstrated to be significantly more Al tolerant than other cereal crops. However, the mechanisms of rice Al tolerance are largely unknown, and no genes underlying natural variation have been reported. We screened 383 diverse rice accessions, conducted a genome-wide association (GWA) study, and conducted QTL mapping in two bi-parental populations using three estimates of Al tolerance based on root growth. Subpopulation structure explained 57% of the phenotypic variation, and the mean Al tolerance in Japonica was twice that of Indica. Forty-eight regions associated with Al tolerance were identified by GWA analysis, most of which were subpopulation-specific. Four of these regions co-localized with a priori candidate genes, and two highly significant regions co-localized with previously identified QTLs. Three regions corresponding to induced Al-sensitive rice mutants (ART1, STAR2, Nrat1) were identified through bi-parental QTL mapping or GWA to be involved in natural variation for Al tolerance. Haplotype analysis around the Nrat1 gene identified susceptible and tolerant haplotypes explaining 40% of the Al tolerance variation within the aus subpopulation, and sequence analysis of Nrat1 identified a trio of non-synonymous mutations predictive of Al sensitivity in our diversity panel. GWA analysis discovered more phenotype–genotype associations and provided higher resolution, but QTL mapping identified critical rare and/or subpopulation-specific alleles not detected by GWA analysis. Mapping using Indica/Japonica populations identified QTLs associated with transgressive variation where alleles from a susceptible aus or indica parent enhanced Al tolerance in a tolerant Japonica background. This work supports the hypothesis that selectively introgressing alleles across subpopulations is an efficient approach for trait enhancement in plant breeding programs and demonstrates the fundamental importance of subpopulation in interpreting and manipulating the genetics of complex traits in rice. While rice (Oryza sativa) is significantly more Al tolerant than other cereals, no genes underlying Al tolerance in rice have been reported. Using genome-wide association (GWA) and bi-parental QTL mapping, we investigated the genetic architecture of Al tolerance in rice. Japonica varieties were twice as Al tolerant as indica and aus varieties. Overall, 57% of the phenotypic variation was correlated with subpopulation, consistent with observations that different genes and genomic regions were associated with Al tolerance in different subpopulations. Four regions identified by GWA co-localized with a priori candidate genes, and two highly significant regions co-localized with previously identified quantitative trait loci (QTL). Haplotype and sequence analysis around the candidate gene, Nrat1, identified a susceptible haplotype explaining 40% of the Al tolerance variation within the aus subpopulation and three non-synonymous mutations within Nrat1 that were predictive of Al sensitivity. Using Indica × Japonica mapping populations, we identified QTLs associated with transgressive variation where alleles from a susceptible indica or aus parent enhanced Al tolerance in a tolerant japonica background. This work demonstrates the importance of subpopulation in interpreting and manipulating complex traits in rice and provides a roadmap for breeders aiming to capture genetic value from phenotypically inferior lines.Keywords
This publication has 79 references indexed in Scilit:
- Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativaNature Communications, 2011
- Genome-wide association studies of 14 agronomic traits in rice landracesNature Genetics, 2010
- Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred linesNature, 2010
- Leveraging natural diversity: back through the bottleneckCurrent Opinion in Plant Biology, 2008
- New insights into the history of rice domesticationTrends in Genetics, 2007
- Recombination and linkage disequilibrium in Arabidopsis thalianaNature Genetics, 2007
- Principal components analysis corrects for stratification in genome-wide association studiesNature Genetics, 2006
- Phylogeography of Asian wild rice, Oryza rufipogon , reveals multiple independent domestications of cultivated rice, Oryza sativaProceedings of the National Academy of Sciences of the United States of America, 2006
- A unified mixed-model method for association mapping that accounts for multiple levels of relatednessNature Genetics, 2005
- QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stagesTheoretical and Applied Genetics, 2000