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.
Highlights
Aluminum (Al) toxicity is the major constraint to crop productivity on acid soils, which comprise over 50% of the world’s arable land [1]
Using genome-wide association (GWA) and bi-parental quantitative trait loci (QTL) mapping, we investigated the genetic architecture of Al tolerance in rice
A one-way ANOVA demonstrated that subpopulation explained 57% of the phenotypic variation observed for Al tolerance (TRG-relative root growth (RRG)) among the 274 accessions that carried a subpopulation classification
Summary
Aluminum (Al) toxicity is the major constraint to crop productivity on acid soils, which comprise over 50% of the world’s arable land [1]. Cereal crops (Poaceae) have been a primary focus of Al tolerance research [2]. This research has demonstrated that levels of Al tolerance vary widely both within and between species [3,4,5,6,7,8]. Of the major cereal species that have been extensively studied (rice, maize, wheat, barley and sorghum), rice demonstrates superior Al tolerance under both field and hydroponic conditions [3,8]. Based on its high level of Al tolerance and numerous genetic and genomic resources, rice provides a good model for studying the genetics and physiology of Al tolerance
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