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, 7 (8), e1002221

Genetic Architecture of Aluminum Tolerance in Rice (Oryza Sativa) Determined Through Genome-Wide Association Analysis and QTL Mapping

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Genetic Architecture of Aluminum Tolerance in Rice (Oryza Sativa) Determined Through Genome-Wide Association Analysis and QTL Mapping

Adam N Famoso et al. PLoS Genet.

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Distribution of Al Tolerance in Rice Diversity Panel.
A) Distribution of Al tolerance across 383 diverse accessions of O. sativa at 160 µM Al3+. Aluminum tolerance (TRG-RRG) was normally distributed around a mean of 0.59 +/−0.24(SD) and ranged from 0.03–1.35. The Al tolerance of the QTL mapping parents are indicated: K = Kasalath, IR = IR64, N = Nipponbare, A = Azucena. B) Variation of Al tolerance (RRG) within genetic varietal groups (>80% ancestry). Admixed accessions share <80% ancestry with either group. The Japonica varietal group (temperate and tropical japonica and aromatic subpopulations) is significantly more tolerant than the Indica varietal group (indica and aus subpopulations) (p<0.0001). Five Indica accessions were identified to be highly Al tolerant outliers and six Japonica outlier accessions were identified, three as highly Al susceptible and three as highly tolerant.
Figure 2
Figure 2. QTLs Identified in IR64 × Azucena RIL Mapping Population.
A–C) Composite interval mapping output for QTL detected in the RIL mapping population using three Al tolerance RRG indices. The Y-axis is the LOD score and the horizontal line is the significant LOD threshold based on 1000 permutations. QTL name and approximate physical position are along bottom of figure and co-localization of QTLs identified with different Al tolerance indices are indicated with dashed vertical lines. A) Total root growth (TRG-RRG); B) Primary root growth (PRG-RRG); C) Longest root growth (LRG-RRG).
Figure 3
Figure 3. GWA Analysis of Al Tolerance within and across Rice Subpopulations.
GWA analysis across and within subpopulations (IND = indica; AUS = aus; TRJ = tropical japonica; TEJ = temperate japonica). A priori candidate genes are listed across the top, with those identified within 200 kb of significant SNPs colored red. Color bands indicate the 23 bi-parental QTL positions from previous reports (grey) or from this study (yellow). SNP color indicates co-localization with QTLs (blue) or candidate genes (red).
Figure 4
Figure 4. Haplotype analysis of the Nrat1 gene region.
A) Haplotypes observed in 373 accessions using the 44,000 SNP data. Haplotype 1 was unique to aus ancestry and associated with Al susceptibility within the aus subpopulation, explaining 40% of the Al tolerance variation within aus. Haplotypes 1, 2, and 3 share the same 4-SNP haplotype (id2001231-id2001243) flanking the Nrat1 gene (1.66 Mb). SNP positions are based on MSU6 annotation and subpopulations are abbreviated as follows: IND = indica, TEJ = temperate japonica, TRJ = tropical japonica, G.V. = groupV/aromatic, Admix = admixed lines without 80% ancestry to any one subpopulation. B) Haplotypes at the Nrat1 gene (1.66 Mb) in the (9) aus and (6) indica accessions sharing the 4-SNP haplotype flanking the Nrat1 gene. Polymorphisms are identified with numbers along bottom of figure. A STOP codon occurs in exon 13 between polymorphism 17 and 18. Gray shaded cells represent the reference allele and plant ID# 173 is the reference genotype ‘Nipponbare’. Yellow shaded cells represent polymorphisms in introns or synonymous polymorphisms in exons. Red shaded cells represent polymorphisms that result in amino acid substitutions (Indel or non-synonymous), unshaded cells marked with “−” indicate missing data, and +* indicates an intron insertion >500 bp.

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