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Genome-wide association mapping of root traits in a japonica rice panel.

Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Gozé E, Kilian A, Ahmadi N, Dingkuhn M - PLoS ONE (2013)

Bottom Line: Nineteen associations were significant at P<1e-05, and 78 were significant at P<1e-04.The greatest numbers of significant associations were detected for deep root mass and the number of deep roots, whereas no significant associations were found for total root biomass or deep root proportion.Several likely candidate genes were found in close proximity to these loci.

View Article: PubMed Central - PubMed

Affiliation: Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR AGAP, Montpellier, France.

ABSTRACT
Rice is a crop prone to drought stress in upland and rainfed lowland ecosystems. A deep root system is recognized as the best drought avoidance mechanism. Genome-wide association mapping offers higher resolution for locating quantitative trait loci (QTLs) than QTL mapping in biparental populations. We performed an association mapping study for root traits using a panel of 167 japonica accessions, mostly of tropical origin. The panel was genotyped at an average density of one marker per 22.5 kb using genotyping by sequencing technology. The linkage disequilibrium in the panel was high (r(2)>0.6, on average, for 20 kb mean distances between markers). The plants were grown in transparent 50 cm × 20 cm × 2 cm Plexiglas nailboard sandwiches filled with 1.5 mm glass beads through which a nutrient solution was circulated. Root system architecture and biomass traits were measured in 30-day-old plants. The panel showed a moderate to high diversity in the various traits, particularly for deep (below 30 cm depth) root mass and the number of deep roots. Association analyses were conducted using a mixed model involving both population structure and kinship to control for false positives. Nineteen associations were significant at P<1e-05, and 78 were significant at P<1e-04. The greatest numbers of significant associations were detected for deep root mass and the number of deep roots, whereas no significant associations were found for total root biomass or deep root proportion. Because several QTLs for different traits were co-localized, 51 unique loci were detected; several co-localized with meta-QTLs for root traits, but none co-localized with rice genes known to be involved in root growth. Several likely candidate genes were found in close proximity to these loci. Additional work is necessary to assess whether these markers are relevant in other backgrounds and whether the genes identified are robust candidates.

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Manhattan plots for four selected root traits.The negative log10-transformed p-values of each test are plotted against the marker position in the genome. Full line: P=1e-05; dotted line: P=5e-04.RBB30 = root mass below 30 cm; DRB = deep root biomass; NBR_30 = number of roots below 30 cm; LENGTH = maximum root length; .
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pone-0078037-g006: Manhattan plots for four selected root traits.The negative log10-transformed p-values of each test are plotted against the marker position in the genome. Full line: P=1e-05; dotted line: P=5e-04.RBB30 = root mass below 30 cm; DRB = deep root biomass; NBR_30 = number of roots below 30 cm; LENGTH = maximum root length; .

Mentions: Most phenotypic traits were affected by panel structure in similar ways. The comparison of the BICs of the three models (GLM, MLM1 and MLM2) showed that MLM2, which included both the population structure and kinship matrix, was the best model for almost all traits (Table 5). MLM1, which included only the kinship matrix, was the best model for NBT, PB and SB. GLM, which included only population structure, was always inferior to the two other models. The smaller number of false positives in MLM compared to GLM is illustrated by the cumulative distribution of p-values compared to the uniform distribution, as shown on the quantile-quantile plots for DRB, LENGTH and NBR_30 (Figure 5). The synthetic results of the association mapping run with the best model for each trait are presented in Table 6. The Manhattan plots for four selected root traits (RBB30, DRB, NBR_30 and LENGTH) are presented in Figure 6. Nineteen markers were significantly associated with a trait at P<1e-05, which corresponded to a q-value below 0.05; 78 markers were significantly associated with a trait at P<1e-04, which corresponded to a q-value below 0.05 in 30 cases (38%) and to a q-value between 0.05 and 0.10 in 28 cases (36%), with the remaining 20 markers having q-values above 0.10. In a few cases, several markers belonging to the same chromosome segment in full LD were found to have the exact same level of significance (e.g., SNPs in the interval from 34,890,451-34,939,105 bp on chromosome 1 for a range of traits). These segments were less than 50 kb in length, except for one interval on chromosome 8 (460 kb). The number of significant markers at P<1e-04 varied among traits, from 0 to 17. DRB and RBB30, the two traits showing the largest range of phenotypic variation, and NBT were associated with the highest number of significant markers, whereas no significant associations were detected for RB or DRP. Some markers were significantly associated with several traits, which meant that only 51 different sites or segments were found to be significant at P<1e-04 for one of the traits. Among those 51 loci, 53% had a minor allele frequency of less than 10%, which corresponded to the representation of markers with low minor allele frequency in the marker set. Two groups of traits had a high level of co-localization of the significant loci. The first group was composed of traits describing root depth (DRP, RBB30 and NBR_30), with 15 loci significant for two traits (on chromosomes 1, 2, 3, 4, 7, 8, 10, 11 and 12) and five loci significant for all three traits (on chromosomes 1, 2, 7 and 10) among the 24 loci with significance for any of the three traits. RB2030, LENGTH, DEPTH and ACP1 were also related to this first group. The second group of traits was composed of SB, PB and RB0020; among the six loci significant for any of the traits (on chromosomes 4, 5, 7 and 11), four were significant for all three traits. NBT was associated with this group, as was RB, but this association was less clear because the levels of significance were lower for this trait. R_S co-localized erratically. One trait, LLGTH, was almost independent, and another trait, ANGLE, was fully independent of the other traits.


Genome-wide association mapping of root traits in a japonica rice panel.

Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Gozé E, Kilian A, Ahmadi N, Dingkuhn M - PLoS ONE (2013)

Manhattan plots for four selected root traits.The negative log10-transformed p-values of each test are plotted against the marker position in the genome. Full line: P=1e-05; dotted line: P=5e-04.RBB30 = root mass below 30 cm; DRB = deep root biomass; NBR_30 = number of roots below 30 cm; LENGTH = maximum root length; .
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3818351&req=5

pone-0078037-g006: Manhattan plots for four selected root traits.The negative log10-transformed p-values of each test are plotted against the marker position in the genome. Full line: P=1e-05; dotted line: P=5e-04.RBB30 = root mass below 30 cm; DRB = deep root biomass; NBR_30 = number of roots below 30 cm; LENGTH = maximum root length; .
Mentions: Most phenotypic traits were affected by panel structure in similar ways. The comparison of the BICs of the three models (GLM, MLM1 and MLM2) showed that MLM2, which included both the population structure and kinship matrix, was the best model for almost all traits (Table 5). MLM1, which included only the kinship matrix, was the best model for NBT, PB and SB. GLM, which included only population structure, was always inferior to the two other models. The smaller number of false positives in MLM compared to GLM is illustrated by the cumulative distribution of p-values compared to the uniform distribution, as shown on the quantile-quantile plots for DRB, LENGTH and NBR_30 (Figure 5). The synthetic results of the association mapping run with the best model for each trait are presented in Table 6. The Manhattan plots for four selected root traits (RBB30, DRB, NBR_30 and LENGTH) are presented in Figure 6. Nineteen markers were significantly associated with a trait at P<1e-05, which corresponded to a q-value below 0.05; 78 markers were significantly associated with a trait at P<1e-04, which corresponded to a q-value below 0.05 in 30 cases (38%) and to a q-value between 0.05 and 0.10 in 28 cases (36%), with the remaining 20 markers having q-values above 0.10. In a few cases, several markers belonging to the same chromosome segment in full LD were found to have the exact same level of significance (e.g., SNPs in the interval from 34,890,451-34,939,105 bp on chromosome 1 for a range of traits). These segments were less than 50 kb in length, except for one interval on chromosome 8 (460 kb). The number of significant markers at P<1e-04 varied among traits, from 0 to 17. DRB and RBB30, the two traits showing the largest range of phenotypic variation, and NBT were associated with the highest number of significant markers, whereas no significant associations were detected for RB or DRP. Some markers were significantly associated with several traits, which meant that only 51 different sites or segments were found to be significant at P<1e-04 for one of the traits. Among those 51 loci, 53% had a minor allele frequency of less than 10%, which corresponded to the representation of markers with low minor allele frequency in the marker set. Two groups of traits had a high level of co-localization of the significant loci. The first group was composed of traits describing root depth (DRP, RBB30 and NBR_30), with 15 loci significant for two traits (on chromosomes 1, 2, 3, 4, 7, 8, 10, 11 and 12) and five loci significant for all three traits (on chromosomes 1, 2, 7 and 10) among the 24 loci with significance for any of the three traits. RB2030, LENGTH, DEPTH and ACP1 were also related to this first group. The second group of traits was composed of SB, PB and RB0020; among the six loci significant for any of the traits (on chromosomes 4, 5, 7 and 11), four were significant for all three traits. NBT was associated with this group, as was RB, but this association was less clear because the levels of significance were lower for this trait. R_S co-localized erratically. One trait, LLGTH, was almost independent, and another trait, ANGLE, was fully independent of the other traits.

Bottom Line: Nineteen associations were significant at P<1e-05, and 78 were significant at P<1e-04.The greatest numbers of significant associations were detected for deep root mass and the number of deep roots, whereas no significant associations were found for total root biomass or deep root proportion.Several likely candidate genes were found in close proximity to these loci.

View Article: PubMed Central - PubMed

Affiliation: Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR AGAP, Montpellier, France.

ABSTRACT
Rice is a crop prone to drought stress in upland and rainfed lowland ecosystems. A deep root system is recognized as the best drought avoidance mechanism. Genome-wide association mapping offers higher resolution for locating quantitative trait loci (QTLs) than QTL mapping in biparental populations. We performed an association mapping study for root traits using a panel of 167 japonica accessions, mostly of tropical origin. The panel was genotyped at an average density of one marker per 22.5 kb using genotyping by sequencing technology. The linkage disequilibrium in the panel was high (r(2)>0.6, on average, for 20 kb mean distances between markers). The plants were grown in transparent 50 cm × 20 cm × 2 cm Plexiglas nailboard sandwiches filled with 1.5 mm glass beads through which a nutrient solution was circulated. Root system architecture and biomass traits were measured in 30-day-old plants. The panel showed a moderate to high diversity in the various traits, particularly for deep (below 30 cm depth) root mass and the number of deep roots. Association analyses were conducted using a mixed model involving both population structure and kinship to control for false positives. Nineteen associations were significant at P<1e-05, and 78 were significant at P<1e-04. The greatest numbers of significant associations were detected for deep root mass and the number of deep roots, whereas no significant associations were found for total root biomass or deep root proportion. Because several QTLs for different traits were co-localized, 51 unique loci were detected; several co-localized with meta-QTLs for root traits, but none co-localized with rice genes known to be involved in root growth. Several likely candidate genes were found in close proximity to these loci. Additional work is necessary to assess whether these markers are relevant in other backgrounds and whether the genes identified are robust candidates.

Show MeSH
Related in: MedlinePlus