The Relationship between Population Structure and Aluminum Tolerance in Cultivated Sorghum

Background: Acid soils comprise up to 50% of the world's arable lands and in these areas aluminum (Al) toxicity impairs root growth, strongly limiting crop yield. Food security is thereby compromised in many developing countries located in tropical and subtropical regions worldwide. In sorghum, SbMATE, an Al-activated citrate transporter, underlies the Alt(SB) locus on chromosome 3 and confers Al tolerance via Al-activated root citrate release. Methodology: Population structure was studied in 254 sorghum accessions representative of the diversity present in cultivated sorghums. Al tolerance was assessed as the degree of root growth inhibition in nutrient solution containing Al. A genetic analysis based on markers flanking Alt(SB) and SbMATE expression was undertaken to assess a possible role for Alt(SB) in Al tolerant accessions. In addition, the mode of gene action was estimated concerning the Al tolerance trait. Comparisons between models that include population structure were applied to assess the importance of each subpopulation to Al tolerance. Conclusion/Significance: Six subpopulations were revealed featuring specific racial and geographic origins. Al tolerance was found to be rather rare and present primarily in guinea and to lesser extent in caudatum subpopulations. Alt(SB) was found to play a role in Al tolerance in most of the Al tolerant accessions. A striking variation was observed in the mode of gene action for the Al tolerance trait, which ranged from almost complete recessivity to near complete dominance, with a higher frequency of partially recessive sources of Al tolerance. A possible interpretation of our results concerning the origin and evolution of Al tolerance in cultivated sorghum is discussed. This study demonstrates the importance of deeply exploring the crop diversity reservoir both for a comprehensive view of the dynamics underlying the distribution and function of Al tolerance genes and to design efficient molecular breeding strategies aimed at enhancing Al tolerance.CGIAR[G3007.04]McKnight FoundationFundacao de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG)National Council for Scientific and Technological Development (CNPq

Association mapping provides insights into the origin and the fine structure of the sorghum aluminum tolerance locus, AltSB

Root damage caused by aluminum (Al) toxicity is a major cause of grain yield reduction on acid soils, which are prevalent in tropical and subtropical regions of the world where food security is most tenuous. In sorghum, Al tolerance is conferred by SbMATE, an Al-activated root citrate efflux transporter that underlies the major Al tolerance locus, AltSB, on sorghum chromosome 3. We used association mapping to gain insights into the origin and evolution of Al tolerance in sorghum and to detect functional variants amenable to allele mining applications. Linkage disequilibrium across the AltSB locus decreased much faster than in previous reports in sorghum, and reached basal levels at approximately 1000 bp. Accordingly, intra-locus recombination events were found to be extensive. SNPs and indels highly associated with Al tolerance showed a narrow frequency range, between 0.06 and 0.1, suggesting a rather recent origin of Al tolerance mutations within AltSB. A haplotype network analysis suggested a single geographic and racial origin of causative mutations in primordial guinea domesticates in West Africa. Al tolerance assessment in accessions harboring recombinant haplotypes suggests that causative polymorphisms are localized to a ∼6 kb region including intronic polymorphisms and a transposon (MITE) insertion, whose size variation has been shown to be positively correlated with Al tolerance. The SNP with the strongest association signal, located in the second SbMATE intron, recovers 9 of the 14 highly Al tolerant accessions and 80% of all the Al tolerant and intermediately tolerant accessions in the association panel. Our results also demonstrate the pivotal importance of knowledge on the origin and evolution of Al tolerance mutations in molecular breeding applications. Allele mining strategies based on associated loci are expected to lead to the efficient identification, in diverse sorghum germplasm, of Al tolerant accessions able maintain grain yields under Al toxicity

Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the poaceae.

In several crop species within the Triticeae tribe of the grass family Poaceae, single major aluminum (Al) tolerance genes have been identified that effectively mitigate Al toxicity, a major abiotic constraint to crop production on acidic soils. However, the trait is quantitatively inherited in species within other tribes, and the possible ancestral relationships between major Al tolerance genes and QTL in the grasses remain unresolved. To help establish these relationships, we conducted a molecular genetic analysis of Al tolerance in sorghum and integrated our findings with those from previous studies performed in crop species belonging to different grass tribes. A single locus, AltSB, was found to control Al tolerance in two highly Al tolerant sorghum cultivars. Significant macrosynteny between sorghum and the Triticeae was observed for molecular markers closely linked to putatively orthologous Al tolerance loci present in the group 4 chromosomes of wheat, barley, and rye. However, AltSB was not located within the homeologous region of sorghum but rather mapped near the end of sorghum chromosome 3. Thus, AltSB not only is the first major Al tolerance gene mapped in a grass species that does not belong to the Triticeae, but also appears to be different from the major Al tolerance locus in the Triticeae. Intertribe map comparisons suggest that a major Al tolerance QTL on rice chromosome 1 is likely to be orthologous to AltSB, whereas another rice QTL on chromosome 3 is likely to correspond to the Triticeae group 4 Al tolerance locus. Therefore, this study demonstrates a clear evolutionary link between genes and QTL encoding the same trait in distantly related species within a single plant family

LD decay in the <i>Alt_SB</i> region.

<p>In red is the prediction obtained by fitting a nonlinear regression model of the squared correlation of allele frequencies (<i>r²</i>) as a function of physical distance between pairs of loci based on the drift-recombination model <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0087438#pone.0087438-Remington1" target="_blank">[40]</a>. The regression coefficient (<i>b₁</i>, **<i>p</i><0.0001) and the fraction of the total variance explained by the nonlinear model (1– SS_R/SS_T) are shown, where SS_R and SS_T are the sum of squares of error and total, respectively.</p

Model comparison for type I error control.

<p>Type I error distribution obtained with the naïve, Q₆, K and Q₆+ K models using 38 SSR loci and phenotypic traits related to Al tolerance. Under the expectation that the randomly distributed SSR loci are not associated with Al tolerance, models that properly control the type I error should show a uniform distribution of <i>p-</i>values along a diagonal line in the cumulative plot. Loci with MAF >0.1 were used.</p

Association analysis for polymorphisms in the <i>Alt_SB</i> region and Al tolerance.

<p>Association analysis with the Q₆+ K model was performed with <i>RNRG_5d</i>. (<b>A</b>) Statistical significance is expressed as –log₁₀(<i>p</i>) and the <i>p</i><0.01 threshold is represented by the red horizontal line. Polymorphisms are shown along the x-axis and are linked to the schematic below this graph which depicts their physical location in the 24.6 kb region where <i>SbMATE</i> (exons shown as gray boxes connected to black lines representing introns) was mapped on chromosome 3 (A1 to A5 depict amplicons harboring polymorphisms, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0087438#pone.0087438.s005" target="_blank">Table S5</a>). The corresponding physical positions in the sorghum genome are shown below the scale and were obtained by sequence similarity analysis (<a href="http://www.phytozome.net" target="_blank">http://www.phytozome.net</a>). The alleles at each loci are shown in the x-axis following the locus designation, with indels represented by the number of repeats, except for the MITE insertion, which was coded as described in the Material and Methods session. (<b>B</b>) Linkage disequilibrium expressed by pairwise <i>D’</i> estimates <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0087438#pone.0087438-Lewontin1" target="_blank">[65]</a> among loci associated with Al tolerance. <i>p</i>-values obtained with the Fisher exact test are shown. (<b>C</b>) Allele substitution effect for the 6083 locus. The slope of the linear regression line indicates an allele substitution effect of 53.9% <i>RNRG_5d</i> (<i>p</i><2E-16).</p