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

Differential responses of sorghum genotypes for tolerance to aluminum in nutrient solutions

Neste trabalho utilizou-se uma técnica de solução nutritiva para identificar, dentre 391 linhagens de sorgo (181 do BAG-sorgo, 71 do CNPMS, 17 do SEPON/ICRISAT, e 122 da coleção de sorgo sacarino), os genótipos que apresentam tolerância ao alumínio. A avaliação do comportamento diferencial dessas linhagens baseou-se no crescimento da raiz seminal primária de plantas jovens de sorgo, em solução nutritiva contendo níveis variados de Al (0,0; 2,25; e 4,5 mg de Al/l para sorgo granífero e 0,0; 2,5; e 5,0 mg de Al/l para sorgo sacarino). A característica usada para a comparação entre genótipos foi o comprimento relativo da raiz seminal (CRSS = CRS+Al/CRS-Al onde CRS = comprimento da raiz seminal). Baseando-se na distribuição percentual dos valores de CRRS, obtidos nas diferentes linhagens, e nos valores de CRRS, encontrados nos materiais controles SC 208 (sensível ao Al) e SC 283 (tolerante ao Al), três classes de resposta ao alumínio foram identificadas: sensível (CRRS 0,70). Dentre os materiais avaliados as seguintes linhagens apresentaram tolerância aos níveis de 4,5 ou 5,0 mg de Al/l: IS 3625, IS 7173 C (SC 283), IS 12666, 5DX61/6/2, 3DX57/1/1/910, 156-P-5-Serere-1, 9DX9/11, Brandes, MN 4004 e MN 1204. O processo mostrou-se eficiente na avaliação de grande número de linhagem, quando se visa a tolerância ao alumínio, sendo recomendada como técnica auxiliar em programas de melhoramento.A nutrient solution technique was used to screen 391 sorghum genotypes (181 from BAG-sorghum, 71 from CNPMS, 17 SEPON from ICRISAT and 122 from sweet sorghum collection) for Al tolerance. The differential behavior was based on the root growth of young sorghum plant grown in nutrient solutions with varied Al (0.0, 2.25 and 4.5 mg of Al/l for grain sorghum and 0.0, 2.5 and 5.0 mg of Al/l for sweet sorghum). For comparison purposes, the relative seminal root length (SRRL = SRL+Al/SRL-Al, where SRL = Seminal Root Rength and SRRL = Seminal Root Relative Length) was estimated. Based upon the percentual frequency distribution of SRRL values obtained for the different genotypes tested and based upon the SRRL values of SC 208 (Al susceptible) and SC 283 (Al-tolerant) three classes of differential responses to Al were identified: Susceptible (SRRL 0.70). Among the materials tested, the following were classified as being tolerant to Al: IS 3625,IS 7173 C (SC 283) IS 12666, 5DX61/6/2, 3DX57/1/1/91O, 156-P-5-Serere-1, 9DX9/11, Brandes, MN 4004 and MN 1204. The technique proved to be effective to screen large number of line for Al tolerance and should be used as a tool in a breeding program

The effect of the AltSB gene on root growth in nutrient solution of isogenic sorghum hybrids

AlTSB, a major gene of the Multidrug and Toxic Compound Extrusion (Mate) family confers tolerance to aluminum toxicity in sorghum. This gene is a transporter gene that is responsible for the exudation of citric acid in the presence of toxic level of aluminum in the soil. The citrate complexes with the toxic aluminum forming a nontoxic compound. During the past several years, isogenic sorghum breeding lines, both cytoplasmic male-sterile lines (A and B-lines) and fertility restoring pollinator lines (R-lines) for this AlTSB gene have been developed at Embrapa Maize and Sorghum. These isogenic lines for AlTSB were used to develop sixteen isogenic sorghum hybrids with zero, one and two alleles for tolerance to aluminum toxicity. These sixteen hybrids are essentially genetically equal but with variation in the dose of the AlTSB allele. Seedlings of these isogenic hybrids were evaluated for root growth in nutrient solution with 0, 11, 20, 27 and 39μM aluminum for seven days at four intervals (0, 3, 5, and 7days). One dose of the gene had a very significant effect on maintaining root growth up to a concentration of 27 μM aluminum. A second dose of the gene continued to have a positive effect for some of the isogenic hybrids confirming the effect of partial dominance for this gene. The presence of the AlTSB gene in sorghum cultivars used in regions with acid soils or subsoils will contribute to the development of a better and deeper root system and promote greater and more sustainable productivity

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

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

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