Abstract
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.
Highlights
Among the various abiotic stresses that limit sorghum production, aluminum (Al) toxicity has been identified as one of the main breeding targets on acid soils [1], which are commonly found in tropical and subtropical regions where sorghum is intensively cultivated
Because acid soils are widespread in the world [3], Al toxicity represents a major constraint for crop production worldwide, in areas where food security still poses a significant challenge to human populations
A varying reduction in both Al tolerance and SbMATE expression from parents to the derived near-isogenic line (NIL) was observed and the NILs differed for SbMATE expression, suggesting that SbMATE expression is regulated at multiple levels. These findings suggest that cis effects are dominant in controlling SbMATE expression, the loss of functional trans-acting factors may lead to potentially strong genetic background effects depending on the donor allele, reducing both SbMATE expression and Al tolerance
Summary
Among the various abiotic stresses that limit sorghum production, aluminum (Al) toxicity has been identified as one of the main breeding targets on acid soils [1], which are commonly found in tropical and subtropical regions where sorghum is intensively cultivated. Because acid soils are widespread in the world [3], Al toxicity represents a major constraint for crop production worldwide, in areas where food security still poses a significant challenge to human populations. Al toxicity and phosphorus deficiency are major constraints for sorghum production in West Africa [4,5]. Yield reduction caused by drought stress, which is common in the region, worsens as roots intoxicated by Al are incapable of penetrating the deep, highly acidic soil layers to acquire water [6]. In view of today’s challenge of feeding nine billion people in the near future, including the most economically disadvantaged [8], modern molecular strategies are needed [9]
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