Aluminum (Al3+) on acidic soils, which represent half of the world’s agricultural lands, damages plant roots. In Africa, where sorghum is a staple food, 20% of the agricultural soils are acidic, significantly reducing yields.

SbMATE confers sorghum Al tolerance via root citrate exudation into the soil, where citrate binds and detoxifies Al3+, but shows reduced expression in some genetic backgrounds. This phenomenon results from the action of a variable tandem repeat flanking a transposon in the SbMATE promoter working in concert with WRKY and zinc finger-DHHC proteins, which bind to the SbMATE promoter and regulate expression in response to Al3+. We can now select for superior alleles of these transcription factors to maximize SbMATE expression, thereby contributing to global food security.




Acidic soils, where aluminum (Al) toxicity is a major agricultural constraint, are globally widespread and are prevalent in developing countries. In sorghum, the root citrate transporter SbMATE confers Al tolerance by protecting root apices from toxic Al3+, but can exhibit reduced expression when introgressed into different lines. We show that allele-specific SbMATE transactivation occurs and is caused by factors located away from SbMATE. Using expression-QTL mapping and expression genome-wide association mapping, we establish that SbMATE transcription is controlled in a bipartite fashion, primarily in cis but also in trans. Multiallelic promoter transactivation and ChIP analyses demonstrated that intermolecular effects on SbMATE expression arise from a WRKY and a zinc finger-DHHC transcription factor (TF) that bind to and trans-activate the SbMATEpromoter. A haplotype analysis in sorghum RILs indicates that the TFs influence SbMATEexpression and Al tolerance. Variation in SbMATE expression likely results from changes in tandemly repeated cis sequences flanking a transposable element (a miniature inverted repeat transposable element) insertion in the SbMATE promoter, which are recognized by the Al3+-responsive TFs. According to our model, repeat expansion in Al-tolerant genotypes increases TF recruitment and, hence, SbMATE expression, which is, in turn, lower in Al-sensitive genetic backgrounds as a result of lower TF expression and fewer binding sites. We thus show that even dominant cis regulation of an agronomically important gene can be subjected to precise intermolecular fine-tuning. These concerted cis/trans interactions, which allow the plant to sense and respond to environmental cues, such as Al3+ toxicity, can now be used to increase yields and food security on acidic soils.





Figure 2: Trans-factor positional cloning based on expression GWAS. (A) Contrasting phenotypes in BR007 (Al-sensitive) and SC283 (Al-tolerant) based on root damage and relative net root growth (%RNRG) assessed in nutrient solution with {27} µM Al3+, in the context of the BR007 × SC283 RILs. QTL mapping was carried out for (B) Al-tolerance and (CSbMATE expression (eQTL) in the BR007 × SC283 RILs. The chromosome 9 region, where a colocated Al-tolerance/eQTL was detected, is expanded. GWAS with (D) Al tolerance and (ESbMATEexpression. SNPs near or within SbMATE previously associated with Al tolerance (20) are depicted as black diamonds. Blue and black dashed lines indicate the SbMATE region (chr 3) and the region harboring significant SNPs on chromosome 9, respectively, which overlap in the RIL QTL map (B and C) and in the GWAS plots (D and E). (F) Details of the chromosome 9 region showing physical positions for SNPs with the strongest association signals with Al tolerance (black dots).