Abstract
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 Al
, but can exhibit reduced expression when introgressed into different lines. We show that allele-specific
transactivation occurs and is caused by factors located away from
Using expression-QTL mapping and expression genome-wide association mapping, we establish that
transcription is controlled in a bipartite fashion, primarily in
but also in
Multiallelic promoter transactivation and ChIP analyses demonstrated that intermolecular effects on
expression arise from a WRKY and a zinc finger-DHHC transcription factor (TF) that bind to and
-activate the
promoter. A haplotype analysis in sorghum RILs indicates that the TFs influence
expression and Al tolerance. Variation in
expression likely results from changes in tandemly repeated
sequences flanking a transposable element (a miniature inverted repeat transposable element) insertion in the
promoter, which are recognized by the Al
-responsive TFs. According to our model, repeat expansion in Al-tolerant genotypes increases TF recruitment and, hence,
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
regulation of an agronomically important gene can be subjected to precise intermolecular fine-tuning. These concerted c
/
interactions, which allow the plant to sense and respond to environmental cues, such as Al
toxicity, can now be used to increase yields and food security on acidic soils.