Repeat variants for the SbMATE transporter protect sorghum roots from aluminum toxicity by transcriptional interplay in<i>cis</i>and<i>trans</i>

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 Al³⁺, but can exhibit reduced expression when introgressed into different lines. We show that allele-specific <i>SbMATE</i> transactivation occurs and is caused by factors located away from <i>SbMATE</i> Using expression-QTL mapping and expression genome-wide association mapping, we establish that <i>SbMATE</i> transcription is controlled in a bipartite fashion, primarily in <i>cis</i> but also in <i>trans</i> Multiallelic promoter transactivation and ChIP analyses demonstrated that intermolecular effects on <i>SbMATE</i> expression arise from a WRKY and a zinc finger-DHHC transcription factor (TF) that bind to and <i>trans</i>-activate the <i>SbMATE</i> promoter. A haplotype analysis in sorghum RILs indicates that the TFs influence <i>SbMATE</i> expression and Al tolerance. Variation in <i>SbMATE</i> expression likely results from changes in tandemly repeated <i>cis</i> sequences flanking a transposable element (a miniature inverted repeat transposable element) insertion in the <i>SbMATE</i> promoter, which are recognized by the Al³⁺-responsive TFs. According to our model, repeat expansion in Al-tolerant genotypes increases TF recruitment and, hence, <i>SbMATE</i> 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 <i>cis</i> regulation of an agronomically important gene can be subjected to precise intermolecular fine-tuning. These concerted c<i>is</i>/<i>trans</i> 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.