SUMMARYImpaired root development caused by aluminum (Al) toxicity is a major cause of grain yield reduction in crops cultivated on acid soils, which are widespread worldwide. In sorghum, the major Al-tolerance locus, Alt SB , is due to the function of SbMATE, which is an Al-activated root citrate transporter. Here we performed a molecular and physiological characterization of various Alt SB donors and near-isogenic lines harboring various Alt SB alleles. We observed a partial transfer of Al tolerance from the parents to the nearisogenic lines that was consistent across donor alleles, emphasizing the occurrence of strong genetic background effects related to Alt SB . This reduction in tolerance was variable, with a 20% reduction being observed when highly Al-tolerant lines were the Alt SB donors, and a reduction as great as 70% when other Alt SB alleles were introgressed. This reduction in Al tolerance was closely correlated with a reduction in SbMATE expression in near-isogenic lines, suggesting incomplete transfer of loci acting in trans on SbMATE. Nevertheless, Alt SB alleles from the highly Al-tolerant sources SC283 and SC566 were found to retain high SbMATE expression, presumably via elements present within or near the Alt SB locus, resulting in significant transfer of the Al-tolerance phenotype to the derived near-isogenic lines. Allelic effects could not be explained by coding region polymorphisms, although occasional mutations may affect Al tolerance. Finally, we report on the extensive occurrence of alternative splicing for SbMATE, which may be an important component regulating SbMATE expression in sorghum by means of the nonsense-mediated RNA decay pathway.

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 SbMATE promoter. A haplotype analysis in sorghum RILs indicates that the TFs influence SbMATE expression 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.

ABSTRACT. Aluminum (Al) toxicity restricts root growth and agricultural yield in acid soils, which constitute approximately 40% of the potentially arable lands worldwide. The two main mechanisms of Al tolerance in plants are internal detoxification of Al and its exclusion from root cells. Genes encoding membrane transporters and accessory transcription factors, as well as cis-elements that enhance gene expression, are involved in Al tolerance in plants; thus studies of these genes and accessory factors should be the focus of molecular breeding efforts aimed at improving Al tolerance in crops. In this review, we describe the main genetic and molecular studies that led to the identification and cloning of genes associated with Al tolerance in plants. We include recent findings on the regulation of genes associated with Al tolerance. Understanding the genetic, molecular, and physiological aspects of Al tolerance in plants is important for generating cultivars adapted to acid soils, thereby contributing to food security worldwide.