Repeat variants for the SbMATE transporter protect sorghum roots from aluminum toxicity by transcriptional interplay incisandtrans

• DOI: 10.1073/pnas.1808400115
• Publication Date: 2018-12-14T02:14:30Z
• Authors: Janaina O. Melo; Laura G. C. Martins; Beatriz A. Barros; Maiana R. Pimenta; Ubiraci G. P. Lana; Christiane E. M. ...; Maria M. Pastina; Claudia T. Guimaraes; Robert E. Schaffert; Leon V. Kochian; Elizabeth P. B. F...; Jurandir V. Magal...
• Keywords: 2. Zero hunger; 0303 health sciences; Anion Transport Proteins; Quantitative Trait Loci; 15. Life on land; Plant Roots; Chromosomes, Plant; 03 medical and health sciences; Gene Expression Regulation, Plant; Tandem Repeat Sequences; Promoter Regions, Genetic; Sorghum; Aluminum; Plant Proteins; Transcription Factors

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-specificSbMATEtransactivation occurs and is caused by factors located away fromSbMATE. Using expression-QTL mapping and expression genome-wide association mapping, we establish thatSbMATEtranscription is controlled in a bipartite fashion, primarily incisbut also intrans. Multiallelic promoter transactivation and ChIP analyses demonstrated that intermolecular effects onSbMATEexpression arise from a WRKY and a zinc finger-DHHC transcription factor (TF) that bind to andtrans-activate theSbMATEpromoter. A haplotype analysis in sorghum RILs indicates that the TFs influenceSbMATEexpression and Al tolerance. Variation inSbMATEexpression likely results from changes in tandemly repeatedcissequences flanking a transposable element (a miniature inverted repeat transposable element) insertion in theSbMATEpromoter, which are recognized by the Al3+-responsive TFs. According to our model, repeat expansion in Al-tolerant genotypes increases TF recruitment and, hence,SbMATEexpression, 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 dominantcisregulation of an agronomically important gene can be subjected to precise intermolecular fine-tuning. These concerted cis/transinteractions, 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.