Low soil phosphorus (P) availability is a major constraint for crop production in tropical regions. The rice (Oryza sativa) protein kinase, PHOSPHORUS-STARVATION TOLERANCE1 (OsPSTOL1), was previously shown to enhance P acquisition and grain yield in rice under P deficiency. We investigated the role of homologs of OsPSTOL1 in sorghum (Sorghum bicolor) performance under low P. Association mapping was undertaken in two sorghum association panels phenotyped for P uptake, root system morphology and architecture in hydroponics and grain yield and biomass accumulation under low-P conditions, in Brazil and/or in Mali. Root length and root surface area were positively correlated with grain yield under low P in the soil, emphasizing the importance of P acquisition efficiency in sorghum adaptation to low-P availability. SbPSTOL1 alleles reducing root diameter were associated with enhanced P uptake under low P in hydroponics, whereas Sb03g006765 and Sb03g0031680 alleles increasing root surface area also increased grain yield in a low-P soil. SbPSTOL1 genes colocalized with quantitative trait loci for traits underlying root morphology and dry weight accumulation under low P via linkage mapping. Consistent allelic effects for enhanced sorghum performance under low P between association panels, including enhanced grain yield under low P in the soil in Brazil, point toward a relatively stable role for Sb03g006765 across genetic backgrounds and environmental conditions. This study indicates that multiple SbPSTOL1 genes have a more general role in the root system, not only enhancing root morphology traits but also changing root system architecture, which leads to grain yield gain under low-P availability in the soil.

Phosphorus (P) fixation on aluminum (Al) and iron (Fe) oxides in soil clays restricts P availability for crops cultivated on highly weathered tropical soils, which are common in developing countries. Hence, P deficiency becomes a major obstacle for global food security. We used multi-trait quantitative trait loci (QTL) mapping to study the genetic architecture of P efficiency and to explore the importance of root traits on sorghum grain yield on a tropical low-P soil. P acquisition efficiency was the most important component of P efficiency, and both traits were highly correlated with grain yield under low P availability. Root surface area was positively associated with grain yield. The guinea parent, SC283, contributed 58% of all favorable alleles detected by single-trait mapping. Multi-trait mapping detected 14 grain yield and/or root morphology QTLs. Tightly linked or pleiotropic QTL underlying the surface area of fine roots (1–2 mm in diameter) and grain yield were detected at positions 1–7 megabase pairs (Mb) and 71 Mb on chromosome 3, respectively, and a root diameter/grain yield QTL was detected at 7 Mb on chromosome 7. All these QTLs were near sorghum homologs of the rice serine/threonine kinase, OsPSTOL1. The SbPSTOL1 genes on chromosome 3, Sb03g006765 at 7 Mb and Sb03g031690 at 60 Mb were more highly expressed in SC283, which donated the favorable alleles at all QTLs found nearby SbPSTOL1 genes. The Al tolerance gene, SbMATE, may also influence a grain yield QTL on chromosome 3. Another PSTOL1-like gene, Sb07g02840, appears to enhance grain yield via small increases in root diameter. Co-localization analyses suggested a role for other genes, such as a sorghum homolog of the Arabidopsis ubiquitin-conjugating E2 enzyme, phosphate 2 (PHO2), on grain yield advantage conferred by the elite parent, BR007 allele. Genetic determinants conferring higher root surface area and slight increases in fine root diameter may favor P uptake, thereby enhancing grain yield under low-P availability in the soil. Molecular markers for SbPSTOL1 genes and for QTL increasing grain yield by non-root morphology-based mechanisms hold promise in breeding strategies aimed at developing sorghum cultivars adapted to low-P soils.

Modifications in root morphology are important strategies to maximize soil exploitation under phosphorus starvation in plants. Here, we used two multiple interval models to map QTLs related to root traits, biomass accumulation and P content in a maize RIL population cultivated in nutrient solution. In addition, we searched for putative maize homologs to PSTOL1, a gene responsible to enhance early root growth, P uptake and grain yield in rice and sorghum. Based on path analysis, root surface area was the root morphology component that most strongly contributed to total dry weight and to P content in maize seedling under low-P availability. Multiple interval mapping models for single (MIM) and multiple traits (MT-MIM) were combined and revealed 13 genomic regions significantly associated with the target traits in a complementary way. The phenotypic variances explained by all QTLs and their epistatic interactions using MT-MIM (23.4 to 35.5 %) were higher than in previous studies, and presented superior statistical power. Some of these QTLs were coincident with QTLs for root morphology traits and grain yield previously mapped, whereas others harbored ZmPSTOL candidate genes, which shared more than 55 % of amino acid sequence identity and a conserved serine/threonine kinase domain with OsPSTOL1. Additionally, four ZmPSTOL candidate genes co-localized with QTLs for root morphology, biomass accumulation and/or P content were preferentially expressed in roots of the parental lines that contributed the alleles enhancing the respective phenotypes. QTL mapping strategies adopted in this study revealed complementary results for single and multiple traits with high accuracy. Some QTLs, mainly the ones that were also associated with yield performance in other studies, can be good targets for marker-assisted selection to improve P-use efficiency in maize. Based on the co-localization with QTLs, the protein domain conservation and the coincidence of gene expression, we selected novel maize genes as putative homologs to PSTOL1 that will require further validation studies.

Sorghum (Sorghum bicolor L. Moench) productivity is severely impeded by low phosphorus (P) and aluminum (Al) toxic soils in sub-Saharan Africa and especially West Africa (WA). Improving productivity of this staple crop under these harsh conditions is crucial to improve food security and farmer’s incomes in WA. This is the first study to examine the genetics underlying sorghum adaptation to phosphorus limitation in a wide range of WA growing conditions. A set of 187 diverse sorghum genotypes were grown in 29 –P and + P field experiments from 2006-2012 in three WA countries. Sorghum grain yield performance under –P and + P conditions was highly correlated (r = 0.85***). Significant genotype-by-phosphorus interaction was detected but with small magnitude compared to the genotype variance component. We observed high genetic diversity within our panel, with rapid linkage disequilibrium decay, confirming recent sequence based studies in sorghum. Using genome wide association mapping based on 220 934 SNPs we identified one genomic region on chromosome 3 that was highly associated to grain yield production. A major Al-tolerance gene in sorghum, SbMATE, was collocated in this region and SbMATE specific SNPs showed very high associations to grain yield production, especially under –P conditions, explaining up to 16% of the genotypic variance. The results suggest that SbMATE has a possible pleiotropic role in providing tolerance to two of the most serious abiotic stresses for sorghum in WA, Al toxicity and P deficiency. The identified SNPs can help accelerate breeding for increased sorghum productivity under unfavorable soil conditions and contribute to assuring food security in WA.

Aluminum (Al) toxicity on acidic soils significantly damages plant roots and inhibits root growth. Hence, crops intoxicated by Al become more sensitive to drought stress and mineral nutrient deficiencies, particularly phosphorus (P) deficiency, which is highly unavailable on tropical soils. Advances in our understanding of the physiological and genetic mechanisms that govern plant Al resistance have led to the identification of Al resistance genes, both in model systems and in crop species. It has long been known that Al resistance has a beneficial effect on crop adaptation to acidic soils. This positive effect happens because the root systems of Al tolerant plants show better development in the presence of soil ionic Al3+ and are, consequently, more efficient in absorbing sub-soil water and mineral nutrients. This effect of Al resistance on crop production, by itself, warrants intensified efforts to develop and implement, on a breeding scale, modern selection strategies to profit from the knowledge of the molecular determinants of plant Al resistance. Recent studies now suggest that Al resistance can exert pleiotropic effects on P acquisition, potentially expanding the role of Al resistance on crop adaptation to acidic soils. This appears to occur via both organic acid- and non-organic acid transporters governing a joint, iron-dependent interplay between Al resistance and enhanced P uptake, via changes in root system architecture. Current research suggests this interplay to be part of a P stress response, suggesting that this mechanism could have evolved in crop species to improve adaptation to acidic soils. Should this pleiotropism prove functional in crop species grown on acidic soils, molecular breeding based on Al resistance genes may have a much broader impact on crop performance than previously anticipated. To explore this possibility, here we review the components of this putative effect of Al resistance genes on P stress responses and P nutrition to provide the foundation necessary to discuss the recent evidence suggesting pleiotropy as a genetic linkage between Al resistance and P efficiency. We conclude by exploring what may be needed to enhance the utilization of Al resistance genes to improve crop production on acidic soils.

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.