Acid soils restrict plant production around the world. One of the major limitations to plant growth on acid soils is the prevalence of soluble aluminium (Al³⁺) ions which can inhibit root growth at micromolar concentrations. Species that show a natural resistance to Al³⁺ toxicity perform better on acid soils. Our understanding of the physiology of Al³⁺ resistance in important crop plants has increased greatly over the past 20 years, largely due to the application of genetics and molecular biology. Fourteen genes from seven different species are known to contribute to Al³⁺ tolerance and resistance and several additional candidates have been identified. Some of these genes account for genotypic variation within species and others do not. One mechanism of resistance which has now been identified in a range of species relies on the efflux of organic anions such as malate and citrate from roots. The genes controlling this trait are members of the ALMT and MATE families which encode membrane proteins that facilitate organic anion efflux across the plasma membrane. Identification of these and other resistance genes provides opportunities for enhancing the Al³⁺ resistance of plants by marker-assisted breeding and through biotechnology. Most attempts to enhance Al³⁺ resistance in plants with genetic engineering have targeted genes that are induced by Al³⁺ stress or that are likely to increase organic anion efflux. In the latter case, studies have either enhanced organic anion synthesis or increased organic anion transport across the plasma membrane. Recent developments in this area are summarized and the structure–function of the TaALMT1 protein from wheat is discussed.

The first confirmed mechanism for aluminum (Al) resistance in plants is encoded by the wheat (Triticum aestivum) gene, TaALMT1, on chromosome 4DL. TaALMT1 controls the Al-activated efflux of malate from roots, and this mechanism is widespread among Al-resistant genotypes of diverse genetic origins. This study describes a second mechanism for Al resistance in wheat that relies on citrate efflux. Citrate efflux occurred constitutively from the roots of Brazilian cultivars Carazinho, Maringa, Toropi, and Trintecinco. Examination of two populations segregating for this trait showed that citrate efflux was controlled by a single locus. Whole-genome linkage mapping using an F2 population derived from a cross between Carazinho (citrate efflux) and the cultivar EGA-Burke (no citrate efflux) identified a major locus on chromosome 4BL, Xcec, which accounts for more than 50% of the phenotypic variation in citrate efflux. Mendelizing the quantitative variation in citrate efflux into qualitative data, the Xcec locus was mapped within 6.3 cM of the microsatellite marker Xgwm495 locus. This linkage was validated in a second population of F2:3 families derived from a cross between Carazinho and the cultivar Egret (no citrate efflux). We show that expression of an expressed sequence tag, belonging to the multidrug and toxin efflux (MATE) gene family, correlates with the citrate efflux phenotype. This study provides genetic and physiological evidence that citrate efflux is a second mechanism for Al resistance in wheat.

Certain soil microorganisms can improve plant growth, and practices that encourage their proliferation around the roots can boost production and reduce reliance on agrochemicals. The beneficial effects of the microbial inoculants currently used in agriculture are inconsistent or short-lived because their persistence in soil and on roots is often poor. A complementary approach could use root exudates to recruit beneficial microbes directly from the soil and encourage inoculant proliferation. However, it is unclear whether the release of common organic metabolites can alter the root microbiome in a consistent manner and if so, how those changes vary throughout the whole root system. In this study, we altered the expression of transporters from the ALUMINUM-ACTIVATED MALATE TRANSPORTER and the MULTIDRUG AND TOXIC COMPOUND EXTRUSION families in rice (Oryza sativa L.) and wheat (Triticum aestivum L.) and tested how the subsequent release of their substrates (simple organic anions, including malate, citrate, and γ-amino butyric acid) from root apices affected the root microbiomes. We demonstrate that these exudate compounds, separately and in combination, significantly altered microbiome composition throughout the root system. However, the root type (seminal or nodal), position along the roots (apex or base), and soil type had a greater influence on microbiome structure than the exudates. These results reveal that the root microbiomes of important cereal species can be manipulated by altering the composition of root exudates, and support ongoing attempts to improve plant production by manipulating the root microbiome.

Suspicions that soluble aluminium (Al) is detrimental to plant growth were reported more than 100 years ago. The rhizotoxicity of Al3+ is now accepted as the major limitation to plant production on acidic soils. Plants differ in their susceptibility to Al3+ toxicity and significant variation can occur within species, even in some major crops. The physiology of Al3+ resistance in some species has been understood for 15 years but the molecular biology has been elucidated only recently. The first gene controlling Al3+ resistance was cloned from wheat (Triticum aestivum L.) in 2004 but others have now been identified in Arabidopsis, barley (Hordeum vulgare L.), rye (Secale cereale L.), sorghum (Sorghum bicolour (L.) Moench) and rice (Oryza sativa L.) with strong additional candidates in wheat and oilseed rape (Brassica napus L.). These genes confer resistance in different ways, but one mechanism occurs in nearly all species examined so far. This mechanism relies on the release of organic anions from roots which bind with the harmful Al3+ cations in the apoplast and detoxify them. The genes controlling this response come from at least two distinct families, suggesting that convergent evolution has occurred. We discuss the processes driving this convergence of protein function and offer opinions for why organic anions are central to the mechanisms of resistance in disparate species. We propose that mutations which modify protein expression or their activation by Al3+ have played important roles in co-opting different transport proteins from other functions.

Background The structure and function of plant roots and their interactions with soil are exciting scientific frontiers that will ultimately reveal much about our natural systems, global water and mineral and carbon cycles, and help secure food supplies into the future. This Special Issue presents a collection of papers that address topics at the forefront of our understanding of root biology.

Fungal pathogens are a major constraint to global crop production; hence, plant genes encoding pathogen resistance are important tools for combating disease. A few resistance genes identified to date provide partial, durable resistance to multiple pathogens and the wheat (Triticum aestivum) Lr67 hexose transporter variant (Lr67res) fits into this category. Two amino acids differ between the wild-type and resistant alleles – G144R and V387L. Exome sequence data from 267 barley (Hordeum vulgare) landraces and wild accessions was screened and neither of the Lr67res mutations was detected. The barley ortholog of Lr67, HvSTP13, was functionally characterized in yeast as a high affinity hexose transporter. The G144R mutation was introduced into HvSTP13 and abolished Glc uptake, whereas the V387L mutation reduced Glc uptake by ∼ 50%. Glc transport by HvSTP13 heterologously expressed in yeast was reduced when coexpressed with Lr67res. Stable transgenic Lr67res barley lines exhibited seedling resistance to the barley-specific pathogens Puccinia hordei and Blumeria graminis f. sp. hordei, which cause leaf rust and powdery mildew, respectively. Barley plants expressing Lr67res exhibited early senescence and higher pathogenesis-related (PR) gene expression. Unlike previous observations implicating flavonoids in the resistance of transgenic sorghum (Sorghum bicolor) expressing Lr34res, another wheat multipathogen resistance gene, barley flavonoids are unlikely to have a role in Lr67res-mediated resistance. Similar to observations made in yeast, Lr67res reduced Glc uptake in planta. These results confirm that the pathway by which Lr67res confers resistance to fungal pathogens is conserved between wheat and barley.