The improved auxin signalling via entire mutation enhances aluminium tolerance in tomato.

Aluminum-Dependent Root-Growth Inhibition in Arabidopsis Results from AtATR-Regulated Cell-Cycle Arrest

Aluminum (Al) toxicity is a major factor limiting crop yields on acid soils. There is considerable genotypic variation for Al tolerance in most common plant species. In maize (Zea mays), Al tolerance is a complex phenomenon involving multiple genes and physiological mechanisms yet uncharacterized. To begin elucidating the molecular basis of maize Al toxicity and tolerance, a detailed temporal analysis of root gene expression under Al stress was performed using microarrays with Al-tolerant and Al-sensitive genotypes. Al altered the expression of significantly more genes in the Al-sensitive genotype, presumably as a result of more severe Al toxicity. Nevertheless, several Al-regulated genes exhibited higher expression in the Al-tolerant genotype. Cell wall-related genes, as well as low phosphate-responsive genes, were found to be regulated by Al. In addition, the expression patterns of genes related to Al-activated citrate release indicated that in maize this mechanism is probably regulated by the expression level and/or function of the citrate transporter. This study is the first comprehensive survey of global transcriptional regulation under Al stress. The results described here will help to further our understanding of how mechanisms of Al toxicity and tolerance in maize are regulated at the transcriptional level.

BackgroundAluminum (Al) toxicity is one of the most important yield-limiting factors of many crops worldwide. The primary symptom of Al toxicity syndrome is the inhibition of root growth leading to poor water and nutrient absorption. Al tolerance has been extensively studied using hydroponic experiments. However, unlike soil conditions, this method does not address all of the components that are necessary for proper root growth and development. In the present study, we grew two maize genotypes with contrasting tolerance to Al in soil containing toxic levels of Al and then compared their transcriptomic responses.ResultsWhen grown in acid soil containing toxic levels of Al, the Al-sensitive genotype (S1587-17) showed greater root growth inhibition, more Al accumulation and more callose deposition in root tips than did the tolerant genotype (Cat100-6). Transcriptome profiling showed a higher number of genes differentially expressed in S1587-17 grown in acid soil, probably due to secondary effects of Al toxicity. Genes involved in the biosynthesis of organic acids, which are frequently associated with an Al tolerance response, were not differentially regulated in both genotypes after acid soil exposure. However, genes related to the biosynthesis of auxin, ethylene and lignin were up-regulated in the Al-sensitive genotype, indicating that these pathways might be associated with root growth inhibition. By comparing the two maize lines, we were able to discover genes up-regulated only in the Al-tolerant line that also presented higher absolute levels than those observed in the Al-sensitive line. These genes encoded a lipase hydrolase, a retinol dehydrogenase, a glycine-rich protein, a member of the WRKY transcriptional family and two unknown proteins.ConclusionsThis work provides the first characterization of the physiological and transcriptional responses of maize roots when grown in acid soil containing toxic levels of Al. The transcriptome profiles highlighted several pathways that are related to Al toxicity and tolerance during growth in acid soil. We found several genes that were not found in previous studies using hydroponic experiments, increasing our understanding of plant responses to acid soil. The use of two germplasms with markedly different Al tolerances allowed the identification of genes that are a valuable tool for assessing the mechanisms of Al tolerance in maize in acid soil.

Achieving sustainable food production to feed the increasing population of the problematic lands of the world is an enormous challenge. Aluminum (Al) toxicity in the acid soil is a major worldwide problem. Liming and nutrient management technologies are worthless due to high lime requirement, and the effect of liming does not persist for long. Besides this, conventional breeding is useful to manage Al toxicity as some plants have evolved mechanisms to cope with Al toxicity in acid soil. Therefore, understanding of Al tolerance mechanisms is prime necessity for improving Al tolerance in crops. Al resistance mechanisms include mainly Al avoidance (Al exclusion) and/or Al tolerance (detoxification of Al inside the cell) mechanisms. In this chapter, we summarize Al behavior in plant root cell. We include recent findings of Al resistance mechanisms and Al-resistant genes which can be useful to produce cultivars adapted to acid soils.

Overexpression of OsGASR1 promotes Al tolerance in rice

Aluminum (Al) toxicity severely limits agricultural productivity in acidic soils worldwide. Although Al tolerance mechanisms have been extensively studied in crops, the molecular basis in forage crops remains poorly understood. Here, we investigated the physiological and transcriptomic responses of white clover (Trifolium repens L.) seedlings to Al toxicity. Al exposure triggered reactive oxygen species (ROS) accumulation and significantly inhibited plant growth and development. RNA-seq revealed a MADS-box transcription factor gene, TrAGL80, which exhibited strong induction under Al toxicity. Interference and silencing of TrAGL80 led to increased ROS levels and reduced malate secretion; conversely, heterologous expression of TrAGL80 in alfalfa (Medicago sativa) improved Al tolerance. We found that TrAGL80 interacts with TrGAPC2 in the nucleus and cytoplasm and that silencing TrGAPC2 reduces white clover Al tolerance. Additionally, we identified TrSCL6 as a negative regulator of TrAGL80 expression, and TrSCL6 negatively regulates Al tolerance by inhibiting malate secretion in white clover. Taken together, our findings unveil a TrSCL6-TrAGL80-TrGAPC2 regulatory module that plays a critical role in mediating Al tolerance in white clover, providing valuable genetic targets for breeding improved Al-resistant forage crops.

BackgroundAluminum (Al) toxicity is an important limitation to food security in tropical and subtropical regions. High Al saturation on acid soils limits root development, reducing water and nutrient uptake. In addition to naturally occurring acid soils, agricultural practices may decrease soil pH, leading to yield losses due to Al toxicity. Elucidating the genetic and molecular mechanisms underlying maize Al tolerance is expected to accelerate the development of Al-tolerant cultivars.ResultsFive genomic regions were significantly associated with Al tolerance, using 54,455 SNP markers in a recombinant inbred line population derived from Cateto Al237. Candidate genes co-localized with Al tolerance QTLs were further investigated. Near-isogenic lines (NILs) developed for ZmMATE2 were as Al-sensitive as the recurrent line, indicating that this candidate gene was not responsible for the Al tolerance QTL on chromosome 5, qALT5. However, ZmNrat1, a maize homolog to OsNrat1, which encodes an Al3+ specific transporter previously implicated in rice Al tolerance, was mapped at ~40 Mbp from qALT5. We demonstrate for the first time that ZmNrat1 is preferentially expressed in maize root tips and is up-regulated by Al, similarly to OsNrat1 in rice, suggesting a role of this gene in maize Al tolerance. The strongest-effect QTL was mapped on chromosome 6 (qALT6), within a 0.5 Mbp region where three copies of the Al tolerance gene, ZmMATE1, were found in tandem configuration. qALT6 was shown to increase Al tolerance in maize; the qALT6-NILs carrying three copies of ZmMATE1 exhibited a two-fold increase in Al tolerance, and higher expression of ZmMATE1 compared to the Al sensitive recurrent parent. Interestingly, a new source of Al tolerance via ZmMATE1 was identified in a Brazilian elite line that showed high expression of ZmMATE1 but carries a single copy of ZmMATE1.ConclusionsHigh ZmMATE1 expression, controlled either by three copies of the target gene or by an unknown molecular mechanism, is responsible for Al tolerance mediated by qALT6. As Al tolerant alleles at qALT6 are rare in maize, marker-assisted introgression of this QTL is an important strategy to improve maize adaptation to acid soils worldwide.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-153) contains supplementary material, which is available to authorized users.

Recent findings on the effect of aluminium (Al) on the functioning of legumes and their associated microsymbionts are reviewed here. Al represents 7% of solid matter in the Earth’s crust and is an important abiotic factor that alters microbial and plant functioning at very early stages. The trivalent Al (Al3+) dominates at pH < 5 in soils and becomes a constraint to legume productivity through its lethal effect on rhizobia, the host plant and their interaction. Al3+ has lethal effects on many aspects of the rhizobia/legume symbiosis, which include a decrease in root elongation and root hair formation, lowered soil rhizobial population, and suppression of nitrogen metabolism involving nitrate reduction, nitrite reduction, nitrogenase activity and the functioning of uptake of hydrogenases (Hup), ultimately impairing the N2 fixation process. At the molecular level, Al is known to suppress the expression of nodulation genes in symbiotic rhizobia, as well as the induction of genes for the formation of hexokinase, phosphodiesterase, phosphooxidase and acid/alkaline phosphatase. Al toxicity can also induce the accumulation of reactive oxygen species and callose, in addition to lipoperoxidation in the legume root elongation zone. Al tolerance in plants can be achieved through over-expression of citrate synthase gene in roots and/or the synthesis and release of organic acids that reverse Al-induced changes in proteins, as well as metabolic regulation by plant-secreted microRNAs. In contrast, Al tolerance in symbiotic rhizobia is attained via the production of exopolysaccharides, the synthesis of siderophores that reduce Al uptake, induction of efflux pumps resistant to heavy metals and the expression of metal-inducible (dmeRF) gene clusters in symbiotic Rhizobiaceae. In soils, Al toxicity is usually ameliorated through liming, organic matter supply and use of Al-tolerant species. Our current understanding of crop productivity in high Al soils suggests that a much greater future accumulation of Al is likely to occur in agricultural soils globally if crop irrigation is increased under a changing climate.

Among various abiotic stresses, heat stress is one of the most damaging, threatening plant productivity and survival all over the world. Warmer temperatures due to climatic anomalies above optimum growing temperatures have detrimental impacts on crop yield potential as well as plant distribution patterns. Heat stress affects overall plant metabolism in terms of physiology, biochemistry, and gene expression. Membrane damage, protein degradation, enzyme inactivation, and the accumulation of reactive oxygen species are some of the harmful effects of heat stress that cause injury to various cellular compartments. Although plants are equipped with various defense strategies to counteract these adversities, their defensive means are not sufficient to defend against the ever-rising temperatures. Hence, substantial yield losses have been observed in all crop species under heat stress. Here, we describe the involvement of various plant growth-regulators (PGRs) (hormones, polyamines, osmoprotectants, antioxidants, and other signaling molecules) in thermotolerance, through diverse cellular mechanisms that protect cells under heat stress. Several studies involving the exogenous application of PGRs to heat-stressed plants have demonstrated their role in imparting tolerance, suggesting the strong potential of these molecules in improving the performance of food crops grown under high temperature.

Differential aluminium toxicity in rice (Oryza sativa L.) landraces from Sikkim Himalaya: cellular Al-management determines tolerance.

Solanaceae including tomato, chilli, potato, eggplant, petunia, and tobacco are the most important vegetables, cash crops, and ornamental plants. Most of them are planted in 43% acid soil in the world. There are remarkable differences in the adaptability of different Solanaceae species to acidic soil. Aluminum (Al) is the major factor limiting crops productivity on acidic soil. Al can rapidly suppress cell division, destroy the cell structure, reduce nutrient and water uptake, and inhibit root elongation growth in Solanaceae plants. This review focuses on recent research advances and development trends in Al toxicity and tolerance in Solanaceae plants. Al avoidance, the alteration of nutrient element distribution, and increase of rhizosphere pH value contributes to Al tolerance in Solanaceae plants. Moreover, secretion of organic acids, enhancement of antioxidant capacity, and induction of Al-tolerant genes also play an important role in Al tolerance of Solanaceae plants. Manipulation of Al-tolerant genes helps to enhance crop production on acid soils. The completion of whole genome sequencing and genome editing technology will provide a platform for genetic improvement of Solanaceae plants.

Root damage caused by aluminum (Al) toxicity is a major cause of grain yield reduction on acid soils, which are prevalent in tropical and subtropical regions of the world where food security is most tenuous. In sorghum, Al tolerance is conferred by SbMATE, an Al-activated root citrate efflux transporter that underlies the major Al tolerance locus, AltSB, on sorghum chromosome 3. We used association mapping to gain insights into the origin and evolution of Al tolerance in sorghum and to detect functional variants amenable to allele mining applications. Linkage disequilibrium across the AltSB locus decreased much faster than in previous reports in sorghum, and reached basal levels at approximately 1000 bp. Accordingly, intra-locus recombination events were found to be extensive. SNPs and indels highly associated with Al tolerance showed a narrow frequency range, between 0.06 and 0.1, suggesting a rather recent origin of Al tolerance mutations within AltSB. A haplotype network analysis suggested a single geographic and racial origin of causative mutations in primordial guinea domesticates in West Africa. Al tolerance assessment in accessions harboring recombinant haplotypes suggests that causative polymorphisms are localized to a ∼6 kb region including intronic polymorphisms and a transposon (MITE) insertion, whose size variation has been shown to be positively correlated with Al tolerance. The SNP with the strongest association signal, located in the second SbMATE intron, recovers 9 of the 14 highly Al tolerant accessions and 80% of all the Al tolerant and intermediately tolerant accessions in the association panel. Our results also demonstrate the pivotal importance of knowledge on the origin and evolution of Al tolerance mutations in molecular breeding applications. Allele mining strategies based on associated loci are expected to lead to the efficient identification, in diverse sorghum germplasm, of Al tolerant accessions able maintain grain yields under Al toxicity.

Breeding for aluminium (Al) tolerance is a vital approach for enhancing the productivity of field crops in acidic soil regions where Al toxicity seems to be the most restraining factor for crop performance. Sunflower is generally considered extremely sensitive to Al toxicity; although no comprehensive information on the evaluation of sunflower genotypes for Al tolerance is available. In this study, 50 sunflower genotypes (set-I and set-II) were evaluated for Al tolerance at the seedling stage under hydroponic conditions. Substantial genetic variability in Al tolerance was observed among the studied genotypes. High estimates of heritability were obtained for both the total root length (TRL) and root regrowth (RRG), together with high estimates of genetic advance. A cluster analysis separated the genotypes into five different groups among the studied germplasm, the genotypes; NDLR-06 and EC-601861 were observed to be highly Al tolerant in terms of root regrowth under Al stress. In conclusion, the findings lreveal the complex mechanisms of Al tolerance in sunflower and may help to find new genetic resource for the improvement of Al tolerance in sunflower breeding.

The transcriptional regulation of aluminum (Al) tolerance in plants is largely unknown, although Al toxicity restricts agricultural yields in acidic soils. Here, we identified a NAM, ATAF1/2, and cup-shaped cotyledon 2 (NAC) transcription factor that participates in Al tolerance in Arabidopsis (Arabidopsis thaliana). Al substantially induced the transcript and protein levels of ANAC070, and loss-of-function mutants showed remarkably increased Al sensitivity, implying a beneficial role of ANAC070 in plant tolerance to Al toxicity. Further investigation revealed that more Al accumulated in the roots of anac070 mutants, especially in root cell walls, accompanied by a higher hemicellulose and xyloglucan level, implying a possible interaction between ANAC070 and genes that encode proteins responsible for the modification of xyloglucan, including xyloglucan endo-transglycosylase/hydrolase (XTH) or ANAC017. Yeast 1-hybrid analysis revealed a potential interaction between ANAC070 and ANAC017, but not for other XTHs. Furthermore, dual-luciferase reporter assay, RT-qPCR, and GUS analysis revealed that ANAC070 could directly repress the transcript levels of ANAC017, and knockout of ANAC017 in the anac070 mutant partially restored its Al sensitivity phenotype, indicating that ANAC070 contributes to Al tolerance mechanisms other than suppression of ANAC017 expression. Further analysis revealed that the core transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) and its target genes, which control Al tolerance in Arabidopsis, may also be involved in ANAC070-regulated Al tolerance. In summary, we identified a transcription factor, ANAC070, that represses the ANAC017-XTH31 module to regulate Al tolerance in Arabidopsis.

Aluminum (Al) toxicity and phosphorus (P) deficiency often coexist in acid soils that severely limit crop growth and production, including soybean (Glycine max). Understanding the physiological mechanisms relating to plant Al and P interactions should help facilitate the development of more Al-tolerant and/or P-efficient crops. In this study, both homogeneous and heterogeneous nutrient solution experiments were conducted to study the effects of Al and P interactions on soybean root growth and root organic acid exudation. In the homogenous solution experiments with a uniform Al and P distribution in the bulk solution, P addition significantly increased Al tolerance in four soybean genotypes differing in P efficiency. The two P-efficient genotypes appeared to be more Al tolerant than the two P-inefficient genotypes under these high-P conditions. Analysis of root exudates indicated Al toxicity induced citrate exudation, P deficiency triggered oxalate exudation, and malate release was induced by both treatments. To more closely mimic low-P acid soils where P deficiency and Al toxicity are often much greater in the lower soil horizons, a divided root chamber/nutrient solution approach was employed to impose elevated P conditions in the simulated upper soil horizon, and Al toxicity/P deficiency in the lower horizon. Under these conditions, we found that the two P-efficient genotypes were more Al tolerant during the early stages of the experiment than the P-inefficient lines. Although the same three organic acids were exuded by roots in the divided chamber experiments, their exudation patterns were different from those in the homogeneous solution system. The two P-efficient genotypes secreted more malate from the taproot tip, suggesting that improved P nutrition may enhance exudation of organic acids in the root regions dealing with the greatest Al toxicity, thus enhancing Al tolerance. These findings demonstrate that P efficiency may play a role in Al tolerance in soybean. Phosphorus-efficient genotypes may be able to enhance Al tolerance not only through direct Al-P interactions but also through indirect interactions associated with stimulated exudation of different Al-chelating organic acids in specific roots and root regions.