Adaptive Mechanisms Make Lupin a Choice Crop for Acidic Soils Affected by Aluminum Toxicity

Almost half of the world’s agricultural soils are acidic, and most of them present significant levels of aluminum (Al) contamination, with Al3+ as the prevailing phytotoxic species. Lupin is a protein crop that is considered as an optimal alternative to soybean cultivation in cold climates. Lupins establish symbiosis with certain soil bacteria, collectively known as rhizobia, which are capable of fixing atmospheric nitrogen. Moreover, some lupin species, especially white lupin, form cluster roots, bottlebrush-like structures specialized in the mobilization and uptake of nutrients in poor soils. Cluster roots are also induced by Al toxicity. They exude phenolic compounds and organic acids that chelate Al to form non-phytotoxic complexes in the rhizosphere and inside the root cells, where Al complexes are accumulated in the vacuole. Lupins flourish in highly acidic soils where most crops, including other legumes, are unable to grow. Some lupin response mechanisms to Al toxicity are common to other plants, but lupin presents specific tolerance mechanisms, partly as a result of the formation of cluster roots. Al-induced lupin organic acid secretion differs from P-induced secretion, and organic acid transporters functions differ from those in other legumes. Additionally, symbiotic rhizobia can contribute to Al detoxification. After revising the existing knowledge on lupin distinct Al tolerance mechanisms, we conclude that further research is required to elucidate the specific organic acid secretion and Al accumulation mechanisms in this unique legume, but definitely, white lupin arises as a choice crop for cultivation in Al-rich acidic soils in temperate climate regions.

Overexpression of the Aldehyde Dehydrogenase Gene ZmALDH Confers Aluminum Tolerance in Arabidopsis thaliana

Aluminum (Al) toxicity is the main factor limiting plant growth and the yield of cereal crops in acidic soils. Al-induced oxidative stress could lead to the excessive accumulation of reactive oxygen species (ROS) and aldehydes in plants. Aldehyde dehydrogenase (ALDH) genes, which play an important role in detoxification of aldehydes when exposed to abiotic stress, have been identified in most species. However, little is known about the function of this gene family in the response to Al stress. Here, we identified an ALDH gene in maize, ZmALDH, involved in protection against Al-induced oxidative stress. Al stress up-regulated ZmALDH expression in both the roots and leaves. The expression of ZmALDH only responded to Al toxicity but not to other stresses including low pH and other metals. The heterologous overexpression of ZmALDH in Arabidopsis increased Al tolerance by promoting the ascorbate-glutathione cycle, increasing the transcript levels of antioxidant enzyme genes as well as the activities of their products, reducing MDA, and increasing free proline synthesis. The overexpression of ZmALDH also reduced Al accumulation in roots. Taken together, these findings suggest that ZmALDH participates in Al-induced oxidative stress and Al accumulation in roots, conferring Al tolerance in transgenic Arabidopsis.

Functional Characterization of Aluminum (Al)-Responsive Membrane-Bound NAC Transcription Factors in Soybean Roots

The membrane-bound NAC transcription (NTL) factors have been demonstrated to participate in the regulation of plant development and the responses to multiple environmental stresses. This study is aimed to functionally characterize soybean NTL transcription factors in response to Al-toxicity, which is largely uncharacterized. The qRT-PCR assays in the present study found that thirteen out of fifteen GmNTL genes in the soybean genome were up-regulated by Al toxicity. However, among the Al-up-regulated GmNTLs selected from six duplicate gene pairs, only overexpressing GmNTL1, GmNTL4, and GmNTL10 could confer Arabidopsis Al resistance. Further comprehensive functional characterization of GmNTL4 showed that the expression of this gene in response to Al stress depended on root tissues, as well as the Al concentration and period of Al treatment. Overexpression of GmNTL4 conferred Al tolerance of transgenic Arabidopsis in long-term (48 and 72 h) Al treatments. Moreover, RNA-seq assay identified 517 DEGs regulated by GmNTL4 in Arabidopsis responsive to Al stress, which included MATEs, ALMTs, PMEs, and XTHs. These results suggest that the function of GmNTLs in Al responses is divergent, and GmNTL4 might confer Al resistance partially by regulating the expression of genes involved in organic acid efflux and cell wall modification.

Silicon Application Induced Alleviation of Aluminum Toxicity in Xaraés Palisadegrass

Aluminum (Al) toxicity is a major abiotic constraint for agricultural production in acidic soils that needs a sustainable solution to deal with plant tolerance. Silicon (Si) plays important roles in alleviating the harmful effects of Al in plants. The genus Urochloa includes most important grasses and hybrids, and it is currently used as pastures in the tropical regions. Xaraés palisadegrass (Urochloa brizantha cv. Xaraés) is a forage that is relatively tolerant to Al toxicity under field-grown conditions, which might be explained by the great uptake and accumulation of Si. However, studies are needed to access the benefits of Si application to alleviate Al toxicity on Xaraés palisadegrass nutritional status, production, and chemical–bromatological composition. The study was conducted under greenhouse conditions with the effect of five Si concentrations evaluated (0, 0.3, 0.6, 1.2, and 2.4 mM) as well as with nutrient solutions containing 1 mM Al in two sampling dates (two forage cuts). The following evaluations were performed: number of tillers and leaves, shoot biomass, N, P, K, Ca, Mg, S, B, Cu, Fe, Mn, Zn, Al, and Si concentration in leaf tissue, Al and Si concentration in root tissue, neutral detergent fiber (NDF), and acid detergent fiber (ADF) content in Xaraés palisadegrass shoot. Silicon supply affected the relation between Si and Al uptake by increasing root Al concentration in detriment to Al transport to the leaves, thereby alleviating Al toxicity in Xaraés palisadegrass. The concentrations between 1.4 and 1.6 mM Si in solution decreased roots to shoots Al translocation by 259% (from 3.26 to 1.26%), which contributed to a higher number of leaves per plot and led to a greater shoot dry mass without affecting tillering. Xaraés palisadegrass could be considered one of the greatest Si accumulator plants with Si content in leaves above 4.7% of dry mass. In addition, Si supply may benefit nutrient-use efficiency with enhanced plant growth and without compromising the chemical–bromatological content of Xaraés palisadegrass.

The response of alfalfa genotypes to different concentrations of mobile aluminium

The morphological traits of alfalfa under acid soil conditions with different mobile aluminium (Al) concentrations were investigated. The study site was Vėžaičiai Branch of the Lithuanian Research Centre for Agriculture and Forestry, 55°70 N, 21°49 E. The experiment featuring the 30 most Al-tolerant alfalfa accessions (populations and cultivars), determined from laboratory trials was established on a Bathygleyic Dystric Retisol in 2018. In 2019 and 2020, the biological and morphological traits were evaluated: plant regrowth, plant height before flowering, wintering, leafiness, stem thickness, plant vigour, stem density, seed yield and resistance to spring black stem leaf spot. The resistance of alfalfa to mobile Al toxicity was determined using a filter-based screening method of selection cycles C1 and C2. The accessions grown in the soil with mobile Al (20.6–23.4 mg/kg) showed better tolerance to Al toxicity in the cycle C2. The hypocotyl tolerance index of these accessions was better at 8, 16, 32 and 64 mm AlCl3 concentrations in the cycle C2. The correlation analysis showed strong significant positive and negative relationships between the morphological traits. A cluster analysis showed that the accessions, grown in the soil with mobile Al (20.6–23.4 mg/kg) were the most resistant to Al toxicity in the cycle C2. These accessions produced a better seed yield and demonstrated lower values of morphological traits compared to cluster 2. Also, these accessions are considered as tolerant to mobile Al toxicity and might be used as donors in breeding for Al toxicity tolerance.

Deciphering the major metabolic pathways associated with aluminum tolerance in popcorn roots using label-free quantitative proteomics

Aluminum toxicity is one of the most important abiotic stresses that affect crop production worldwide. The soluble form (Al3+) inhibits root growth by altering water and nutrients uptake, which also reduces plant growth and development. Under a long term Al3+ exposure, plants can activate several tolerance mechanisms, and to date, there are no reports of large-scale proteomic data of maize in response to this ion. To investigate the post-transcriptional regulation in response to Al toxicity, we performed a label-free quantitative proteomics for comparative analysis of two Al-contrasting popcorn inbred lines and an Al-tolerant commercial hybrid during 72 h under Al-stress. A total of 489 differentially accumulated proteins (DAPs) were identified in the Al-sensitive inbred line, 491 in the Al-tolerant inbred line, and 277 in the commercial hybrid. Among them, 120 DAPs were co-expressed in both Al tolerant genotypes. Bioinformatics analysis indicated that starch and sucrose metabolism, glycolysis/gluconeogenesis, and carbohydrate metabolism were significant biochemical processes regulated in response to Al toxicity. The up accumulation of sucrose synthase and the increase of sucrose content and starch degradation suggest that these components may enhance popcorn tolerance to Al stress. The up-accumulation of citrate synthase suggests a key role of this enzyme in the detoxification process in the Al-tolerant inbred line. The integration of transcriptomic and proteomic data indicated that the Al tolerance response presents a complex regulatory network into the transcription and translation dynamics of popcorn roots development.

The Aluminum Distribution and Translocation in Two Citrus Species Differing in Aluminum Tolerance

Background: Many citrus orchards of south China suffer from soil acidification, which induced aluminum (Al) toxicity. The Al-immobilization in vivo is crucial for Al detoxification. However, the distribution and translocation of excess Al in citrus species were not well illustrated.Results: The seedlings of ‘Xuegan’ [Citrus sinensis (L.) Osbeck] and ‘Shatianyou’ [Citrus grandis (L.) Osbeck] that differed in Al tolerance were hydroponically treated with nutrient solution (Control) or supplemented by 1.0 mM Al3+ (Al toxicity) for 21 days after three months of pre-culture. The Al distribution at the tissue level of citrus species following the order: lateral roots > primary roots > leaves > stems. The fragmentation of fresh lateral roots revealed the ratio of Al distribution at the cell wall, cell organelle and cytoplasmic supernatant was about 8:2:1 of two citrus species under Al stress. Besides, the Al distribution at the lateral root cell wall components suggested the pectin is the most Al-accumulating site in citrus species. Compared to C. grandis, C. sinensis had a significantly higher Al concentration on the cell wall of lateral roots whereas remarkably lower Al levels on the leaves and stems. Furthermore, the Al translocation revealed by the absorption kinetics of the cell wall demonstrated that C. sinensis had a higher Al retention and stronger Al affinity on the root cell wall than C. grandis. According to the FTIR (Fourier transform infrared spectroscopy) analysis, the Al distribution and translocation might be affected by modifying the structure and components of the citrus lateral root cell wall. Conclusions: A higher Al-retention, mainly targeted by the pectin of the root cell wall, and a lower Al translocation efficiency from roots to shoots contributed to a higher Al tolerance of C. sinensis than C. grandis.

Mechanistic Association of Quantitative Trait Locus with Malate Secretion in Lentil (Lens culinaris Medikus) Seedlings under Aluminium Stress

Aluminium (Al) toxicity acts as a major delimiting factor in the productivity of many crops including lentil. To alleviate its effect, plants have evolved with Al exclusion and inclusion mechanisms. The former involves the exudation of organic acid to restrict the entry of Al3+ to the root cells while latter involves detoxification of entered Al3+ by organic acids. Al-induced secretion of organic acids from roots is a well-documented mechanism that chelates and neutralizes Al3+ toxicity. In this study, F6 recombinant inbred lines (RILs) derived from a cross between L-7903 (Al-resistant) and BM-4 (Al-sensitive) were phenotyped to assess variation in secretion levels of malate and was combined with genotypic data obtained from 10 Al-resistance linked simple sequence repeat (SSRs) markers. A major quantitative trait loci (QTL) was mapped for malate (qAlt_ma) secretion with a logarithm of odd (LOD) value of 7.7 and phenotypic variation of 60.2%.Validated SSRs associated with this major QTL will be useful in marker assisted selection programmes for improving Al resistance in lentil.

Influence of Aluminum at Low pH on the Rhizosphere Processes of Masson Pine (Pinus Massoniana Lamb)

Trees in general are very tolerant of aluminum (Al, mainly Al3+ at pH ≦ 5.0), and the small effects seen in the contaminated soils may mislead people that the contamination is unimportant. We believe that the assessments with Al-sensitive Masson pine could have revealed a bigger difference. The key point of this study was to characterize the Al toxicity for Masson Pine. The objectives were to discover the specific eco-physiological relationship between pine roots and rhizosphere Al, and to investigate the Al effects on several parameters, measured in the rhizosphere of Masson pine. Masson pine seedlings were cultivated on a hydroponic setup. Through comprehensive laboratory dose-gradient experiments, Al-triggered composition of the root-released compounds and several rhizospheric parameters were determined by chromatography or spectroscopy. This study gives an important evidence of the Al-toxicity effects on the composition of root-released compounds and the root growth of Masson pine. Results showed that higher rhizospheric Al at pH 4.5 might contribute to increased release of sugars, and also could stimulate the release of oxalic acid and malic acid. The total of secreted amino acids were correlated with the rhizosphere Al. Zero additional Al induced no rhizosphere pH elevation, but Al-induced rhizosphere acidification (pH from 4.50 to 4.22) was observed at Al 100 µM. Greater additions of Al (>300 µM) suppressed the rhizosphere acidification at pH 3.92. Added Al had a negative effect on the dry weight of pine roots, but an opposite effect on Al accumulated in the roots was observed. The four endogenous hormones were also determined in the pine roots. Gibberellic acid (GA3) decreased, whereas abscisic acid (ABA) increased simultaneously with the addition of Al. Their inflexional concentrations were most frequently observed at 100 µM, which might be the threshold of Al toxicity for Masson pine. The secondary metabolites assayed have been studied in relation to the rhizospheric Al. The rhizosphere Al species at low pH can trigger pine roots to release the sugars (glucose, fructose + aldose), organic acids (oxalic acid, and malic acid), amino acids, secondary metabolites, and endogenous hormones during their growth. Meanwhile it also affected the growth of pine roots. This is an extensive study, which can help understanding the toxicity of Al to this important pioneer species of acid forest soils in south China.