Figure - available from: Scientific Reports
This content is subject to copyright. Terms and conditions apply.
Al-induced changes in the Glu pathway for Pro biosynthesis in rye seedlings. Metabolite levels and enzyme activities were determined in leaves and roots of Al-tolerant (Beira) and Al-sensitive (RioDeva) genotypes after 24 h and 48 h of exposure and 48 h of recovery. Bars: purple: genotype Beira; red: genotype RioDeva; light color: control (no Al); dark color: 5 mg L⁻¹ Al. Panels: (a,b): glutamine (Gln); (c,d): glutamine synthetase (GS); (e,f): glutamate (Glu); (g,h): pyrroline-5-carboxylate dehydrogenase (P5CDH); (i,j): pyrroline-5-carboxylate synthase (P5CS). γGH: γ-glutamyl hydroxamate. The results are the mean of 3 or 4 experiments (SD, see Methods). Letters indicate a significant difference at P < 0.05 (capital letters: tolerant line; small letters: sensitive line).
Source publication
Aluminium (Al) toxicity limits crop productivity, particularly at low soil pH. Proline (Pro) plays a role in protecting plants against various abiotic stresses. Using the relatively Al-tolerant cereal rye (Secale cereale L.), we evaluated Pro metabolism in roots and shoots of two genotypes differing in Al tolerance, var. RioDeva (sensitive) and var...
Citations
... Aluminum affects biosynthesis and disturbs the balance of endogenous amino acids in plants [3,54,55]. The roots of wheat seedlings responded to Al toxicity by increased exudation of many proteinogenic amino acids [56]. ...
... The protective action of amino acids against Al toxicity has been repeatedly reported: arginine is involved in the biosynthesis of putrescine, leading to decreased Al retention in the cell walls of wheat [57]; cysteine increased the activity of glutathione [58]; GABA induced the antioxidant system in barley [59] and Arabidopsis thaliana [60]; glycine played a stress alleviating role as a component of glycine betaine in rice [61] and glycine-rich proteins in A. thaliana [62]; phenylalanine was involved in the biosynthesis of phenylpropanoids and flavonoids with defense functions in alfalfa [63,64]; proline protected root cells as an osmolyte [55,61,65]; threonine activated H + -ATPase in soybean [66]. Four of these amino acids (Arg, Cys, GABA, and Gly) were exuded more by the E107 (brz) mutant treated with Al (Figure 8a-d). ...
It is well known that plant-growth-promoting rhizobacteria (PGPRs) increase the tolerance of plants to abiotic stresses; however, the counteraction of Al toxicity has received little attention. The effects of specially selected Al-tolerant and Al-immobilizing microorganisms were investigated using pea cultivar Sparkle and its Al-sensitive mutant E107 (brz). The strain Cupriavidus sp. D39 was the most-efficient in the growth promotion of hydroponically grown peas treated with 80 µM AlCl3, increasing the plant biomass of Sparkle by 20% and of E107 (brz) by two-times. This strain immobilized Al in the nutrient solution and decreased its concentration in E107 (brz) roots. The mutant showed upregulated exudation of organic acids, amino acids, and sugars in the absence or presence of Al as compared with Sparkle, and in most cases, the Al treatment stimulated exudation. Bacteria utilized root exudates and more actively colonized the root surface of E107 (brz). The exudation of tryptophan and the production of IAA by Cupriavidus sp. D39 in the root zone of the Al-treated mutant were observed. Aluminum disturbed the concentrations of nutrients in plants, but inoculation with Cupriavidus sp. D39 partially restored such negative effects. Thus, the E107 (brz) mutant is a useful tool for studying the mechanisms of plant–microbe interactions, and PGPR plays an important role in protecting plants against Al toxicity.
... It is however essential, for agronomical, agroecological, and ecological reasons, to obtain a direct understanding of abiotic stress sensing and signaling mechanisms in cultivated crops [3,43,46] and in natural plant communities [3,4,47]. For example, in the cases of natural extremophile plants (Table 2) [48-54], of wild or cultivated tree species (Table 3) [48, 55-62], or of major cereal or pseudocereal crops other than rice (Table 4) [46, [63][64][65][66][67][68][69][70], some relationships between adaptive biochemical or physiological responses and signaling processes have been characterized or hypothesized. ...
Characterizing the mechanisms of plant sensitivity and reactivity to physicochemical cues related to abiotic stresses is of utmost importance for understanding plant-environment interactions, adaptations of the sessile lifestyle, and the evolutionary dynamics of plant species and populations. Moreover, plant communities are confronted with an environmental context of global change, involving climate changes, planetary pollutions of soils, waters and atmosphere, and additional anthropogenic changes. The mechanisms through which plants perceive abiotic stress stimuli and transduce stress perception into physiological responses constitute the primary line of interaction between the plant and the environment, and therefore between the plant and global changes. Understanding how plants perceive complex combinations of abiotic stress signals and transduce the resulting information into coordinated responses of abiotic stress tolerance is therefore essential for devising genetic, agricultural, and agroecological strategies that can ensure climate change resilience, global food security, and environmental protection. Discovery and characterization of sensing and signaling mechanisms of plant cells are usually carried out within the general framework of eukaryotic sensing and signal transduction. However, further progress depends on a close relationship between the conceptualization of sensing and signaling processes with adequate methodologies and techniques that encompass biochemical and biophysical approaches, cell biology, molecular biology, and genetics. The integration of subcellular and cellular analyses as well as the integration of in vitro and in vivo analyses are particularly important to evaluate the efficiency of sensing and signaling mechanisms in planta. Major progress has been made in the last 10–20 years with the caveat that cell-specific processes and in vivo processes still remain difficult to analyze and with the additional caveat that the range of plant models under study remains rather limited relatively to plant biodiversity and to the diversity of stress situations.Key wordsClimate changeDroughtExtreme temperaturesFood securityMultiple stressOxidative stressStress responsesSignal transductionStress sensors
... In this study, we used rye (Secale cereale L.), which is considered the most Al-tolerant Triticacae cereal (Ryan et al., 2011) and compared responses in an Al-tolerant (Beira) and an Al-sensitive (RioDeva) genotype De Sousa et al., 2020). Specifically, our study aimed to investigate the subcellular distribution of Al in leaves and its relation to the effects on photosynthesis and respiration. ...
Aluminum (Al) toxicity limits crops growth and production in acidic soils. Compared to roots, less is known
about the toxic effects of Al in leaves. Al subcellular compartmentalization is also largely unknown. Using rye
(Secale cereale L.) Beira (more tolerant) and RioDeva (more sensitive to Al) genotypes, we evaluated the patterns
of Al accumulation in leaf cell organelles and the photosynthetic and metabolic changes to cope with Al toxicity.
The tolerant genotype accumulated less Al in all organelles, except the vacuoles. This suggests that Al
compartmentalization plays a role in Al tolerance of Beira genotype. PSII efficiency, stomatal conductance,
pigment biosynthesis, and photosynthesis metabolism were less affected in the tolerant genotype. In the Calvin
cycle, carboxylation was compromised by Al exposure in the tolerant genotype. Other Calvin cycle-related en�zymes, phoshoglycerate kinase (PGK), glyceraldehyde 3-phosphate dehydrogenase (GAPDH), triose-phosphate
isomerase (TPI), and fructose 1,6-bisphosphatase (FBPase) activities decreased in the sensitive line after 48 h
of Al exposure. Consequentially, carbohydrate and organic acid metabolism were affected in a genotype-specific
manner, where sugar levels increased only in the tolerant genotype. In conclusion, Al transport to the leaf and
compartmentalization in the vacuoles tolerant genotype’s leaf cells provide complementary mechanisms of Al
tolerance, protecting the photosynthetic apparatus and thereby sustaining growth.
... The significant positive effect of proline that appeared in this study may be due to its role in stabilizing subcellular structures (such as membranes and proteins), scavenging free radicals, and buffering cellular redox potential under stress. It may also act as a source of energy, carbon, and nitrogen to support plant growth under stress and as a protein-compatible hydrotrope, reducing cytoplasmic acidosis and maintaining metabolically acceptable NADP + /NADPH ratios (de Sousa et al., 2020). Exogenous proline, an amino acid that enhances growth and other physiological characteristics of plants, assists plants in recovering from stress rapidly, maintaining the turgidity of cells under stress, and increasing photosynthesis rates (Hayat et al., 2012). ...
The salinity of irrigation water is one of the major abiotic stresses that have a variable reaction to soil structure, which has detrimental impacts on seedling development and quality. The osmolytes can help lessen these adverse effects on the establishment of Moringa oleifera seedlings. Therefore, this study was conducted in Egypt (30″53′30, 87″ N and 30″41′29, 77″ E) using polyethylene bags during May-July 2020 and 2021. Three factors in a factorial split-split plot experiment were arranged in randomized complete block design. The main plots were soil structure; sand:clay 2:1 (V/V) and sand 100 %, whereas the subplot treatments were salinity levels; tap water as a control 0.5, 1.5, 4, and 6 dS m −1 , and sub-subplot osmolytes; tap water as a control, and glycine betaine, mannitol, proline, and sorbitol all at 0.2 g L −1 as a soil drench. This study aimed to evaluate the effects of osmolytes and soil structure on growth parameters and phenylalanine ammonia lyase (PAL) gene expression in Moringa seedlings. The study concluded that Moringa seedlings in sand:clay performed significantly (P ˂ 0.05) better than those in the sand. With increasing salinity levels, osmolytes enhanced all seedling growth parameters and PAL gene expression compared with the control in the two soil structures. The order of tolerance to salinity stress was sorbitol ˃ proline ˃ mannitol ˃ glycine betaine ˃ control. Moringa seedlings produced in sand:clay treated with 0.2 g L −1 sorbitol and salinity at 4 or 6 dS m −1 were superior in most growth parameters and PAL gene expression.
... In our experiments drought-susceptible genotype (Dobrudjanka) had highest increase in proline content, while on the contrary, droughtresistant Jantar had lowest proline content under drought stress. It could be speculated that accumulated free proline was useful in recovery processes as C and N sources for resuming normal metabolic processes upon stress relief (de Sousa et al. 2020). Obtained here results also support the probability of the above hypothesis. ...
Extreme environmental conditions are among the factors most frequently responsible for serious reduction in crop yield. Various abiotic stresses threaten wheat production worldwide and drought in particular is especially harmful when occurring at early vegetation phases. Four wheat varieties were compared with respect to their drought tolerance by withholding water in soil pot experiments and their ability to recover after re-watering was assessed based on changes in physiological and biochemical parameters. Drought caused significant decrease in leaf water content, increased the accumulation of hydrogen peroxide, malondialdehyde, free proline, and enhanced electrolyte leakage from cellular membranes. Water deprivation provoked oxidative stress which activated plants’ antioxidant defense system. The intensity of stress perception differed among the four wheat genotypes and they displayed diverse strategies for overcoming the imposed stress. While drought-resistant varieties responded to the stress via enhanced activity of ROS detoxifying enzymes, drought-sensitive genotypes employed coping mechanism involving accumulation of non-enzymatic components of the antioxidant defense system which were useful during the recovery process.
... In this study, we used rye (Secale cereale L.), which is considered the most Al-tolerant Triticacae cereal (Ryan et al., 2011) and compared responses in an Al-tolerant (Beira) and an Al-sensitive (RioDeva) genotype De Sousa et al., 2020). Specifically, our study aimed to investigate the subcellular distribution of Al in leaves and its relation to the effects on photosynthesis and respiration. ...
... We found higher N content and NR activity in lotus, especially under stress conditions. NR activity, N levels, and N/C ratios were less reduced in the tolerant rye line, which showed an upregulated Orn pathway [71]. Overall, Pro content strongly increased in barley and lotus, although through different mechanisms, and possibly is directly linked with the N status in plants. ...
Arbuscular mycorrhizal fungi (AMF) can promote plant growth and induce stress tolerance. Proline is reported to accumulate in mycorrhizal plants under stressful conditions, such as aluminum (Al) stress. However, the detailed changes induced in proline metabolism under AMF-plant symbiosis has not been studied. Accordingly, this work aimed to study how Al-stressed grass (barley) and legume (lotus) species respond to AMF inoculation at growth and biochemical levels. The associated changes in Al uptake and accumulation, the rate of photosynthesis, and the key enzymes and metabolites involved in proline biosynthesis and degradation pathways were studied. Soil contamination with Al induced Al accumulation in tissues of both species and, consequently, reduced plant growth and the rate of photosynthesis, while more tolerance was noticed in lotus. Inoculation with AMF significantly reduced Al accumulation and mitigated the negative impacts of Al on growth and photosynthesis in both species; however, these positive effects were more pronounced in barley plants. The mitigating action of AMF was associated with upregulation of proline biosynthesis through glutamate and ornithine pathways, more in lotus than in barley, and repression of its catabolism. The increased proline level in lotus was consistent with improved N metabolism (N level and nitrate reductase). Overall, this study suggests the role of AMF in mitigating Al stress, where regulation of proline metabolism is a worthy mechanism underlying this mitigating action.
... To the best of our knowledge, the current study will be one of the earliest studies aimed at investigating the effects of different concentrations of crude oil in the soil on growth, oxidative stress, and antioxidative response in rye plants. Moreover, since genotypes within the species are known to vary in their resistance to environmental stress, two rye varieties were chosen for the current study due to their resistance to low temperatures, soil acidity, and increased concentration of aluminum ions [31][32][33]. The results of the current study will contribute to an increased knowledge about (i) the growth and physiological responses of two rye varieties to various levels of oil pollution in the soil, (ii) oxidative stress induced in rye plants in conditions of soil pollution with crude oil, and (iii) the reaction of low molecular weight antioxidants and antioxidative enzymes in two rye varieties growing on the oil-contaminated soil. ...
... The current study was devoted to investigating the effect of different oil concentrations on two rye varieties-Krona and Valdai. Previous studies have shown that these varieties differ in winter hardiness and their resistance to low temperatures, acidification, and high content of aluminum ions in the soil [31][32][33]. The current study revealed that a significant decrease in shoot biomass was observed in the Krona variety at 6% oil concentration in the soil (by 24% lower compared to the control) and in the Valdai variety at 12% oil concentration in the soil (by 25% lower compared to the control). ...
... Proline accumulation in plants can regulate the osmotic potential of cells, stabilize the cell structure, and remove excess reactive oxygen species, thereby improving the resistance of rye to environmental stress [31,48]. The current study revealed that proline content in rye shoots increased with an increase in the oil concentration in the soil. ...
Rye (Secale cereale L.) is one of the most important cereal crops in Eastern and Northern Europe, showing better tolerance to environmental stress factors compared to wheat and triticale. Plant response to the crude oil-polluted soil depends on plant species, oil concentration, time of exposure, etc. The current study is aimed at investigating the growth, oxidative stress and the response of antioxidative system of two rye varieties (Krona and Valdai) cultivated on crude oil-contaminated soils at different concentrations (1.5, 3.0, 6.0, and 12.0%). Inhibition of rye growth was observed at crude oil concentrations of above 3% for above-ground plant parts and of above 1.5% for roots. A decrease in content of chlorophyll a and total chlorophylls in Krona variety was detected at 1.5% oil concentration in soil and in Valdai variety at 3% oil concentration. Compared with the control, the content of malondialdehyde was significantly increased in the Krona variety at 3% oil concentration and in Valdai variety at 6% oil concentration. The crude oil-induced oxidative stress was minimized in rye plants by the enhanced contents of low-molecular antioxidants (proline, non-protein thiols, ascorbic acid, phenolic compounds) and activities of superoxide dismutase, catalase, ascorbate peroxidase, and glutathione peroxidase. The strongest positive correlation was detected between the content of malondialdehyde and contents of proline (r = 0.89–0.95, p ≤ 0.05) and phenolic compounds (r = 0.90–0.94, p ≤ 0.05) as well as superoxide dismutase activity (r = 0.81–0.90, p≤ 0.05). Based on the results of a comprehensive analysis of growth and biochemical parameters and of the cluster analysis, Valdai variety proved to be more resistant to oil pollution. Due to this, Valdai variety is considered to be a promising rye variety for cultivation on moderately oil-polluted soils in order to decontaminate them. At the same time, it is necessary to conduct further studies aimed at investigating oil transformation processes in the soil-rye system, which would make it possible to determine the efficiency of using this cereal for soil remediation.
Aluminum (Al) is the third most ubiquitous metal in the earth’s crust. A decrease in soil pH below 5 increases its solubility and availability. However, its impact on plants depends largely on concentration, exposure time, plant species, developmental age, and growing conditions. Although Al can be beneficial to plants by stimulating growth and mitigating biotic and abiotic stresses, it remains unknown how Al mediates these effects since its biological significance in cellular systems is still unidentified. Al is considered a major limiting factor restricting plant growth and productivity in acidic soils. It instigates a series of phytotoxic symptoms in several Al-sensitive crops with inhibition of root growth and restriction of water and nutrient uptake as the obvious symptoms. This review explores advances in Al benefits, toxicity and tolerance mechanisms employed by plants on acidic soils. These insights will provide directions and future prospects for potential crop improvement.
Excess aluminum (Al) is a stressful condition that affects plant growth and yield quality. This study evaluates growth responses and changes in the contents of photosynthetic pigments and organic solute in maize (Zea mays L.) plants inoculated with Trichoderma asperelloides isolates (T01, T02, T74, T76, or T96) and treated with increasing doses of Al (0, 50, 100, 150, and 200 µM of Al). Uninoculated unstressed plants served as control. Absolute growth rate, root length, dry biomass (shoot, roots and total) and shoot:root ratio were significantly affected in Al-stressed maize plants inoculated with T. asperelloides. Also, chlorophylls (a, b and total) were significantly reduced, whereas carotenoids and anthocyanins increased in those plants. Except for carotenoids, all parameters increased in plants inoculated with T. asperelloides, especially T01 or T02 isolates. Anthocyanins increased by 50% in plants inoculated with T74 and treated with 100 or 150 µM Al as compared to control plants. Total soluble carbohydrates increased by 74% and 101% in plants inoculated with T74 and T76, respectively, and treated with 200 µM Al. Total free amino acids increased more than 50% in plants inoculated with T02 and treated with 150 and 200 µM Al. Free prolines increased by 90%, 145% and 165% in plants inoculated with T74 and treated 100, 150 and 200 µM Al, respectively, in comparison to the unstressed control plants. We concluded that T. asperelloides positively affected growth, photosynthetic pigments, and organic solutes of Al-stressed plants, especially those inoculated with T01, T02, or T74 isolates.
Supplementary information:
The online version contains supplementary material available at 10.1007/s13205-022-03310-3.
