How does aluminum affect plants

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New Phytologist , — Similarly, in roots and cell suspensions of tea plants, Al induces the activation of antioxidant enzymes, increases the integrity of the membrane and reduces lignification and aging, which could be a possible reason for the stimulation of root growth Ghanati et al. The beneficial effect of Al on plants has also been associated with the regulation of C and N metabolism. The shrub M. In tea plant roots, it has been suggested that the secretion of caffeine induced by Al can increase root growth by inhibiting callus deposits Morita et al.

Also, Al positively regulates the biosynthetic pathway of caffeine in suspension cells of C. There is also evidence indicating that Al increases the content of chlorophyll, carotenoids, sugars, amin oacids such as proline and cysteine, hormones, and metabolites of the Shikimico acid pathway in woody and crop plants Hajiboland et al. In fact, glucose has been suggested as an energy source which is a key element in the promotion of root growth, in the presence of Al. Moreover, glucose and abscisic acid ABA may participate as signaling molecules which promote the root growth induced by Al, acting on the metabolism of N and C Moriyama et al.

For instance, Al increases the concentration of soluble sugars and differentially regulates the expression of NAC transcription factors, which in turn may enhance growth and biomass production in rice plants Moreno-Alvarado et al. In corn, stimulation of leaf growth has been associated with greater protein synthesis Wang et al. It has also been suggested that the beneficial effect of Al on root growth and morphological changes is associated with changes in the levels of plant growth regulators PGR.

Aluminum is capable of inducing, directly or indirectly, synthesis or transportation of PGR. In the conifer Picea abies , an increase in the levels of indole-acetic acid IAA , cytokinins and gibberellins has been reported in the roots in the presence of Al; these changes are in correlation with the morphological changes and the stimulation of lateral roots close to the root apex.

The formation of new roots in Q. Aluminum plays an important role in the color changes of some hyperaccumulator plants. In hydrangea Hydrangea macrophylla , Al and pH are important factors for the change of color in the sepals, from red to blue Ito et al.

The blue coloring is formed from the union of Al with metalloanthocyanins, delphinidin 3-glucoside and 5- O -caffeoylquinic acid Oyama et al. In the genus Camellia , the purple color of Camellia japonica flowers cv.

Sennen-fujimurasaki and the intense yellow tone of Camellia chrysanthaes are generated by the chelation of the Al ions with anthocyanins and flavonoids quercetin , respectively Tanikawa et al.

Anthropologically, the leaves and bark of species of the genus Simplocos are used by weavers as mordant in textile dyeing due to their high content of Al Schmitt et al.

Aluminum is also the primary factor in reducing crop yields in acid soils Ma et al. The initial and most dramatic Al toxicity symptom is the inhibition of root elongation Delhaize and Ryan, Because Al is a highly reactive element, there are innumerable mechanisms of toxicity involving the cell wall Jones et al.

Aluminum is widely reported as toxic to most plants Sade et al. There are a number of symptoms caused by aluminum toxicity in plants Figure 3 , all associated with severe changes in the root system Kopittke and Blamey, Al interferes with cell division at the root apex and lateral roots, increases the rigidity of the cell wall by cross-linking of pectins and reduces DNA replication because of increased rigidity of the double helix Zhang et al.

Moreover, Al induces a series of cellular toxic changes concerning cell division and nucleolus, and localization and expression of the nucleolar proteins such as fibrillarin Zhang et al. Aluminum tends to bond with phosphorus P in a less available and insoluble form in soils and plant roots, thereby creating a P deficiency for plant growth.

Aluminum also decreases root respiration, interferes with enzymes governing the deposition of polysaccharides in cell walls, decreases the synthesis and transport of cytokinins, and modifies the structure and function of plasma membranes which interfere with the uptake, transport, and use of multiple elements Ca, Mg, P, and K , as well as water uptake by roots plants Foy, ; Foy et al. In plants these symptoms are linked to disorders that are generally divided into two categories: 1 long-term responses, requiring hours to develop, and 2 short-term responses that can be measured within a few minutes or even a few seconds after exposure to Al Taylor, ; Simoes et al.

The first signs of these responses related to Al toxicity have been observed after one hour Ownby and Popham, Moreover, the most important response to the application of Al seems to be short term interruption of Ca influx through the plasma membrane Jones et al. Aluminum and other metals are non-biodegradable, they remain in the environment and are able to circulate in the food chain, posing a serious threat not only to plants but also to animals and humans Jackson and Huang, ; Exley, ; Ashenef, For example, tea plants contain a substantial amount of Al in leaves, and thus it is present in tea leaf infusions.

Although only a small proportion of Al is available for absorption in the gastrointestinal tract and the renal excretion of Al is fairly effective, this metal can cause serious problems or possible health risks in humans Exley, ; Mehra and Baker, Plants have developed different mechanisms of tolerance to counteract the toxic effects of Al. These mechanisms can be divided into two forms Figure 3 : mechanisms of exclusion or resistance to Al, the function being to avoid or reduce the entrance of Al to the cell; and mechanisms of internal tolerance which compartmentalize Al in vacuoles or stabilize them in order to inhibit its toxicity.

A small increment in the rhizospheres pH reduces the solubility, activity, toxicity and content of Al in plants through exclusion of the metal in the root apoplast Yang Y. OA can also increase or reduce rhizosphere pH in the presence of other metals, as well as Al Kochian et al.

Aluminum plays a positive role in growth increase in tea Konishi et al. Soil acidification might maintain the solubility and Al uptake in tea. In contrast, acidification of the rhizosphere increases toxicity and metal accumulation in Al-sensitive species Houman et al.

The root cell wall is the main binding site of Al and thus is the target of Al toxicity and exclusion in plants Horst et al.

At present, physiological, biochemical and molecular evidence is available which has demonstrated that modification of the cell wall composition plays an important role in the resistance to Al Levesque-Tremblay et al. The increase in the polysaccharide content of the cell wall induced by Al can reduce water and nutrient uptake, as well as cellular wall elasticity Nguyen et al. Among the cereals, rice is the crop with most tolerance to Al Yang et al. In rice cultivars which differ in their Al-resistance, a positive correlation between polysaccharide content pectin and hemicellulose in the root apex and the accumulation of Al has been observed, indicating the importance of the cell wall composition in the exclusion of Al Yang et al.

The pectin content and its degree of methylation in the cell wall contribute to the differences in resistance to Al Eticha et al. In Arabidopsis and other plant species, the regulation of genes and expansin enzymes, pectin methyltransferases and xiloglucano endohydrolases reduce binding and accumulation of Al in the root apex by changing the load and the porosity of the cell wall Yang J.

The physicochemical and physiological properties of the plasma membrane also affect tolerance of the plants to Al. The lipid composition of the plasma membrane PM has an important role in Al-tolerance Wagatsuma et al. The phospholipids create a negative charge on the surface of the PM and increase the sensitivity to Al, as a result of the union of the metal to the PM. In rice and timber species M. Similarly, the sterol content also plays an important role in the tolerance to stress by Al.

High sterol content in combination with low contents of phospholipids is a common strategy for Al-tolerance in different plant species Khan et al. It has also been suggested that a small peptide, anchoring the PM, could prevent Al-influx in root cells through bonding with cation and thus contribute to the resistance in rice Xia et al. The release of OA in the root is the Al exclusion mechanism most widely described in plants Kochian et al. The organic anions, malate, citrate and oxalate are secreted by the root and chelate Al in a non-toxic Al-OA complex, protecting the root apex and permitting it to grow.

Malate and citrate are ubiquitous in all plant cells given that they are part of the tricarboxylic acid TCA cycle in the mitochondria, while oxalate participates in the regulation of Ca and the detoxification of metals Brunner and Sperisen, Evidence in different species of cultivable plants and timber trees indicates that OA efflux confers resistance to Al Delhaize et al. In a wheat genotype resistant to Al Delhaize et al. The heterologous expression of TaALMT1 in barley Hordeum vulgare and tobacco Nicotiana tabacum allowed the malate efflux and an increase in Al-resistance Delhaize et al.

On the other hand, the citrate efflux is mediated by the family of MATE proteins Multidrug and toxic compound extrusion. To date, the molecular components of oxalate efflux have not been identified.

In tea plants and other woody species such as poplar Populus tremula and buckwheat Fagopyrum esculentum , oxalate is an important element in the detoxification of Al in the root Qin et al. In addition to the OA, the exudation of other organic compounds in the root has been suggested for the chelation of Al Kochian et al. Studies on Eucalyptus camaldulensis have revealed secretion in the root of a ligand with low molecular weight binding to Al Tahara et al. In tea plants, an increase in the release of caffeine, a phenolic compound, has been observed in response to exposition to Al Morita et al.

Other ligands released in the root include the phenolic compounds catechol, catechin, and quercetin , flavonoids, succinate, phosphates, UDP-glucose and polysaccharides in the form of mucilage Kidd et al.

In fact, root mucilage plays an important role as a mechanism of resistance to metals Morel et al. Mucilage is a gelatinous material consisting of polysaccharides of high molecular weight which are exuded from the most external layers of the root apex.

Due to the fact that the mucilage contains uronic acid and pectin, the carboxil groups of this acid and of the pectin can ligate metallic cations such as Al Watanabe et al. In cowpea Vigna unguiculata , wheat and corn a strong binding of mucilage-Al has been reported and this bond is not toxic for the plant Horst et al. The function of the root cap or calyptra and the border cells is to protect the mother cells of the root apex from microbes and soil stresses, and also to receive and transmit environmental signals which will ultimately determine root growth Endo et al.

In many plant species, the root cap and border cells produce and exude mucilage, rich in polysaccharides, which can bind to metallic cations Horst et al. In genotypes of bean Phaseolus vulgaris , barley, soybean and castor Ricinus communis , resistant to Al, the exclusion of the metal is associated with the immobilization and detoxification of Al with the mucilage secreted by the root cap and border cells Miyasaka and Hawes, ; Zhu et al.

In contrast, the mucilage secreted by the root cap of M. In pea Pisum sativum plants, it has been observed that removal of the border cells increases the sensitivity and absorption of Al, indicating the important role of the border cells as mechanisms of Al exclusion Yu et al.

Furthermore, in Acacia mangium , a legume tropical forest tree known to be resistant to Al, the root apex was found to be surrounded by a cap type structure, the purpose of which is to protect the root from the flexion induced by Al Endo et al. Recent evidence has demonstrated that the exogenous addition and availability of certain elements prevents Al toxicity in plants.

Similarly, the exogenous addition of Si in corn prevents the inhibition of root elongation and callous deposition through the formation of hydroxy aluminosilicates in the root apex Wang et al. In pea and rice, the application of Si reduced the content of Al in the roots, stem and leaves Singh et al. In addition to being cofactor of many enzymes and a central component of chlorophyll, Mg also prevents metal phytotoxicity, including Al. High concentrations of Mg mM prevent Al toxicity by competing in uptake and interaction with the binding sites in the cell wall and the plasma membrane Bose et al.

Prevention of Al toxicity by supplementation with B has been reported in a large number of plants. Boron can act synergically with Ca and prevent binding of Al to the cell wall Hossain et al.

Recent evidence in pomelo Citrus grandis suggests that B prevents Al-toxicity by regulating different genes associated with modification of the cell wall, cellular transport, metabolism, signal transduction and antioxidant activity Wang et al.

Similarly, the addition of P prevents the effect of Al-toxicity on root growth and photosynthetic machinery of C. The P-deficiency also reduces Al-toxicity by changing the properties of the plasma membrane and cell wall, while high P increases the toxicity of the metal, possibly through the precipitation of Al-P on the root surface Maejima et al. Hormones and polyamines play an important role in the tolerance to stress by Al. The exogenous addition of auxins indole-acetic acid, IAA reduces the accumulation of Al in the root apex in wheat Wang et al.

Both processes participate in resistance to stress by Al through chelation of Al-citrate and pH changes in the rhizosphere Wang S. The polyamine putrescine Put and nitric oxide are also involved in the modulation of citrate secretion from roots of red bean Wang et al.

The Al-induced root inhibition could be alleviated by Put through decreased ethylene production Yu Y. Putrescine has been identified as an important signaling molecule involved in Al tolerance in plants Chen et al.

Some factors of abiotic stress such as drought and hypoxia can indirectly reduce the accumulation of Al and its effect on plants. In bean, drought stress changes the porosity of the cell wall and reduces the Al-binding Zhang et al. Mycorrhiza association can also prevent Al-toxicity in acid soils Seguel et al.

The mechanism of internal detoxification of Al involves the chelation of metal with OA and subsequent sequestration into the vacuole. Many tolerant plants, including the hyperaccumulators of Al, use the OA for the sequestration of Al in the cytosol of the root cells and also to remobilize or to translocate Al toward the shoots. Fagopyrum esculentum uses oxalate for the internal and external chelation of Al Ma et al.

Oxalate is the predominant ligand in the root cytosol of tea and forms Al-oxalate compounds Morita et al. A mechanism similar to that of tea is observed in buckwheat Wang et al. In the shrub M. In addition to the OAs, the phenolic compounds can bind to Al and form a complex in the cytosol. For example, in tea plants, catechin forms a complex with Al Nagata et al. In the sepals of H. It has also been suggested that the hydroxamates can bind to Al in the root Poschenrieder et al.

In the sap of tea leaves, the Al-F compound has been identified as a mechanism of tolerance to F Yang Y. Transportation through biological membranes requires transport proteins. In plants, Al transportation through the plasma membrane and the vacuole tonoplast has not been widely studied.

AtALS3 is a partial, type ABC transporter which is located in the PM of the epidermal cells of the root cortex, and in phloem cells throughout the plant.

It is believed that AtASL3 distributes Al inside the plant far from the root apex sensitive to Al , by transporting Al directly or bound to a ligand Kang et al. However, it has been suggested that it might participate in Al efflux from the root after absorption of the metal Larsen et al.

In fact, the Al efflux has been proposed as an exclusion mechanism Arunakumara et al. Mutation of the transporter AtALS3 results in hypersensitivity to Al and an increase in the accumulation of the metal in the roots of Arabidopsis Larsen et al. AtALS1 is also a partial, type ABC protein and probably participates in intracellular transportation of Al in vacuoles of root cells and vascular cells of the plant Larsen et al.

OsALS1 is located in the tonoplast of root cells and participates in the compartmentalization of Al in the vacuoles, which is required for the internal detoxification of Al in rice Huang et al. The Nrat1 transporter is a member of the Nramp family of transporters located in the PM of all root apex cells, except in the epidermal cells Xia et al.

It has been demonstrated that the protein Nrat1 exhibits the activity of Al transportation, but not for divalent metals such as Fe, Mn, and Cd or Al-citrate compounds Xia et al. Moreover, it has been suggested that Nrat1 is required for detoxification of Al in the cell wall as it reduces metal levels through Al-influx to the root cells and their subsequent compartmentalization in the vacuole, possibly by OsALS1 Xia et al.

Given that the mutant nrat1 presents increased sensitivity to Al and the over-expression of Nrat1 in yeast, rice and Arabidopsis increases Al uptake Xia et al. Recently, Wang et al. Moreover, a recent report mentions that endocytic vesicular traffic can contribute to the internalization of Al in the root apex of rice.

In plants, the mechanisms of exclusion and tolerance to Al are intimately related to mitochondrial activity, mitochondrial metabolism and OA transportation Nunes-Nesi et al. Overexpression of the enzymes citrate synthase, malate dehydrogenase and pyruvate phosphate dikinase confers resistance to Al by increasing the synthesis and exudation of OA Deng et al.

Therefore, the increase in mitochondrial biochemical activity is important for the synthesis of OA under stress by Al. Alternative metabolic routes of cellular respiration also participate in tolerance to stress by Al. Similarly, the overexpression of mitochondrial alternative oxidase AOX increases the respiration and reduces the oxidative stress induced by Al in the mitochondria Panda et al. Lou et al. In tomato Solanum lycopersicum roots proteins have been identified which play an important role in Al exclusion and tolerance Zhou S.

Gallagher et al. Toxicity by Al is also associated with the metabolism of nitrogen N Foy and Fleming, Transcriptome analyses in lucerne roots reveal candidate Al-stress-responsive genes involved in ribosome, protein biosynthesis, TCA cycle, membrane transport organic, small molecules and ions and hormonal regulation. However, the ribosome protein genes was the pathway with the largest numbers of genes differentially up-regulated, which suggested a high biological importance for ribosomal genes and an alternative in response to Al stress in plants Liu et al.

Recently identified Arabidopsis mutants with increased Al tolerance provide evidence of DNA as one of the main targets of Al Eekhout et al. Al treatment results in binding of Al to the negative charges of the phosphodiester backbone DNA. In fact, nuclei have been reported to accumulate Al even in the presence of low environmental concentrations. Also, Al stress gives rise to changes in the localization and expression of the nucleolar proteins and inhibition of DNA synthesis, as well as promoting DNA fragmentation and the generation of micronuclei Zhang et al.

In Arabidopsis plants, this Al- induced DNA damage triggered the activation of a cell cycle arrest causing root growth inhibition, at least partly Rounds and Larsen, Eekhout et al.

The DDR pathway introduces a transient cell-cycle arrest during the process of DNA repair, through the coordinated expression of DNA repair and cell-cycle inhibitory genes, thus ensuring that both the daughter cells inherit a complete and error free copy of the genome.

This insight could lead the way for novel strategies to generate Al-tolerant crop plants Hu et al. Much interest has been shown recently in the use of biostimulants and stimulants in agriculture with the aim of increasing root growth, nutrient uptake and tolerance to stress in plants.

Plant biostimulants or agricultural stimulants include microorganisms and a diversity of substances, among which are the beneficial elements Calvo et al. Aluminum Al , cobalt Co , selenium Se , sodium Na , and silicon Si are considered to be beneficial elements for plants, given that, despite the fact that they are not required by all plants, they can promote growth and are essential for certain plant taxa, depending on the environmental conditions, concentration of the element and plant species.

These elements can also increase tolerance to abiotic stress drought, salinity, high temperatures, cold, UV light, toxicity or nutrient deficiency as well as biotic stress pathogens and herbivores when administered at low concentrations. Aluminum stimulates growth in plants of economic importance such as the tea shrub and can maintain or fix floral colors, as in the case of hydrangeas; therefore its application as a biostimulant of a desirable response in these plants is feasible Fang et al.

However, high concentrations of Al can pose a serious threat to agricultural production due to inhibition of root elongation and plant growth through a diversity of mechanisms with the participation of Al, including interactions in the symplast, plasma membrane and the cell wall Kochian et al. In addition to the plants, Al can also cause serious problems in the nervous system, lungs and kidneys of human beings. Tea is an important dietetic source of Al for human beings.

There is a great need to understand how environmental factors can have an influence on the accumulation of Al in tea leaves in order to create strategies for the reduction of Al uptake in tea plants de Silva et al. The root system is complex and a wide variety of root phenotypes have been identified which contribute to the adaptation to toxicity by Al Rao et al. A greater root surface induced by Al can increase the uptake of water and nutrients by plants Hajiboland et al.

Further studies on the use of low concentrations of Al to prevent the effect of different conditions of stress must be considered. EB-Q designed, planned, wrote, and checked the manuscript. CE-M wrote the manuscript. IE-M checked the manuscript. MM-E group leader, wrote and checked the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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