Exploring Aluminum Tolerance Mechanisms in Plants with Reference to Rice and Arabidopsis: A Comprehensive Review of Genetic, Metabolic, and Physiological Adaptations in Acidic Soils

Abstract

Aluminum (Al) makes up a third of the Earth's crust and is a widespread toxic contaminant, particularly in acidic soils. It impacts crops at multiple levels, from cellular to whole plant systems. This review delves into Al's reactivity, including its cellular transport, involvement in oxidative redox reactions, and development of specific metabolites, as well as the influence of genes on the production of membrane channels and transporters, alongside its role in triggering senescence. It discusses the involvement of channel proteins in calcium influx, vacuolar proton pumping, the suppression of mitochondrial respiration, and the initiation of programmed cell death. At the cellular nucleus level, the effects of Al on gene regulation through alterations in nucleic acid modifications, such as methylation and histone acetylation, are examined. In addition, this review outlines the pathways of Al-induced metabolic disruption, specifically citric acid metabolism, the regulation of proton excretion, the induction of specific transcription factors, the modulation of Al-responsive proteins, changes in citrate and nucleotide glucose transporters, and overall metal detoxification pathways in tolerant genotypes. It also considers the expression of phenolic oxidases in response to oxidative stress, their regulatory feedback on mitochondrial cytochrome proteins, and their consequences on root development. Ultimately, this review focuses on the selective metabolic pathways that facilitate Al exclusion and tolerance, emphasizing compartmentalization, antioxidative defense mechanisms, and the control of programmed cell death to manage metal toxicity.

Keywords: antioxidant defense; environmental pollution; organic acid exudation; programmed cell death; toxic metals; vacuolar processing enzymes.

Figure 1

Illustration of soil acidification’s impact on Al chemistry, highlighting its transformation into various inorganic forms. Al reactivity varies with solubility, heavily influenced by ionic changes. Different Al species are formed based on acidic pH levels, with Al ions (Al³⁺) being the most predominant in acidic conditions, forming stable complexes with sulfate ions (SO₄²⁻), hydroxide (OH⁻), phosphate ions (PO₄²⁻), and silicon (Si). As pH increases, aluminum toxicity diminishes, leading to diverse complexes like aluminum hydroxide ions [Al(OH)₃, [Al(OH)⁴]⁻, Al(H₂O)₆³⁺] and other insoluble hydroxides. Al³⁺ actively enters plant roots in environments with a pH lower than 5. At neutral pH (~7), Al(OH)₃ forms, characterized by higher insolubility and non-toxicity. In environments with a pH greater than 7, aluminate [Al(OH)⁴]⁻ or aluminate anion species occur, often complexing with other molecular species such as AlO₄Al₁₂(OH)₂₄(H₂O)₁₂⁷⁺.

Figure 2

Integrated approach for ROS-mediated cellular tolerance of plants to Al toxicity. Al shares a common path for organic acid transporters (OA: Al³⁺) where the ions diffuse inside the cytosol and interact with the mitochondrial oxidative cycle. Malate dehydrogenase (MDH) and succinate dehydrogenase (SDH) are the major enzymatic sources where nicotinamide adenine dinucleotide [NAD(H) + H⁺] contributes electrons from O₂ into superoxide anions (O₂^•−) and hydrogen peroxide (H₂O₂). In sensitive cultivars, H₂O₂ leads the formation of hydroxide ions (OH⁻) with the Fenton reaction. On the other hand, the nucleus is activated in nuclear membrane oxidation, which also produces free radicals and the induction of other genes: angiotensin II receptor type 1, nitrate transporter 1 (ATR1, NRT1, etc.). Al-induced release of cytochrome c inhibits caspase-like activity, forwarding cell apoptosis. Chloroplasts’ reactions in another form can also induce ROS formation through the introduction of ethylene-dependent gravitropism-deficient and yellow-green light 3 (EGY3)-like metalloproteases that are efficient in the production of H₂O₂, which is retrograded in downstream signaling. The EGY3 can also induce malate transporters, where Al³⁺ can invade PSI. The latter is induced to develop O₂^•−/OH⁻-like free radicals and are engaged in chloroplast membrane oxidation. Al³⁺ can also induce a chain of oxidative reactions where nucleotides are released freely by the action of xanthine oxidase-like activities.

Figure 3

Depiction of NH₄⁺ and NO₃⁻ absorption by Al at root–soil interfaces. NH₄⁺ lowers the rhizospheric pH, increasing the inhibition of metal uptake in plant roots due to competitive inhibition between Al³⁺ and H⁺. Conversely, rhizospheric pH becomes more alkaline with NO₃⁺ accumulation, aiding in the desorption of metals into the rhizosphere but enhancing their transport into roots. Nitrate addition increases the negative electrical potential on the root surface, facilitating the conversion of NH₄⁺ to NO₃⁻. Excess NH₄⁺/H⁺ can displace soluble NO₃⁻ in roots. In sensitive cultivars, NH₄⁺ can influence the binding of ataxia telangiectasia mutated (ATM) and ataxia telangiectasia mutated rad3-related (ATR) with suppressor of gamma response 1 (SOG1) for DNA damage recognition, leading to arrested cell growth in roots under high Al stress. The caption also references key enzymes and transporters involved in nitrogen metabolism: nitrite reductase (NiR), nitrate reductase (NR), glutamine synthase (GS), glutamate dehydrogenase (GDH), glutamine oxoglutarate aminotransferase (GOGAT), nitrate transporter 1/peptide transporter family (NPF), and nitrate transporter 2 family (NRT2).

Figure 4

Illustration of Al tolerance mechanisms in plants through bio-exclusion during stress. The plant’s response to Al stress includes the formation of Al–organic acid (* oxaloacetate and * citrate as predominat residues) complexes, leading to increased alkalization of the root surface. This process involves the induction of Al-malate transporters (* ALMT), activation of proton ATPases, and alterations in cell wall polysaccharide composition. These adaptations aim to minimize Al accumulation within cells, thereby mitigating oxidative damages through enhanced antioxidation pathways.

Figure 5

Depicting the genotoxic effects of Al through various intermediate gene expressions that individually or synergistically influence cellular phenomena. Initially, Al³⁺ stimulates ATP production, while simultaneously downregulating the expression of other electron transport carriers, leading to the dismutation of oxygen into free radical ROS. This ROS production triggers the tonoplast membrane, where Ca²⁺ activates mitochondrial permeability transition (MPT) channels. Concurrently, vacuole-mediated cell death is facilitated by the overexpression of vacuole-localized cysteine protease genes like vacuolar processing enzyme genes (VPE1, VPE1b, VPE2, VPE3), releasing Al from the vacuole into the cytosol. The over-activation of MPT channels disrupts the proton motive force (∆ψ_m) and causes spillage of cytochrome c oxidase, underlying the oxidative damage. The TCA cycle is activated, triggering anaplerotic reactions and inducing genes for malate synthase, citrate synthase, and oxaloacetate decarboxylase. Mitochondrial membrane leakage, linked to the overexpression of mitochondrial membrane permeability transition pore (MPTP) proteins and increased protease activity, also contributes to this process. Collectively, these events culminate in programmed cell death (PCD) of the roots, completing the cycle of Al toxicity.

Figure 6

A hypothetical model for control of organic acid (citrate) exudation in roots against Al ion (Al³⁺) toxicity. At the nuclear level, activation of SENSITIVE TO PROTON RHIXOTOXICITY 1 (STOP1) initiates the signaling pathway, which otherwise activates multidrug and toxic compound extrusion 1, Arabidopsis thaliana aluminum activated malate transporter 1, and amylotrophic lateral sclerosis 3 (AIMTE, MATE, ALS3) genes. STOP1 also upregulates the expression of RNA export 1 (RAE1), which, in feedback regulation, reduces STOP1 through degradation and ubiquitination. Signal transduction and activation of RNA 1 and 2 (STAR1, STAR2) otherwise induce UDP glucose-like residues, which conjugate with Al for extracellular detoxification. Transcription factors like Oryza sativa wrinkled transcription factor (OsWRKY22) form dimers with ADP-ribosyltransferase 1 (ART1) and collectively induce citrate biosynthesizing genes. Expressed proteins from the Nramp family (Nrat1) on the cellular membrane engulf Al³⁺ within the apoplastic space for chelation.

Figure 7

The involvement and crosstalk of plant growth substances against Al sensitivity in plants. Growth hormones like Aux, GA, ABA, CK, JA, and ET induce several cellular processes in roots of plants exposed to Al hyper-accumulation. Both external and internal detoxification by exclusion, sequestering, and chelation reactions are important under hormonal influence. Reduction of H⁺ by inhibition of H⁺/ATPase activity is important to downregulate the acidification of apoplasts of roots to reduce Al ions (Al³⁺). ET induces auxin accumulation as well as auxin transportation by pin formed 2 (PIN2)-mediated polar transport that results in root growth inhibition. Acidification of cell wall by organic acids (malate, citrate, oxalate) is important for ligand formation with metal. ABA and ET have synergistic actions with negative regulation, where RBOH and short-term response, respectively, are important. ABA can also induce ROS biosynthesis, which directly influences Al tolerance genes. Other substances like JA and CK are distantly related to Al tolerance by overexpression of coronatine insensitive 1 and myeloblastosis viral oncogene homologue 2 (COI1, MYC2) and direct inhibition of root growth.