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21 August 2024

Systematic Investigation of Aluminum Stress-Related Genes and Their Critical Roles in Plants

,
and
1
College of Life Science, Henan Normal University, Xinxiang 453007, China
2
Xinxiang Academy of Agricultural Sciences, Xinxiang 453000, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci.2024, 25(16), 9045;https://doi.org/10.3390/ijms25169045
This article belongs to the Section Molecular Plant Sciences
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Abstract

Aluminum (Al) stress is a dominant obstacle for plant growth in acidic soil, which accounts for approximately 40–50% of the world’s potential arable land. The identification and characterization of Al stress response (Al-SR) genes in Arabidopsis, rice, and other plants have deepened our understanding of Al’s molecular mechanisms. However, as a crop sensitive to acidic soil, only eight Al-SR genes have been identified and functionally characterized in maize. In this review, we summarize the Al-SR genes in plants, including their classifications, subcellular localizations, expression organs, functions, and primarily molecular regulatory networks. Moreover, we predict 166 putative Al-SR genes in maize based on orthologue analyses, facilitating a comprehensive understanding of the impact of Al stress on maize growth and development. Finally, we highlight the potential applications of alleviating Al toxicity in crop production. This review deepens our understanding of the Al response in plants and provides a blueprint for alleviating Al toxicity in crop production.

1. Introduction

Acidic soil is globally widespread, encompassing approximately 40–50% of the world’s potentially arable lands, and it constrains crop production worldwide significantly [1,2]. As the most abundant metal element in the earth’s crust, aluminum (Al) mainly exists as insoluble aluminosilicates or Al oxides, which are non-toxic to plant growth, while it exhibits high toxicity toward plants of Al3+ in acidic environments (pH < 5.5) [3]. The predominant obstacle to plant growth in acidic soil is commonly attributed to Al toxicity [4]. Thus, the exploration of the toxic mechanism of Al stress and the characterization of the Al stress response (Al-SR) genes in plants will facilitate potential applications for alleviating Al stress, as well as the crop breeding of and genetic improvement in Al-tolerant varieties.
The effects of Al toxicity on plants are irreversible, even in the presence of a micromolar concentration of Al in the soil [4]. Al toxicity is associated with the interaction between Al and the cell walls, plasma membranes, and symplasms of apical root cells in plants [5]. The primary manifestation of Al stress on plants is the suppression of root elongation, subsequently leading to the restricted uptake of water and nutrients [6,7]. For self-protection, plants have evolved strategies to cope with Al stress, among which internal tolerance and external exclusion are widely considered the primary mechanisms [3,8]. So far, hundreds of Al-SR genes have been cloned in plants, represented by AtSTOP1 in Arabidopsis and OsART1 in rice [9,10,11,12,13,14,15,16,17]. However, as a crop sensitive to acidic soil [18], only a small number of Al-SR genes have been identified and functionally characterized in maize.
Here, we focus on the progress and perspective of Al-SR genes and their roles in the Al response in plants. Based on the cloned Al-SR genes, we propose the regulation mainly of networks of the Al response, utilizing AtSTOP1 and OsART1 as the key regulators in Arabidopsis and rice, respectively. Furthermore, we predict 166 putative Al-SR genes in maize based on orthologue and RNA-seq analyses. Moreover, we outline the potential strategies for alleviating Al stress in crop production, including crop rotation, the exogenous application of other elements, and molecular breeding.

2. Overview of Al-SR Genes in Plants

In Arabidopsis (76), rice (28), wheat (13), maize (8), and sorghum (5), at least 130 Al-SR genes have been cloned; however, compared to Arabidopsis and rice, fewer Al-SR genes have been functionally identified in maize (Figure 1A). To summarize the molecular mechanisms of the cloned Al-SR genes comprehensively, we classified these Al-SR genes into transporters, transcription factors, kinases/phosphatase, and those related to sugar metabolism, hormones, ROS metabolism, and other processes based on their functions, which contain 31, 30, 21, 8, 11, 10, and 19 genes, respectively (Figure 1B).
Figure 1. Identified aluminum stress-related genes, their subcellular localizations, and their roles in plants, and the expression analysis of the cloned maize aluminum stress-related genes in different developmental stages of maize roots. (A) The cloned aluminum stress-related genes in Arabidopsis, rice, maize, wheat, and sorghum. (B) Classification of the cloned aluminum stress-related genes into transporters, transcription factors, kinases/phosphatase, and those related to sugar metabolism, hormones, ROS metabolism, and other processes. (C) The protein subcellular localizations of the aluminum stress-related genes in plants.
Among all the reported Al-SR genes, 90 were investigated for their protein subcellular localizations (Figure 1C). These proteins were localized in several organelles, such as the vacuole membrane/channel, vesicle membrane, plasma membrane, nucleus, etc. Among them, most proteins were localized in the nucleus (29), but fewer were localized in the Golgi (only one) (Figure 1C). These results indicate that the response to Al stress may take place in various organelles in plants.
Moreover, twelve Al-SR gene-encoding proteins were found to be localized in several organelles (e.g., the nucleus-, cytoplasm-, and endoplasmic reticulum-localized AtEIN2) (Figure 1C) [19]. SbSTAR1 [20,21], ZmMATE6 [22], OsMGT1 [23], OsASR1/5 [24], ZmALDH [25], AtNPR1 [19], SbGLU1 [20,21,26], and AtPP2C.D5/6/7 [27,28] were localized in the cytoplasm and nucleus, indicating that these genes may function in multiple organelles for Al stress.
Collectively, the protein subcellular localization information of Al-SR genes is largely consistent with their functions in the response to Al stress. Nevertheless, the detailed molecular mechanism of the response to Al stress is largely unclear and needs to be further investigated.

3. Al-SR Genes and Their Essential Roles in Plants

3.1. Transporters

Transporters are ubiquitous in all living organisms and constitute an integral component of the biological system [29]. In plants, there exists a diverse array of transporters, including ATP-binding cassette (ABC) transporters, multidrug and toxic compound extrusion (MATE) transporters, natural resistance-associated macrophage proteins (NRAMP), and so on [30].
Among the 31 Al-SR transporters, 8 ABC transporters have been identified (Table 1 and Table S1). For example, AtSTAR1, the ortholog of OsSTAR1 and SbSTAR1, interacts with AtALS3. These are all involved in the basic detoxification of Al [20,21,31,32]. OsSTAR2 interacts with OsSTAR1, forming heterodimers in response to Al stress in rice [32]. AtALS1 and OsALS1 interact to sequestrate Al into the vacuoles [33,34]. ZmPGP1 is associated with reducing auxin accumulation in the root tips to regulate Al stress in maize [35]. Nine MATE transporters, such as AtMATE, increase Al resistance and improve carbon-use efficiency for Al resistance and AtFRDL3-mediated efflux of citrate into the root vasculature in Arabidopsis [36,37,38,39]. OsFRDL2 is involved in the Al-induced secretion of citrate, and OsFRDL4 responds to aluminum tolerance by enhancing its expression in rice [40,41,42]. SbMATE mediates Al-activated citrate efflux from the root apices in sorghum [20,43,44,45,46,47,48,49,50,51]. ZmMATE1 and ZmMATE2 are involved in citrate efflux in oocytes, as demonstrated in experiments on maize [52,53]. ZmMATE6 enhances Al tolerance in transgenic Arabidopsis [22]. TaMATE2 is related to Al tolerance in bread wheat [54]. ZmMATE1 is the ortholog of AtFRDL3, OsFRDL2, and TaMATE2, which play similar roles in Al-SR. Malate can regulate plant physiology, thereby facilitating the alleviation of Al-induced stress. There are five identified malate transporters, including AtALMT1 [36,37,55,56,57,58], AtALMT9 [59,60,61], AtALMT12 [62,63], OsALMT4 [63,64], and TaALMT1 [57,65]. These participate in malate transport in response to Al stress in plants. In addition, there are four metal transporters, including OsNrat1 [66,67,68], OsMGT1 [23], SbNrat1 [69], and ZmNRAMP4 [70]; two auxin transporters, including OsPIN2 [71,72] and OsAUX3 [73]; one oxalate transporter, called AtOT [74]; and two aquaporins, including AtNIP1;2 [75,76] and OsNIP1;2 [77]. These are closely correlated to the response to Al stress. Taken together, transporters play vital roles in material transport and are involved in Al-SR in plants.
Table 1. Functional classifications of the reported Al-SR genes in Arabidopsis, rice, wheat, maize, and sorghum.

3.2. Transcription Factor

The maize genome contains a total of 2216 protein-coding genes that have been predicted to be transcription factor (TF) genes [145]. Up to now, at least 30 Al-SR TF genes have been cloned in Arabidopsis, rice, sorghum, maize, and wheat (Table 1 and Table S1), including 10 zinc finger TFs of AtSTOP1 [11,12,14,85] and AtSTOP2 [88] in Arabidopsis. OsART1 [9,10,15,16,17,34] and OsART2 [9] in rice, SbSTOP1a/b/c/d [86] and SbZNF1 [48] in sorghum, and TaSTOP1 [87] in wheat. Among them, AtSTOP1 and its orthologs in other plants, including OsART1, and SbSTOP1a/b/c/d, play common roles in Al stress by regulating other functional genes. The six WRKY TFs, including AtWRKY46, work as transcriptional repressors of AtALMT1 [89], and AtWRKY47 is involved Al stress via the regulation of cell wall-modifying genes [90] in Arabidopsis. OsWRKY22 promotes Al tolerance by the activation of OsFRDL4 in rice [42]. SbWRKY1, SbWRKY22, and SbWRKY65 positively regulate Al tolerance in sorghum [20,48]. The two abscisic acid, stress, ripening-induced (ASR) family TFs of OsASR1 and OsASR5 work as complementary transcription factors in regulating Al-responsive genes in rice [24,91,92]. The two HD-Zip TFs of AtHB7and AtHB12 respond to Al stress by regulating root growth in Arabidopsis [93], and one basic-leucine zipper (bZIP) TF of SbHY5 facilitates light-induced aluminum tolerance in sorghum by activating the expression of SbMATE and SbSTOP1s [146]. The two MYB TFs of AtMYB103 positively regulate Al sensitivity by mediating the modulation of the O-acetylation level of cell wall xyloglucan and act upstream of TRICHOME BIREFRINGENCE-LIKE27 in Arabidopsis [96]. OsMYB30 is regulated by OsART1 to response aluminum resistance in cell-wall modification in rice [95]. The two NAC TFs of ANAC017 regulate Al tolerance through the modulation of genes involved in cell-wall modification [97]. AtSOG1 suppresses growth reduction in plants under Al stress [98,99]. The JA signaling regulator of MYC2, a bHLH transcription factor, upregulates the response to Al stress of Arabidopsis root tips [100]. Additionally, another four TFs, including AtLUH [101,102], AtSLK2 [101], AtPIF4 [7], and AtRBR1 [103], are also involved in Al tolerance in plants, indicating that these transcription factors may play core roles in plants under Al stress. However, further analysis is necessary for some TFs to gain a more comprehensive understanding, although the target genes of most TFs have been identified as responsive to Al stress.

3.3. Kinases/Phosphatase

Kinases and phosphatase play pivotal roles in plant stress response [146,147]. Up to now, at least 20 Al-SR kinases/phosphatase genes have been cloned in Arabidopsis, rice, sorghum, maize, wheat, and other plants (Table 1 and Table S1). The cell wall-associated receptor kinase AtWAK1 increases Al tolerance in terms of root growth [104]. The activity of AtCK2 kinase contributes to the development of Al toxicity tolerance, and regulates the DNA damage response (DDR) pathway by phosphorylating SOG1 [105]. The loss functions of AtRAE1, AtRAE2, AtRAE3/AtHPR1, and AtRAH1 reduce Al resistance by acting as an E3 ligase to regulate the stability of the target proteins, such as AtSTOP1 and AtALMT1 [35,106,107,108]. However, the loss function of AtESD4/RAE5 or AtSIZ1 increases the transcriptional-level AtALMT1, thereby enhancing the resistance to Al in atesd4/rae5 or atsiz1 [109,111,148,149]. The AtMEKKK1-MKK1/2-MPK4 cascade plays a crucial role in Al signaling and confers resistance to Al by enhancing AtSTOP1 accumulation through phosphorylation-mediated mechanisms in Arabidopsis [112,150]. OsSAL1, a member of the PP2C.D family, is the ortholog of AtPP2C.D5/D6/D7 in Arabidopsis. Remarkably, both the ossal1 mutant and the atpp2c.d5/d6/d7 triple mutant exhibit more Al resistance compared to the WT, suggesting conserved yet complex roles of these phosphatases in modulating plant stress responses [27,28]. Additionally, OsSAL1 interacts with and dephosphorylates the plasma membrane H+-ATPase OsA7 to exert negative regulation on its function in Al stress [27]. AtATR phosphorylates AtSUV2 in vivo under Al stress [114]. In addition, the expression of certain genes is influenced by Al stress and other stress. For instance, the atpah1/pah2 double mutant exhibits enhanced susceptibility to Al under low-phosphorus conditions [113]. The expression of OsArPK, an Al-related protein kinase gene, is induced in the roots following prolonged exposure to high concentrations of Al [115].

3.4. Sugar Metabolism

The cellular sugar status remains relatively stable under normal growth conditions but is adversely affected by various environmental perturbations [151,152]. In plants, at least eight Al-SR sugar metabolism-related genes have been cloned (Table 1 and Table S1). AtEXPA10 is an Al-inducible expansin gene that is regulated by AtART1 and plays an important role in modulating Al accumulation within root cell walls [116]. The expression of ZmXTH is significantly induced by Al toxicity, and the overexpression of ZmXTH in Arabidopsis enhances the tolerance to Al toxicity by reducing Al accumulation in both the roots and cell walls [117]. AtXTH15 and AtXTH31 are endo-trans-glucosylase-hydrolases and exhibit enhanced Al resistance in their mutants [118,119]. AtTBL27 influences the sensitivity of Arabidopsis to Al by modulating the Al-binding capacity in hemicellulose [96,120]. The identification of AtPME46 revealed its ability to reduce the binding of Al to cell walls, thereby alleviating Al-induced inhibition of root growth through the downregulation of PME enzyme activity [101]. Furthermore, the modified characteristics of hemicellulose contribute to its reduced Al accumulation in the atparvus mutant [121]. The β-1,3-glucanase SbGLU1 reduced callose deposition and increased tolerance to Al toxicity, highlighting the intricate interplay between cell wall components and aluminum stress responses in plants [20,26,122].

3.5. Hormone-Related Genes

Plant hormones occupy a central role in regulating essential aspects of growth, development, and adaptive responses to environmental stress [153]. At least 11 Al-SR hormone-related genes have been cloned in plants (Table 1 and Table S1). For example, AtEIN2 and AtNPR1 are ethylene and salicylic acid signal factors. The loss functions of AtEIN2 and AtNPR1 display more susceptibility to Al stress than WT [19]. The local biosynthesis of auxin regulated by YUCs in the root apex transition zone mediates the inhibition of root growth in response to Al stress [7]. AtTAA1 is specifically upregulated in the root apex TZ in response to Al treatment [7,124]. Additionally, AtCOI1-mediated Al-induced root growth inhibition under Al stress was controlled by ethylene [100]. AtSUR1 and AtSUR2 promote IAA biosynthesis and auxin conjugation, respectively, and the sur1 and sur2 mutants exhibit increased sensitivity to Al stress [118,125,126].

3.6. ROS Metabolism

Reactive oxygen species (ROS) serve as crucial signaling molecules that facilitate prompt cellular responses to various stimuli in plants [154]. The production of ROS is significantly increased in plants under biotic or abiotic stresses, disrupting the homeostasis of -OH, O2-, and H2O2. To maintain the balance of ROS in vivo, some enzymes and low-molecular-weight compounds participate in antioxidant mechanisms in plants, including superoxide dismutases (SODs), catalases (CATs), ascorbate peroxidases (APx), glutathione peroxidases (GPx), ascorbic acid, glutathione, and tocoferol [155]. Up to now, at least 10 Al-SR hormone-related genes have been cloned in Arabidopsis, rice, sorghum, maize, and wheat (Table 1 and Table S1).
In rice, H2O2 accumulation is significantly increased in OsApx1/2-silenced plants and presents higher Al tolerance than WT [127]. The overexpression of AtGR can maintain GSH levels, reinforcing the detoxification functions in plants and providing an efficient approach for enhancing Al tolerance [128]. The expressions of AtGST1 and AtGST11 are activated in response to Al stresses [129]. The AtPrx64 gene increases root growth and mitigates the accumulation of Al and ROS in the roots [130]. AtAOX1a mitigates Al-induced programmed cell death (PCD) by preserving mitochondrial function and enhancing the expression of protective functional genes [131]. ZmAT6 and ZmALDH confer Al tolerance via ROS scavenging and reduce Al accumulation in roots [25,132]. The involvement of AtNADP-ME1 in regulating malate levels in the root apex leads to an elevation in the content of this organic acid [133]. In general, these ROS metabolism genes dynamically respond to aluminum stress by meticulously regulating ROS homeostasis, ensuring plant survival and resilience under adverse conditions.

3.7. Other Processes

Apart from the Al stress-related genes mentioned above, several additional genes have been reported to regulate Al stress response in plants (Table 1 and Table S1). Examples include AtGRP3, which encodes a glycine-rich protein [134], AtVHA-a2/a3, which encodes a subunit of the vacuolar H+-ATPase (V-ATPase) [8], AtSUV2, a putative plant ATRIP homologue [114], and AtALT1, a thioesterase [78]. These negatively control Al stress in plants. AtCBL1, a calcineurin B-like calcium sensor [135], AtALS7, a ribosomal biogenesis factor [136], AtSWA2, a CCAAT-box binding factor [136], AtRAD51, a DNA repair family protein gene [103], AtCYCB1, a cyclin protein gene [103], AtTANMEI/ALT2, a WD40 protein gene [138], and AtPGIP1, a P450-dependent monooxygenase gene [139], positively regulate Al stress in Arabidopsis. OsGERLP [137], Os4CL3/4/5 [7,95,140,141,142], and OsCS1 [143] positively regulate Al stress in rice. Additionally, TaWali1 and TaWali5 positively regulate Al stress in wheat [144]. In a word, the response to Al stress is an intricate process, necessitating the coordination of multiple substances and genes.

4. The Primary Molecular Regulatory Network for the Cloned Al Stress-Related Genes in Plants

Plant response to Al stress is a fairly complicated process. Here, a molecular regulatory network for the cloned Al-SR genes in plants, which mainly include similar STOP1-related pathways in Arabidopsis and ART1-related pathways in rice, is summarized and updated, considering the functional properties (Figure 2).
Figure 2. The primary signaling pathways of the cloned aluminum stress-related genes involved in plants.

4.1. STOP1-Related Pathway in Arabidopsis

STOP1 (SENSITIVE TO PROTEIN RHIZOTOXICITY 1) is a zinc finger transcription factor that plays important roles in Al tolerance [11,12,14,54,85,86]. In Arabidopsis, AtSTOP1 plays a central role in Al tolerance because of its ability to connect upstream kinases and downstream target genes (Figure 2). The AtMEKKK1-AtMKK1/2-AtMPK4 cascade exerts a positive regulatory effect on AtSTOP1 phosphorylation and stability. The phosphorylation of AtSTOP1 diminishes its interaction with the F-box protein AtRAE1 [112]. AtRAE1 interacts with and facilitates the ubiquitin-26S proteasome pathway-mediated degradation of AtSTOP1, while Al stress induces the accumulation of AtSTOP1 [6]. Meanwhile, AtRAH1, AtSIZ1, and AtESD4/RAE5 interact with AtSTOP1 and regulate AtSTOP1 SUMOylation under Al stress [106,109,149]. Additionally, AtRAE3 regulates AtSTOP1 mRNA exports under Al stress [107]. AtSTOP2 works as a physiologically minor isoform of AtSTOP1, and AtSTOP2 is directly regulated by AtSTOP1 [88]. In addition, AtSTOP1 regulates malate transporter gene AtALMT1 [58], MATE transporter gene AtMATE [36,37], aquaporin gene AtNIP1;2 [75,76], P450-dependent monooxygenase gene AtPGIP1 [139], and ABC transporter gene AtALS1, and AtALS1 interacts with AtSTAR1 to form heterodimers [31].

4.2. ART1-Related Pathway in Rice

ART1 (Al resistance transcription factor 1), a C2H2-type zinc finger transcription factor, which is the ortholog of AtSTOP1, regulates the gene expressions associated with Al tolerance in rice [16]. OsART1 confers Al resistance by repressing the modification of cell wall properties regulated by OsMYB30, thereby enhancing the effect of Al resistance [95], and in turn repressing Os4CL5-dependent 4-coumaric acid accumulation, which is similar to the functions of Os4CL3 and Os4CL4 [7,140,141,142]. The MATE family protein genes of OsFRDL2 and OsFRDL4 are directly regulated by OsART1 and involved in the Al-induced secretion of citrate [40,41,42,80]. OsART1 directly regulates metal transporter gene OsNRAT1, and OsNRAT1 serves as the initial step in sequestering Al3+ into the vacuoles, thereby alleviating Al toxicity [66,67,68]. OsEXPA10, an Al-inducible expansion gene, is regulated by OsART1 and promotes Al accumulation in the root cell of rice [116]. Similar to AtSTOP1, OsART1 regulates OsSTAR1, which is orthologous with AtSTAR1. OsSTAR1 forms heterodimers with OsSTAR2 at tonoplasts [32]. In general, AtSTOP1 and OsART1 play pivotal roles in the response to Al stress in Arabidopsis and rice, making the STOP1/ART1-related pathways valuable models for studying Al stress in maize and other plant species.

5. Prediction of Putative Al Stress-Related Genes in Maize

Compared to Arabidopsis and rice, only eight maize Al stress-related genes have been identified in maize. Among them, five cloned Al stress-related genes encode transporters. For example, ZmPGP1, an ABCB transporter, mediated auxin efflux in an action, regulated Al stress, and was associated with reduced auxin accumulation in root tips [35,156]. ZmMATE1, ZmMATE2, and ZmMATE6 belong to the MATE family. Maize is Al-tolerant with a higher ZmMATE1 copy number; however, ZmMATE2 is involved in a novel Al-tolerance mechanism [52,53,79]. ZmMATE6 displays a greater Al-activated release of citrate from the roots and is significantly resistant to Al toxicity [22]. ZmNRAMP4 is a metal transporter that enhances Al tolerance via the cytoplasmic sequestration of Al in maize [70]. Translocating the expression of ZmXTH, a xyloglucan endotransglucosylase/hydrolase gene, enhances tolerance to Al toxicity by reducing the Al accumulation in the roots and cell wall in Arabidopsis [117]. Two Al stress-related genes belong to ROS metabolism genes. For example, ZmAT6 confers Al tolerance via ROS scavenging [132]. ZmALDH participates in Al-induced oxidative stress and Al accumulation in roots [25]. To discover more Al stress-related genes in maize, putative Al stress-related genes in maize are predicted based on ortholog analysis and maize root RNA-seq analyses. Here, a total of 166 putative maize genes associated with Al stress were identified by analyzing the orthologs of other plants based on the Ensembl Plants website (https://plants.ensembl.org/index.html, accessed on 26 February 2024). Those 166 putative Al stress-related genes in maize are distributed among the ten chromosomes of maize with variable numbers, from twelve on chromosome 6 and chromosome 10 to twenty-eight on chromosome 2 (Figure 3, Figure S1, and Table S1). The in silico mapping information can facilitate gene cloning and evolutionary studies of the Al stress-related genes in maize.
Figure 3. The precise chromosomal locations of the 166 predicted aluminum stress-related genes in the maize genome.

6. Potential Applications to Alleviate Al Stress in Crop Production

The toxicity of Al poses a global challenge in acidic soils (pH < 5.5), leading to diminished crop growth and reduced productivity [1]. Previous studies have shown that Al have pleiotropic functions of beneficial or toxic effect to plants and other organisms, depending on factors such as the metal concentration, the chemical form of Al, the growth conditions, and the plant species [157]. Consequently, alleviating Al stress and even harnessing Al resources efficiently is imperative for sustainable agricultural production. To mitigate Al stress, we propose potential applications to alleviate Al stress in crop production based on the current research (Figure 4).
Figure 4. Potential applications to alleviate aluminum stress in crop production.
In previous studies, crop rotation has been considered as an effective way to alleviate heavy-metal stress [158]. Implementing a crop rotation strategy that involves the selection of low Al-accumulating cultivars, along with effective water and manure management practices, to achieve the purpose of soil improvement, can potentially serve as an efficacious approach to mitigate Al-induced damage (Figure 4). Additionally, applying other exogenous elements in crop growth is also a viable method (Figure 4). For example, the alleviation of Al toxicity by H2S is associated with an increase in ATPase activity, as well as a reduction in Al uptake and oxidative stress in barley at the seedling stage [159]. The uptake of NH4+ leads to a decrease in pH, which in turn alters the properties of the cell wall and reduces the Al accumulation by NH4+-induced mechanisms, rather than through direct competition for binding sites between Al3+ and NH4+ [84]. The application of exogenous Si treatment results in the formation of hydroxy Al silicates within the apoplast of the root apex, thereby effectively detoxifying Al [160]. For breeders, the issue of crop Al toxic needs to be solved from the original source, such as the development of new Al-tolerant varieties by using molecular breeding techniques (Figure 4). In summary, it is imperative to explore more efficient and convenient approaches in order to alleviate the detrimental effects of Al stress on crop production, aiming for enhanced quality and yield.

7. Conclusions and Perspectives

Al stress is a significant hazard in plant growth in low-pH environments, and thus, it affects organ development and ultimately reduces the grain yield in crops [161]. Here, we systematically investigated the Al-SR genes and their roles in controlling the response of plants to Al. To date, most of the cloned Al-SR genes have been identified in Arabidopsis and rice, with a number of genes reported in maize (only eight). Here, we predicted 166 maize orthologs of Al-SR genes in other plants and determined their precise chromosome localizations in the maize genome (Figure 3). This research provides a batch of targets genes to study the molecular mechanisms and genetic improvement of the Al response of maize by using CRISPR/Cas9 mutagenesis or other biotechnologies. In acidic soil conditions, even trace amounts of Al can elicit severe and irreversible toxicity symptoms in higher plants, drastically hindering water and nutrient uptake, and thereby imposing considerable stress on plant growth [4]. Therefore, we provide some potentially effective applications for mitigating Al stress in crop production, aiming to cultivate healthy and high-yielding crops even under the challenging conditions imposed by Al toxicity. Therefore, the investigation of the functional mechanisms of Al-SR genes and the exploration of new methods to mitigate Al stress are formidable tasks to enhance the crop grain yield. These tasks should be given priority considerations in future work.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijms25169045/s1.

Author Contributions

Conceptualization, W.L. and C.F.; validation, C.F., J.W. and W.L.; formal analysis, C.F., J.W. and W.L.; resources, C.F. and J.W. writing—original draft preparation, C.F. and J.W.; writing—review and editing, W.L. and C.F.; visualization, W.L. and C.F.; supervision, W.L.; project administration, W.L. and C.F.; funding acquisition, W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Key R&D and Promotion Projects in Henan Province (242102111164), the Henan Science & Technology Research and Development Plan Joint Fund (222301420106), the Zhongyuan Scholar Workstation of Henan Province (244400510009), and the Observation and Research Field Station of Taihang Mountain Forest Ecosystems of Henan Province, Xinxiang 453007, Henan, China.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data are shown in the main manuscript and in the Supplementary Materials.

Conflicts of Interest

The authors declare no conflicts of interest.

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