ZmMATE6 from maize encodes a citrate transporter that enhances aluminum tolerance in transgenic Arabidopsis thaliana

Du, Hanmei; Ryan, Peter R.; Lee, Chan; Li, Hongjie; Hu, Wanpeng; Yan, Weina; Huang, Ying; He, Wei; Luo, Bowen; Zhang, Xiao; Zhou, Shufeng; Zhang, Suzhi

doi:10.1016/j.plantsci.2021.111016

Cited by 18 publications

(9 citation statements)

References 63 publications

(54 reference statements)

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“…Since Lotus japonicus was not included in our study, we are uncertain whether the nodule-specific LjMATE1 (a member of IIID), which assists the translocation of iron from the root to nodules ( Takanashi et al, 2013 ), is retained in conserved synteny blocks. Recently, ZmMATE6 was identified as contributing to aluminum tolerance through citrate transport ( Du H. et al, 2021 ). ZmMATE6 was a member of the IIIB subgroup located in the Poaceae-specific synteny community (i.e., IIIB2), which had no connection with other communities ( Figure 6 ).…”

Section: Discussionmentioning

confidence: 99%

A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants

et al. 2022

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Multidrug and toxic compound extrusion (MATE) transporters comprise a multigene family that mediates multiple functions in plants through the efflux of diverse substrates including organic molecules, specialized metabolites, hormones, and xenobiotics. MATE classification based on genome-wide studies remains ambiguous, likely due to a lack of large-scale phylogenomic studies and/or reference sequence datasets. To resolve this, we established a phylogeny of the plant MATE gene family using a comprehensive kingdom-wide phylogenomic analysis of 74 diverse plant species. We identified more than 4,000 MATEs, which were classified into 14 subgroups based on a systematic bioinformatics pipeline using USEARCH, blast+ and synteny network tools. Our classification was performed using a four-step process, whereby MATEs sharing ≥ 60% protein sequence identity with a ≤ 1E-05 threshold at different sequence lengths (either full-length, ≥ 60% length, or ≥ 150 amino acids) or retaining in the similar synteny blocks were assigned to the same subgroup. In this way, we assigned subgroups to 95.8% of the identified MATEs, which we substantiated using synteny network clustering analysis. The subgroups were clustered under four major phylogenetic groups and named according to their clockwise appearance within each group. We then generated a reference sequence dataset, the usefulness of which was demonstrated in the classification of MATEs in additional species not included in the original analysis. Approximately 74% of the plant MATEs exhibited synteny relationships with angiosperm-wide or lineage-, order/family-, and species-specific conservation. Most subgroups evolved independently, and their distinct evolutionary trends were likely associated with the development of functional novelties or the maintenance of conserved functions. Together with the systematic classification and synteny network profiling analyses, we identified all the major evolutionary events experienced by the MATE gene family in plants. We believe that our findings and the reference dataset provide a valuable resource to guide future functional studies aiming to explore the key roles of MATEs in different aspects of plant physiology. Our classification framework can also be readily extendable to other (super) families.

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Section: Discussionmentioning

confidence: 99%

A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants

et al. 2022

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“…The metal treatments, time-course analysis, and manipulation of Al concentrations were performed as described previously [ 51 ]. The roots and/or the shoots from all the treated seedlings were immediately frozen in liquid nitrogen, and stored at −80 °C for RNA extraction.…”

Section: Methodsmentioning

confidence: 99%

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

Lee

Jin

et al. 2022

IJMS

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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.

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“…Citrate and malate are the main types of OA secreted in many plant species. For example, crops such as rice [20], maize [21], and pea [22] have been shown to release citrate in response to Al stress. Malate secretion has been identified in plants like rape [23] and sorghum [24].…”

Section: Of 17mentioning

confidence: 99%

“…In contrast, oxalic acid secretion has been detected in buckwheat and taro, with no known transporters identified for its secretion in response to Al toxicity. Numerous experiments have pinpointed the involvement of families such as multidrug and toxic compound extrusion (MATE), responsible for encoding citrate transporters on the plasma membrane, and Al-activated malate transporter (ALMT), an anion channel activated by Al 3+ on the plasma membrane, in facilitating the release of the respective OAs from plant root cells into the rhizosphere under Al stress [20][21][22][23][24][25][26][27]. However, transporters for oxalic acid secretion in response to Al toxicity remain unidentified.…”

Section: Of 17mentioning

confidence: 99%

Physiological and Transcriptomic Analysis Reveals That Melatonin Alleviates Aluminum Toxicity in Alfalfa (Medicago sativa L.)

Liu,

Cheng,

Wang

et al. 2023

IJMS

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Aluminum (Al) toxicity is the most common factor limiting the growth of alfalfa in acidic soil conditions. Melatonin (MT), a significant pleiotropic molecule present in both plants and animals, has shown promise in mitigating Al toxicity in various plant species. This study aims to elucidate the underlying mechanism by which melatonin alleviates Al toxicity in alfalfa through a combined physiological and transcriptomic analysis. The results reveal that the addition of 5 μM melatonin significantly increased alfalfa root length by 48% and fresh weight by 45.4% compared to aluminum treatment alone. Moreover, the 5 μM melatonin application partially restored the enlarged and irregular cell shape induced by aluminum treatment, resulting in a relatively compact arrangement of alfalfa root cells. Moreover, MT application reduces Al accumulation in alfalfa roots and shoots by 28.6% and 27.6%, respectively. Additionally, MT plays a crucial role in scavenging Al-induced excess H2O2 by enhancing the activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), consequently reducing malondialdehyde (MDA) levels. More interestingly, the RNA-seq results reveal that MT application significantly upregulates the expression of xyloglucan endotransglucosylase/hydrolase (XTH) and carbon metabolism-related genes, including those involved in the glycolysis process, as well as sucrose and starch metabolism, suggesting that MT application may mitigate Al toxicity by facilitating the binding of Al to the cell walls, thereby reducing intracellular Al accumulation, and improving respiration and the content of sucrose and trehalose. Taken together, our study demonstrates that MT alleviates Al toxicity in alfalfa by reducing Al accumulation and restoring redox homeostasis. These RNA-seq results suggest that the alleviation of Al toxicity by MT may occur through its influence on cell wall composition and carbon metabolism. This research advances our understanding of the mechanisms underlying MT’s effectiveness in mitigating Al toxicity, providing a clear direction for our future investigations into the underlying mechanisms by which MT alleviates Al toxicity in alfalfa.

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ZmMATE6 from maize encodes a citrate transporter that enhances aluminum tolerance in transgenic Arabidopsis thaliana

Cited by 18 publications

References 63 publications

A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants

A Systematic Phylogenomic Classification of the Multidrug and Toxic Compound Extrusion Transporter Gene Family in Plants

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

Physiological and Transcriptomic Analysis Reveals That Melatonin Alleviates Aluminum Toxicity in Alfalfa (Medicago sativa L.)

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