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GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana.

ABSTRACT: BACKGROUND:Multidrug and toxic compound extrusion (MATE) transporters, which exist widely in plants, function as crucial regulators in plant resistance to aluminum (Al) toxicity by inducing citrate efflux. However, the functions of most MATE family members in soybean (Glycine soja) remain to be elucidated. RESULTS:Expression pattern analysis showed that GsMATE was constitutively expressed in different soybean organs, with the highest level in root compared with those in stem, leaf and cotyledon. In addition, Al stress induced expression of GsMATE in soybean. Temporal analysis indicated that GsMATE expression was greatly enhanced by increasing concentrations of aluminum [Al3+] after short exposure, reaching the high levels detected in the BW69 (Al-resistant) and the JW81 (Al-sensitive) lines of Glycine soja of wild soybean at 6 h and 8 h, respectively. Furthermore, transient GsMATE expression in Arabidopsis protoplasts showed that GsMATE protein localized to the plasma membrane. Overexpression of GsMATE on an Arabidopsis columbia-0 (Col-0) background resulted in increased Al tolerance in transgenic plants. Analysis of hematoxylin staining showed that the roots of GsMATE transgenic lines were stained less intensely than those of the wild-type exposured to the same AlCl3 concentrations. Therefore, GsMATE enhanced the resistance of transgenic plants to Al toxicity by reducing Al accumulation in Arabidopsis roots. CONCLUSIONS:In summary, our results indicate that GsMATE is responsive to aluminum stress and may participate in the regulation of sensitivity to Al toxicity in Arabidopsis. In addition, the GsMATE protein is an Al-induced citrate transporter of the MATE family and exerts an essential role in Al tolerance in Glycine soja.

SUBMITTER: Ma Q

PROVIDER: S-EPMC6162897 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana.

Ma Qibin Q Yi Rong R Li Lu L Liang Zhongyi Z Zeng Tingting T Zhang Yu Y Huang He H Zhang Xiao X Yin Xiangli X Cai Zhandong Z Mu Yinghui Y Cheng Yanbo Y Zeng Qiaoying Q Li Xiuping X Nian Hai H

BMC plant biology 20180929 1

<h4>Background</h4>Multidrug and toxic compound extrusion (MATE) transporters, which exist widely in plants, function as crucial regulators in plant resistance to aluminum (Al) toxicity by inducing citrate efflux. However, the functions of most MATE family members in soybean (Glycine soja) remain to be elucidated.<h4>Results</h4>Expression pattern analysis showed that GsMATE was constitutively expressed in different soybean organs, with the highest level in root compared with those in stem, leaf ...[more]

PMID: 30268093

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Project description:Aluminum (Al) toxicity poses a significant challenge for the yield improvement of chickpea, which is an economically important legume crop with high nutritional value in human diets. The genetic basis of Al-tolerance in chickpea remains unclear. Here, we assessed the Al-tolerance of 8 wild Cicer and one cultivated chickpea (PBA Pistol) accessions by measuring the root elongation in solution culture under control (0 μM Al3+) and Al treatments (15, 30 μM Al3+). Compared to PBA Pistol, the wild Cicer accessions displayed both tolerant and sensitive phenotypes, supporting wild Cicer as a potential genetic pool for Al-tolerance improvement. To identify potential genes related to Al-tolerance in chickpea, genome-wide screening of multidrug and toxic compound extrusion (MATE) encoding genes was performed. Fifty-six MATE genes were identified in total, which can be divided into 4 major phylogenetic groups. Four chickpea MATE genes (CaMATE1-4) were clustered with the previously characterized citrate transporters MtMATE66 and MtMATE69 in Medicago truncatula. Transcriptome data showed that CaMATE1-4 have diverse expression profiles, with CaMATE2 being root-specific. qRT-PCR analyses confirmed that CaMATE2 and CaMATE4 were highly expressed in root tips and were up-regulated upon Al treatment in all chickpea lines. Further measurement of carboxylic acids showed that malonic acid, instead of malate or citrate, is the major extruded acid by Cicer spp. root. Protein structural modeling analyses revealed that CaMATE2 has a divergent substrate-binding cavity from Arabidopsis AtFRD3, which may explain the different acid-secretion profile for chickpea. Pangenome survey showed that CaMATE1-4 have much higher genetic diversity in wild Cicer than that in cultivated chickpea. This first identification of CaMATE2 and CaMATE4 responsive to Al3+ treatment in Cicer paves the way for future functional characterization of MATE genes in Cicer spp., and to facilitate future design of gene-specific markers for Al-tolerant line selection in chickpea breeding programs.

Project description: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.

Dataset Information

GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana.

Publications

GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana.

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