- Research article
- Open Access
Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean
© Liu et al. 2016
Received: 10 January 2016
Accepted: 29 February 2016
Published: 11 March 2016
Multidrug and toxic compound extrusion (MATE) family is an important group of the multidrug efflux transporters that extrude organic compounds, transporting a broad range of substrates such as organic acids, plant hormones and secondary metabolites. However, genome-wide analysis of MATE family in plant species is limited and no such studies have been reported in soybean.
A total of 117 genes encoding MATE transporters were identified from the whole genome sequence of soybean (Glycine max), which were denominated as GmMATE1 - GmMATE117. These 117 GmMATE genes were unevenly localized on soybean chromosomes 1 to 20, with both tandem and segmental duplication events detected, and most genes showed tissue-specific expression patterns. Soybean MATE family could be classified into four subfamilies comprising ten smaller subgroups, with diverse potential functions such as transport and accumulation of flavonoids or alkaloids, extrusion of plant-derived or xenobiotic compounds, regulation of disease resistance, and response to abiotic stresses. Eight soybean MATE transporters clustered together with the previously reported MATE proteins related to aluminum (Al) detoxification and iron translocation were further analyzed. Seven stress-responsive cis-elements such as ABRE, ARE, HSE, LTR, MBS, as well as a cis-element of ART1 (Al resistance transcription factor 1), GGNVS, were identified in the upstream region of these eight GmMATE genes. Differential gene expression analysis of these eight GmMATE genes in response to Al stress helps us identify GmMATE75 as the candidate gene for Al tolerance in soybean, whose relative transcript abundance increased at 6, 12 and 24 h after Al treatment, with more fold changes in Al-tolerant than Al-sensitive cultivar, which is consistent with previously reported Al-tolerance related MATE genes.
A total of 117 MATE transporters were identified in soybean and their potential functions were proposed by phylogenetic analysis with known plant MATE transporters. The cis-elements and expression patterns of eight soybean MATE genes related to Al detoxification/iron translocation were analyzed, and GmMATE75 was identified as a candidate gene for Al tolerance in soybean. This study provides a first insight on soybean MATE family and their potential roles in soybean response to abiotic stresses especially Al toxicity.
Multidrug and toxic compound extrusion (MATE) family is the most recent categorized multidrug efflux transporter family, which is a secondary transporter family that couples the translocation of substrates with an electrochemical gradient of cations (such as H+ or Na+ ions) across the membrane [1, 2]. The X-ray structure of the MATE transporter, NorM from Vibrio cholerae, reveals a unique topology of its predicted 12 transmembrane (TM) helices, which is distinct from any other known multidrug resistance transporter .
MATE transporters are widely distributed in bacteria, fungi, mammals and plants . Hvorup et al.  found 203 sequenced proteins in the MATE family, which could be divided into 15 subfamilies. Omote et al.  identified 861 MATE transporters from Archaea, Eubacteria and Eukarya and classified them into three large subfamilies comprising 14 smaller subgroups. There are 56, over 40 and 53 putative MATE transporters in Arabidopsis thaliana , Medicago truncatula  and Oryza sativa , respectively.
The bacterial MATE transporters can export organic cations for multidrug resistance [9, 10]. In yeast (Saccharomyces cerevisiae), the Erc1 MATE-type transporter confers resistance to ethionine . The mammalian MATE transporters can excrete the metabolic waste and xenobiotic organic cations in the kidney and liver [12, 13]. The plant MATE family transports a broad range of substrates such as organic acids, plant hormones and secondary metabolites [14–16]. Recently, the functions of many MATE transporters have been illustrated in plants , including transport of secondary metabolites such as alkaloids , flavonoids [7, 19], and anthocyanidin [20–23], detoxification of toxic compounds or heavy metals [6, 24], regulation of disease resistance [25–27], efflux of plant hormones such as abscisic acid (ABA) , iron translocation [29–31] and aluminum (Al) detoxification [32–35], which indicates MATE transporters play important roles in a wide range of biological processes in plants.
Al toxicity is considered as the main factor limiting crop yield on acidic soils . Under Al stress, root exudation of organic acids, such as malate, citrate, and oxalate, is an important mechanism in plant resistance to Al toxicity [37, 38]. The genes controlling organic anion efflux from roots have been isolated from several crop species [39, 40]. MATE transporters have been shown to mediate the citrate efflux to confer plant tolerance to Al toxicity . The MATE transporters involved in detoxification of Al were first identified from sorghum (Sorghum bicolor, SbMATE) and barley (Hordeum vulgare, HvAACT1) by map-based cloning, respectively [14, 32]. Later study found that the function of HvAACT1 protein is to release citrate to facilitate the translocation of iron from roots to shoots, and the 1-kb insertion in the upstream of the HvAACT1 coding region in the Al-tolerant barley variety enhances and alters its expression to root tips, which is important to detoxifying Al and adaptation to acidic soils in barley . Overexpression of HvAACT1 increases citrate efflux and Al tolerance in wheat and barley . BoMATE from cabbage (Brassica oleracea) requires Al3+ to activate citrate efflux, leading to enhanced Al tolerance in A. thaliana . Several other MATE transporters, such as EcMATE1 (Eucalyptus camaldulensis), OsFRDL4 (O. sativa), and ZmMATE1 (Zea mays), are found localized to plasma membranes in the root tips and related to plant tolerance to Al toxicity [42–44].
Compared with other plant species, little work on MATE transporters has been done in soybean (Glycine max (L.) Merr.), which is an important oil crop worldwide. To date, only one MATE transporter, GmFRD3b (G. max ferric reductase defective 3b), was reported to play a role in iron efficiency in soybean . With the public available whole genome sequence  and RNA-seq Atlas  of G. max, it is possible to identify the genome-wide MATE genes in soybean and investigate their expression patterns and possible functions. Plant MATE transporters have been shown to be involved in diverse functions including Al tolerance. By comparing the sequences of soybean MATE family with the known MATE transporters from other plant species, the possible roles of soybean MATE transporters could be proposed and help us to further test their function. In this study, we performed a genome-wide search of all putative MATE transporters in soybean. Their chromosomal distribution, gene duplication, phylogenetic relationship, structures of genes and proteins, and expression patterns were analyzed. Soybean MATE genes related to Al detoxification/iron translocation were further investigated by promoter analysis and differential gene expression analysis between the root tips of Al-tolerant and Al-sensitive soybean cultivars in response to Al. This study would provide useful information on the research of MATE transporters in soybean.
Results and discussion
Genome-wide identification of soybean MATE transporters
A total of 117 genes encoding MATE transporters (Additional file 1: Table S1) were identified from the soybean whole genome (see details in Methods), which were denominated as GmMATE1 - GmMATE117 according to the soybean nomenclature based on their physical locations . The genomic sequences, coding sequences, and protein sequences of these 117 soybean MATE members (Additional file 2) were downloaded from Phytozome (http://phytozome.jgi.doe.gov/pz/portal.html) .
The details of all 117 soybean MATE proteins, including the length, molecular weight, number of TM, isoelectric point (pI), and predicted subcellular location, are listed in Additional file 3: Table S2. The Soybean MATE proteins consist of 80 to 593 amino acids, containing 2 to 13 TMs, whereas in Arabidopsis, the lengths of MATE proteins range from 400 to 700 amino acids and most with 12 TMs , indicating there are more variations within the soybean MATE family. The predicted molecular weights of soybean MATE proteins range from 8.71 to 64.28 kDa, and the predicted pI values are between 5.13 and 9.70. Their predicted subcellular locations include plasma membrane, chloroplast, cytoplasm, vacuole, endoplasmic reticulum, and extracellular, with 82.91 % (97 out of 117 MATE proteins) located in the plasma membrane, 7.69 % (9 out of 117) located in chloroplast, 5.12 % (6 out of 117), 2.56 % (3 out of 117), 0.85 % (1 out of 117) and 0.85 % located in cytoplasm, vacuole, endoplasmic reticulum, and extracellular, respectively.
Chromosomal locations and duplication patterns of soybean MATE genes
Compared with the number of MATE genes in A. thaliana , M. truncatula , and O. sativa , which contains 56, over 40, and 53 MATE genes, respectively, MATE family in soybean is remarkably large with 117 members, which might result from two whole-genome duplication events in soybean . We further investigated the duplication patterns of soybean MATE family. The duplication analyses showed 96 out of 117 GmMATE genes (82.05 %) were present in duplications (Fig. 1; Additional file 4: Table S3), which indicates duplications contributed largely to the amplification of MATE family in the soybean genome, supporting the previous observation that duplications play important roles in the evolution of large gene families . We observed 25 (21.37 %) GmMATE genes with tandem duplications (on chromosomes 3, 5, 7, 9, 10, 11, 13, 16, 17 and 20), and 71 (60.68 %) GmMATE genes with segmental duplications (Additional file 4: Table S3). Duplication events of GmMATE genes were found on all 20 soybean chromosomes.
Phylogenetic analyses of the soybean MATE family
Subfamily C1 contains three subgroups, C1-1, C1-2 and C1-3. C1-1 consists of 19 sequences, including 11 MATE proteins from soybean and eight previously reported MATE transporters, such as AtFFT (A. thaliana, flower flavonoid transporter) , SlMATE (Solanum lycopersicum MATE) , VvAM1 and VvAM3 (Vitis vinifera anthoMATE1 and 3) [21, 22]. AtFFT is a flavonoid transporter that affects flavonoid levels in Arabidopsis . SlMATE encodes a putative anthocyanin permease, which is co-regulated with ANT1 (anthocyanin) transcription factor, indicating it may function as an anthocyanin vacuolar transporter in tomato leaves . VvAM1 and VvAM3 were found to be involved in the transport of acylated anthocyanins into vacuoles in grapevine [21, 22]. There are 21 soybean MATE proteins in the C1-2 subgroup, with no previously known MATE proteins. There are 11 proteins in the C1-3 subgroup, including five soybean MATE proteins and six previously reported MATE transporters such as AtTT12 (A. thaliana transparent testa 12) , MtMATE1 (M. truncatula MATE1) , NtMATE1 and NtMATE2 (Nicotiana tabacum, MATE1 and 2) , and VvMATE1 (V. vinifera, MATE1) . Arabidopsis TT12, the first MATE transporter found to transport flavonoids , was originally isolated during screening of mutants with altered seed coloration. MtMATE1 from M. truncatula was a functional ortholog of AtTT12 and localized in the tonoplast . NtMATE1 and NtMATE2 were suggested to transport alkaloids from the cytosol into the vacuole in tobacco . The grapevine MATE transporter VvMATE1 was involved in the accumulation of proanthocyanidins . The functions of the known MATE transporters in this clade suggest the MATE subfamily C1 might be involved in (vacuolar) transport and accumulation of flavonoids or alkaloids in plants.
There are 34 soybean MATE proteins in subfamily C2, which are divided into two subgroups. Subgroup C2-1 has 13 soybean MATE proteins and a known MATE protein AtALF5 (A. thaliana aberrant lateral root formation 5), in which mutation led to defects in lateral root formation and increased sensitivity of roots to various compounds, therefore it is thought to confer plant resistance to toxins . Subgroup C2-2 contains 21 soybean MATE members, as well as AtDTX1 (A. thaliana detoxification 1) and NtJAT1 (N. tabacum jasmonate-inducible alkaloid transporter 1) [6, 53]. AtDTX1 was found to mediate the efflux of plant-derived antibiotics and other toxic compounds, and was also able to detoxify the heavy metal, Cd2+ . Tobacco NtJAT1 showed nicotine efflux activity in yeast and was suggested to function as a secondary transporter for nicotine translocation . Therefore, subfamily C2 might be related to the efflux of various compounds.
Subfamily C3 could be further classified into two subgroups. None of the known MATE proteins appears in subgroup C3-1 (six soybean MATE proteins). Subgroup C3-2 contains 29 soybean MATE proteins and three known MATE proteins, AtADS1 (A. thaliana activated disease susceptibility 1, which is also known as Arabidopsis abnormal shoot 3, ABS3) [25, 54], AtDTX50 (A. thaliana detoxification efflux carrier 50) , and AtZF14 (also known as bush and chlorotic dwarf 1, BCD1 or Arabidopsis abnormal shoot 4, ABS4) [15, 54, 55]. Previous research indicated that AtADS1/ABS3 is a negative regulator of plant disease resistance . AtDTX50 functions as an ABA efflux transporter, which regulates ABA sensitivity, stomatal conductance and drought tolerance in Arabidopsis . Overexpression of AtZF14/BCD1/ABS4 increased leaf initiation rate and it is also involved in iron homeostasis [15, 55]. Recently, AtZF14/BCD1/ABS4 and AtADS1/ABS3 were also found to regulate hypocotyl cell elongation . The functions of MATE subfamily C3 seem diversified and need further investigation.
There are three subgroups in subfamily C4. Subgroup C4-1 only contains one soybean MATE protein. Subgroup C4-2 has six soybean MATE proteins and AtEDS5, which is essential for salicylic acid (SA) dependent disease resistance [26, 27]. Subgroup C4-3 contains 22 members, including eight soybean MATE proteins (one of which, GmMATE47, is the known GmFRD3 that has been reported to play a role in iron efficiency ), and 14 previously reported MATE proteins from other plant species that are all related to Al detoxification and/or iron translocation (Additional file 5: Table S4), indicating these eight soybean MATE proteins in subgroup C4-3 might be involved in Al detoxification/iron translocation in soybean.
Gene structures and protein motifs of soybean MATE family
Expression patterns of GmMATE genes in different soybean tissues
Characterization of putative cis-regulatory elements in the promoter regions of subgroup C4-3 GmMATE genes
Number and position of GGNVS element in the promoter region of eight C4-3 soybean MATE genesa
No. of GGNVS
Position of GGNVSb
Expression of the subgroup C4-3 GmMATE genes in response to Al toxicity
A comprehensive genome-wide analysis of MATE family is performed in an important legume species and oil crop, soybean. A total of 117 MATE transporters were identified in soybean and could be classified into four subfamilies, C1, C2, C3 and C4. The soybean MATE family displays great variation in gene structure, protein motif, and tissue expression pattern, which indicates their diverse functions. The expansion of soybean MATE family was largely due to segmental duplications. Seven stress-responsive cis-acting elements and the cis-acting element of ART1 (GGNVS) were identified in the upstream regions of eight GmMATE genes in subgroup C4-3, which contains previously reported MATE genes related to Al detoxification and/or iron translocation. One gene from C4-3 subgroup, GmMATE75, showed differential relative transcript abundance between the root tips of Al-tolerant and Al-sensitive soybean cultivars in response to Al treatment, indicating its potential role in soybean tolerance to Al toxicity. This study provides a foundation to further investigate the functions of soybean MATE genes including the candidate gene for Al tolerance in soybean.
Identification of MATE transporters in soybean
A total of 57 MATE (Pfam: PF01554) protein sequences in Arabidopsis were collected from Phytozome v10.3  (http://phytozome.jgi.doe.gov/pz/portal.html). Soybean putative MATE protein sequences were retrieved by BLASTP searches against the target (Glycine max Wm82.a2.v1) proteome at Phytozome v10.3 using 57 A. thaliana MATE protein sequences as queries (E-value was ≤ 1e-7). These putative MATE sequences were filtered by the presence of conserved MATE domain (Pfam: PF01554) using the Pfam (http://pfam.xfam.org/)  and the Simple Modular Architecture Research Tool (SMART, http://smart.embl-heidelberg.de/smart/batch.pl) , and a total of 117 soybean MATE proteins with MATE domain were identified. Data files containing the information of the final 117 soybean MATE (including their corresponding physical locations on soybean chromosomes, genomic sequences, coding sequences, and protein sequences) were downloaded from Phytozome (http://phytozome.jgi.doe.gov/pz/portal.html)  (Additional file 1: Table S1 and Additional file 2). Theoretical isoelectric point (pI) and molecular weight (MW) of soybean MATE proteins were computed by ExPASy Compute pI/Mw tool (http://www.expasy.ch/tools/pi_tool.html) [71–73]. The subcellular localizations of the MATE proteins were predicted using WoLF PSORT (http://www.genscript.com/wolf-psort.html)  and the numbers of transmembrane helices were predicted by TMHMM Server v. 2.0 (http://www.cbs.dtu.dk/services/TMHMM/) .
Phylogenetic and structural analyses of MATE transporters in soybean
The full protein sequences of 117 soybean MATE (Additional file 1: Table S1 and Additional file 2) and 35 previously reported MATE from other plant species (Additional file 5: Table S4) were used for multiple sequence alignments by ClustalW in MEGA 6.0 . The unrooted phylogenetic tree was then constructed by MEGA 6.0  using the Maximum Likelihood (ML) algorithm with 1000 bootstraps, where the amino acid substitution model was equal input model with uniform rates among sites, using partial deletion (95 % site coverage as cutoff) for gaps and missing data. Gene structure analysis was performed using the Gene Structure Display Server (GSDS) program with default settings . Motifs in MATE proteins were statistically identified using the online tool of Multiple EM for Motif Elicitation (MEME)  (http://meme-suite.org/) with default settings: Motif Width: between 6 and 50 wide (inclusive). Site Distribution: zero or one occurrence (of a contributing motif site) per sequence. The maximum number of motif was set at 12 .
Chromosomal locations and gene duplication analysis
The chromosomal locations of GmMATE genes were illustrated by MapChart . Segmental and tandem duplication events of the soybean MATE family were identified using the Multiple Collinearity Scan toolkit (MCScan)  from the Plant Genome Duplication Database  with default settings: BLASTP was used to search for potential anchors (E <1e-5, top 5 matches) between every possible homolougous pair, and these pairs were used as the input for MCscan. Syntenic blocks were identified using the E-value ≤ 1e − 10 as a significance cutoff. Tandem duplication was defined as homologous genes with less than ten gene loci in-between and >50 % similarity at protein level on a single chromosome .
Characterization of putative cis-elements in the promoter regions of subgroup C4-3 soybean MATE genes
The 1500 bp upstream sequences (Additional file 8) relative to the translation start codon of the eight C4-3 subgroup GmMATE genes were downloaded from Phytozome . The cis-elements in the 1500 bp upstream regions were predicted using the PlantCare database (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/) .
Tissue expression patterns of MATE genes in soybean
The RNA-seq data of soybean MATE genes (Additional file 6: Table S5; Additional file 7: Table S6) were downloaded from Phytozome v10.3  and RNA-seq Atlas  of G. max which is available on SoyBase (http://soybase.org/soyseq/) . Since the RNA-seq Atlas on SoyBase was released in 2010 where the RNA-seq reads have been mapped only to the initial soybean genome assembly (Wm82.a1.v1.), the 21 GmMATE genes that were uniquely identified in the later assembly Wm82.a2.v1 are not represented in this dataset, and there are 19 GmMATE genes have the relative transcript abundance as 0 in all tested tissues. Therefore, we used the RNA-seq data from Phytozome to investigate the tissue expression patterns of soybean MATE family. The heat map with hierarchical clustering of 113 GmMATE genes from Phytozome (excluding 4 GmMATE genes with the relative transcript abundance as 0 across all tested tissues) was constructed to visualize their tissue expression patterns, using average linkage clustering with Euclidean distance by MeV 4.9 software .
Eight GmMATE genes from four subfamilies were randomly selected to be verified by quantitative real-time PCR (qRT-PCR). Soybean tissues were collected according to the developmental stages described by Marc Libault . The seeds of soybean cultivar Kefeng-1 (KF) were germinated in moist sterile sand. Root tips of 3-day-old seedlings were harvested. The seedlings were transferred to the glasshouse under long-day conditions (16-h day/8-h night) at 26/24 °C temperature circulations. Shoot apical meristem (SAM) from V2 stage plants, first trifoliate leaves, stems, and flowers from R2 stage plants, pods from R4 stage plants, and seeds from R6 stage plants were harvested and immediately frozen in liquid nitrogen and stored at − 80 °C. The experiment was performed in triplicates.
Al treatment and RNA isolation
The seeds of Al-tolerant soybean cultivar KF and Al-sensitive cultivar Guangfengmaliaodou (GF) (obtained from the National Center for Soybean Improvement, Nanjing, China), were germinated in moist sterile sand and grown under a photoperiod of 14-h day/10-h night and 26/24 °C (day/night) temperature circulations for three days. Then the seedlings were transferred to 0.5 mM CaCl2 (pH = 4.3) for 24 h before Al treatment. The seedlings were then exposed to 0.5 mM CaCl2 (pH = 4.3) solution containing either 0 μM AlCl3 (control) or 25 μM AlCl3 (treatment) for 6 h, 12 h and 24 h, respectively. The root tips (0–2 mm) were collected and immediately frozen in liquid nitrogen and stored at − 80 °C. The experiment was performed in triplicates.
Total RNA was extracted from all samples using TRIzol according to the manufacturer’s protocol (Invitrogen, USA).
The first-strand cDNAs were synthesized using a PrimerScript First Strand cDNA synthesis kit (TaKaRa, Japan) following the manufacturer’s protocol, in a total of 20 μl reaction volume including 1 μg of total RNA, 4 μl 5X PrimeScript RT Master Mix, and RNAase-free ddH2O. The Semi-quantitative RT-PCR was performed in a final volume of 20 μl containing 2 μl of diluted cDNA, 10 μl 2X Premix Taq version 2.0 Mix (TaKaRa, Japan), and 200 nM of forward and reverse primers (Additional file 11: Table S8). The thermal cycling conditions were set as follows: different cycles of 95 °C for 30 s, 54.5–55 °C for 30 s (54.5, 55 °C for GmMATE75 and GmEF-1a, respectively), and 72 °C for 45 s. The number of cycles is based on the genes and designed primers, which is labeled in the results. The housekeeping gene GmEF-1α was used as the internal control . Electrophoresis was performed using 1 % agarose gels.
Quantitative real-time PCR (qRT-PCR)
Gene-specific primers were designed using primer primer 5.0 (Premier Biosoft International, USA) and synthesized by Invitrogen (Shanghai, China). Quantitative real-time PCR was performed on a Roche 480 Realtime detection system (Roche Diagnostics, Switzerland) following the manufacturer’s instructions. The qRT-PCR was performed in a final volume of 15 μl containing 2 μl cDNA, 7.5 μl 2X SYBR Premix Ex Taq (TaKaRa, Japan), and 200 nM of forward and reverse primers. The amplification program was set as follows: initial denaturation at 95 °C for 5 min; 40 cycles of denaturation at 95 °C for 10 s, annealing at 58 °C for 20 s, and extension at 72 °C for 20 s. The amplification efficiencies (E) of primer pairs for 15 genes (including the housekeeping gene GmEF-1α) were estimated by qRT-PCR using 1X, 5X, 10X, 20X, and 30X dilutions of cDNA, according to the equation: E = [10-1/slope]-1 . Primers and amplification efficiencies of qRT-PCR reactions were shown in Additional file 11: Table S8. The amplicon specificity was verified by melting curve analysis (Additional file 12: Figure S2) and agarose gel electrophoresis. Each experiment was performed in triplicates. The relative expression values were calculated by 2−ΔΔCT method according to Livak and Schmittgen . The housekeeping gene GmEF-1α was used as an internal control  and its invariant expression under our experimental conditions were shown in Additional file 13: Table S9 which showed relative constant Ct values across all samples. The relative expression level of GmMATE genes in response to Al stress (treatment, 25 μM AlCl3) was in comparison to their corresponding samples under normal conditions (control, 0 μM AlCl3) at each time point.
Availability of supporting data
Phylogenetic datasets have been deposited in TreeBase and are accessible via the URL: http://purl.org/phylo/treebase/phylows/study/TB2:S18947?x-accesscode=5794eb5d85e615eed0fe24f0500a289b&format=html.
This work was supported by the National Natural Science Foundation of China (31371645), the National High-tech R & D Program of China (2013AA102602), the Fundamental Research Funds for the Central Universities, the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT13073), the Program for New Century Excellent Talents in University (NCET-12-0891), the Program for High-level Innovative and Entrepreneurial Talents in Jiangsu Province, and the Jiangsu Higher Education PAPD Program.
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- Kuroda T, Tsuchiya T. Multidrug efflux transporters in the MATE family. Biochim Biophys Acta. 2009;1794(5):763–8.View ArticlePubMedGoogle Scholar
- Shoji T. ATP-binding cassette and multidrug and toxic compound extrusion transporters in plants: a common theme among diverse detoxification mechanisms. Int Rev Cell Mol Biol. 2014;309:303–46.View ArticlePubMedGoogle Scholar
- He X, Szewczyk P, Karyakin A, Evin M, Hong WX, Zhang Q, et al. Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature. 2010;467(7318):991–4.View ArticlePubMedPubMed CentralGoogle Scholar
- Omote H, Hiasa M, Matsumoto T, Otsuka M, Moriyama Y. The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci. 2006;27(11):587–93.View ArticlePubMedGoogle Scholar
- Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem. 2003;270(5):799–813.View ArticlePubMedGoogle Scholar
- Li LG, He ZY, Pandey GK, Tsuchiya T, Luan S. Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem. 2002;277(7):5360–8.View ArticlePubMedGoogle Scholar
- Zhao J, Dixon RA. MATE transporters facilitate vacuolar uptake of epicatechin 3’-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell. 2009;21(8):2323–40.View ArticlePubMedPubMed CentralGoogle Scholar
- Tiwari M, Sharma D, Singh M, Tripathi RD, Trivedi PK. Expression of OsMATE1 and OsMATE2 alters development, stress responses and pathogen susceptibility in Arabidopsis. Sci Rep. 2014;4:3964.View ArticlePubMedPubMed CentralGoogle Scholar
- Miyamae S, Ueda O, Yoshimura F, Hwang J, Tanaka Y, Nikaido H. A MATE family multidrug efflux transporter pumps out fluoroquinolones in Bacteroides thetaiotaomicron. Antimicrob Agents Chemother. 2001;45(12):3341–6.View ArticlePubMedPubMed CentralGoogle Scholar
- Kaatz GW, McAleese F, Seo SM. Multidrug resistance in Staphylococcus aureus due to overexpression of a novel multidrug and toxin extrusion (MATE) transport protein. Antimicrob Agents Chemother. 2005;49(5):1857–64.View ArticlePubMedPubMed CentralGoogle Scholar
- Shiomi N, Fukuda H, Fukuda Y, Murata K, Kimura A. Nucleotide sequence and characterization of a gene conferring resistance to ethionine in yeast saccharomyces cerevisiae. J Ferment Bioeng. 1991;71(4):211–5.View ArticleGoogle Scholar
- Hiasa M, Matsumoto T, Komatsu T, Moriyama Y. Wide variety of locations for rodent MATE1, a transporter protein that mediates the final excretion step for toxic organic cations. Am J Physiol-cell Ph. 2006;291(4):C678–86.View ArticleGoogle Scholar
- Ullrich KJ. Specificity of transporters for ‘organic anions’ and ‘organic cations’ in the kidney. Biochim Biophys Acta. 1994;1197(1):45–62.View ArticlePubMedGoogle Scholar
- Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, Wang Y-H, et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet. 2007;39(9):1156–61.View ArticlePubMedGoogle Scholar
- Seo PJ, Park J, Park M-J, Kim Y-S, Kim S-G, Jung J-H, et al. A Golgi-localized MATE transporter mediates iron homoeostasis under osmotic stress in Arabidopsis. Biochem J. 2012;442:551–61.View ArticlePubMedGoogle Scholar
- Thompson EP, Wilkins C, Demidchik V, Davies JM, Glover BJ. An Arabidopsis flavonoid transporter is required for anther dehiscence and pollen development. J Exp Bot. 2010;61(2):439–51.View ArticlePubMedPubMed CentralGoogle Scholar
- Takanashi K, Shitan N, Yazaki K. The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnology. 2014;31(5):417–30.View ArticleGoogle Scholar
- Shoji T, Inai K, Yazaki Y, Sato Y, Takase H, Shitan N, et al. Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots. Plant Physiol. 2009;149(2):708–18.View ArticlePubMedPubMed CentralGoogle Scholar
- Debeaujon I, Peeters AJM, Leon-Kloosterziel KM, Koornneef M. The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell. 2001;13(4):853–71.View ArticlePubMedPubMed CentralGoogle Scholar
- Perez-Diaz R, Ryngajllo M, Perez-Diaz J, Pena-Cortes H, Casaretto JA, Gonzalez-Villanueva E, et al. VvMATE1 and VvMATE2 encode putative proanthocyanidin transporters expressed during berry development in Vitis vinifera L. Plant Cell Rep. 2014;33(7):1147–59.View ArticlePubMedGoogle Scholar
- Gomez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, Verries C, et al. Grapevine MATE-type proteins act as vacuolar H + −dependent acylated anthocyanin transporters. Plant Physiol. 2009;150(1):402–15.View ArticlePubMedPubMed CentralGoogle Scholar
- Gomez C, Conejero G, Torregrosa L, Cheynier V, Terrier N, Ageorges A. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of anthoMATE transporters and GST. Plant J. 2011;67(6):960–70.View ArticlePubMedGoogle Scholar
- Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, et al. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell. 2003;15(8):1689–703.View ArticlePubMedPubMed CentralGoogle Scholar
- Diener AC, Gaxiola RA, Fink GR. Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell. 2001;13(7):1625–38.View ArticlePubMedPubMed CentralGoogle Scholar
- Sun X, Gilroy EM, Chini A, Nurmberg PL, Hein I, Lacomme C, et al. ADS1 encodes a MATE‐transporter that negatively regulates plant disease resistance. New Phytol. 2011;192(2):471–82.View ArticlePubMedGoogle Scholar
- Nawrath C, Heck S, Parinthawong N, Metraux JP. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell. 2002;14(1):275–86.View ArticlePubMedPubMed CentralGoogle Scholar
- Ishihara T, Sekine KT, Hase S, Kanayama Y, Seo S, Ohashi Y, et al. Overexpression of the Arabidopsis thaliana EDS5 gene enhances resistance to viruses. Plant Biol. 2008;10(4):451–61.View ArticlePubMedGoogle Scholar
- Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L. A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol Plant. 2014;7(10):1522–32.View ArticlePubMedGoogle Scholar
- Durrett TP, Gassmann W, Rogers EE. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. 2007;144(1):197–205.View ArticlePubMedPubMed CentralGoogle Scholar
- Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK. A rice FRD3-like (OsFRDL1) gene is expressed in the cells involved in long-distance transport. Soil Sci Plant Nutr. 2004;50(7):1133–40.View ArticleGoogle Scholar
- Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF. OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol. 2009;149(1):297–305.View ArticlePubMedPubMed CentralGoogle Scholar
- Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, et al. An aluminum-activated citrate transporter in barley. Plant Cell Physiol. 2007;48(8):1081–91.View ArticlePubMedGoogle Scholar
- Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, et al. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun. 2012;3:713.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhou G, Delhaize E, Zhou M, Ryan PR. The barley MATE gene, HvAACT1, increases citrate efflux and Al(3+) tolerance when expressed in wheat and barley. Ann Bot. 2013;112(3):603–12.View ArticlePubMedPubMed CentralGoogle Scholar
- Wu X, Li R, Shi J, Wang J, Sun Q, Zhang H, et al. Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana. Plant Cell Physiol. 2014;55(8):1426–36.View ArticlePubMedGoogle Scholar
- Magalhaes JV, Maron LG, Piñeros MA, Guimarães CT, Kochian LV. Aluminum tolerance in sorghum and maize. In: Varshney RK, Tuberosa R, editors. Translational genomics for crop breeding: abiotic stress, yield and quality, vol. 2. New Jersey: Wiley Blackwell; 2013. p. 83–98.View ArticleGoogle Scholar
- Lyubenova L, Kuhn AJ, Höltkemeier A, Schröder P. Root exudation pattern of Typha latifolia L. plants after copper exposure. Plant Soil. 2013;370(1–2):187–95.View ArticleGoogle Scholar
- Fernández-Aparicio M, Kisugi T, Xie X, Rubiales D, Yoneyama K. Low strigolactone root exudation: a novel mechanism of broomrape (orobanche and phelipanche spp.) resistance available for faba bean breeding. J Agr Food Chem. 2014;62(29):7063–71.View ArticleGoogle Scholar
- Delhaize E, Ma JF, Ryan PR. Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci. 2012;17(6):341–8.View ArticlePubMedGoogle Scholar
- Zhou G, Delhaize E, Zhou M, Ryan PR. Biotechnological solutions for enhancing the aluminium resistance of crop plants. In: Shanker AK, Venkateswarlu B, editors. Abiotic stress in plants—mechanisms and adaptations. Brisbane: InTech; 2011. p. p119–42.Google Scholar
- Magalhaes JV. How a microbial drug transporter became essential for crop cultivation on acid soils: aluminium tolerance conferred by the multidrug and toxic compound extrusion (MATE) family. Ann Bot. 2010;106(1):199–203.View ArticlePubMedPubMed CentralGoogle Scholar
- Sawaki Y, Kihara-Doi T, Kobayashi Y, Nishikubo N, Kawazu T, Kobayashi Y, et al. Characterization of Al-responsive citrate excretion and citrate-transporting MATEs in Eucalyptus camaldulensis. Planta. 2013;237(4):979–89.View ArticlePubMedGoogle Scholar
- Yokosho K, Yamaji N, Ma JF. An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J. 2011;68(6):1061–9.View ArticlePubMedGoogle Scholar
- Maron LG, Piñeros MA, Guimarães CT, Magalhaes JV, Pleiman JK, Mao C, et al. Two functionally distinct members of the MATE (multi‐drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J. 2010;61(5):728–40.View ArticlePubMedGoogle Scholar
- Rogers EE, Wu X, Stacey G, Nguyen HT. Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol. 2009;166(13):1453–9.View ArticlePubMedGoogle Scholar
- Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463(7278):178–83.View ArticlePubMedGoogle Scholar
- Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, et al. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 2010;10(1):160.View ArticlePubMedPubMed CentralGoogle Scholar
- Patil G, Valliyodan B, Deshmukh R, Prince S, Nicander B, Zhao M, et al. Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics. 2015;16(1):520.View ArticlePubMedPubMed CentralGoogle Scholar
- Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(D1):D1178–86.View ArticlePubMedPubMed CentralGoogle Scholar
- See DR, Brooks S, Nelson JC, Brown-Guedira G, Friebe B, Gill BS. Gene evolution at the ends of wheat chromosomes. Proc Natl Acad Sci. 2006;103(11):4162–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Cannon SB, Mitra A, Baumgarten A, Young ND, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004;4(1):10.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhao J, Huhman D, Shadle G, He XZ, Sumner LW, Tang Y, et al. MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. Plant Cell. 2011;23(4):1536–55.View ArticlePubMedPubMed CentralGoogle Scholar
- Morita M, Shitan N, Sawada K, Van Montagu MCE, Inze D, Rischer H, et al. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc Natl Acad Sci. 2009;106(7):2447–52.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang R, Liu X, Liang S, Ge Q, Li Y, Shao J, et al. A subgroup of MATE transporter genes regulates hypocotyl cell elongation in Arabidopsis. J Exp Bot. 2015;66(20):6327–43.View ArticlePubMedGoogle Scholar
- Burko Y, Geva Y, Refael-Cohen A, Shleizer-Burko S, Shani E, Berger Y, et al. From Organelle to Organ: ZRIZI MATE-Type Transporter is an Organelle Transporter that Enhances Organ Initiation. Plant Cell Physiol. 2011;52(3):518–27.View ArticlePubMedGoogle Scholar
- Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, et al. TM4 microarray software suite. Method Enzymol. 2006;411:134–93.View ArticleGoogle Scholar
- Grant D, Nelson RT, Cannon SB, Shoemaker RC. SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res. 2010;38(Database issue):D843–6.View ArticlePubMedPubMed CentralGoogle Scholar
- Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, et al. Interaction between two cis‐acting elements, ABRE and DRE, in ABA‐dependent expression of Arabidopsis rd29A gene in response to dehydration and high‐salinity stresses. Plant J. 2003;34(2):137–48.View ArticlePubMedGoogle Scholar
- Walker JC, Howard EA, Dennis ES, Peacock WJ. DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc Natl Acad Sci. 1987;84(19):6624–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Larkindale J, Vierling E. Core genome responses involved in acclimation to high temperature. Plant Physiol. 2008;146(2):748–61.View ArticlePubMedPubMed CentralGoogle Scholar
- Shukla PS, Agarwal P, Gupta K, Agarwal PK. Molecular characterisation of a MYB transcription factor from a succulent halophyte involved in stress tolerance. AoB plants. 2015;7:plv054.View ArticlePubMedPubMed CentralGoogle Scholar
- Brown A, Dunn M, Goddard N, Hughes M. Identification of a novel low-temperature-response element in the promoter of the barley (Hordeum vulgare L) gene blt101. 1. Planta. 2001;213(5):770–80.View ArticlePubMedGoogle Scholar
- Mou S, Liu Z, Guan D, Qiu A, Lai Y, He S. Functional analysis and expressional characterization of rice ankyrin repeat-containing protein, Os PIANK1, in basal defense against Magnaporthe oryzae attack. PLoS One. 2013;8:e59699.View ArticlePubMedPubMed CentralGoogle Scholar
- Sazegari S, Niazi A, Ahmadi FS. A study on the regulatory network with promoter analysis for Arabidopsis DREB-genes. Bioinformation. 2015;11(2):101.View ArticlePubMedPubMed CentralGoogle Scholar
- Tsutsui T, Yamaji N, Feng MJ. Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. Plant Physiol. 2011;156(2):925–31.View ArticlePubMedPubMed CentralGoogle Scholar
- Ma JF, Nagao S, Sato K, Ito H, Furukawa J, Takeda K. Molecular mapping of a gene responsible for Al‐activated secretion of citrate in barley. J Exp Bot. 2004;55(401):1335–41.View ArticlePubMedGoogle Scholar
- Famoso AN, Zhao K, Clark RT, Tung C-W, Wright MH, Bustamante C, et al. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet. 2011;7(8):e1002221. doi:10.1371/journal.pgen.1002221.View ArticlePubMedPubMed CentralGoogle Scholar
- You J, Zhang H, Liu N, Gao L, Kong L, Yang Z. Transcriptomic responses to aluminum stress in soybean roots. Genome. 2011;54(11):923–33.View ArticlePubMedGoogle Scholar
- Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42(Database issue):D222–30.View ArticlePubMedPubMed CentralGoogle Scholar
- Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2015;43(D1):D257–60.View ArticlePubMedPubMed CentralGoogle Scholar
- Bjellqvist B, Hughes GJ, Pasquali C, Paquet N, Ravier F, Sanchez JC, et al. The focusing positions of polypeptides in immobilized pH gradients can be predicted from their amino acid sequences. Electrophoresis. 1993;14(10):1023–31.View ArticlePubMedGoogle Scholar
- Bjellqvist B, Basse B, Olsen E, Celis JE. Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis. 1994;15(3–4):529–39.View ArticlePubMedGoogle Scholar
- Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, et al. Protein identification and analysis tools in the ExPASy Server. Methods Mol Biol. 1999;112:531–52.PubMedGoogle Scholar
- Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35(Web Server issue):W585–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Krogh A, Larsson B, Von Heijne G, Sonnhammer E. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–80.View ArticlePubMedGoogle Scholar
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Hu B, Jin JP, Guo AY, Zhang H, Luo JC, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2015;31:1296–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Bailey TL, Bodén M, Buske FA, Frith M, Grant CG, Clementi L, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Voorrips R. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002;93(1):77–8.View ArticlePubMedGoogle Scholar
- Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40(7):e49. doi:10.1093/nar/gkr1293.View ArticlePubMedPubMed CentralGoogle Scholar
- Lee T-H, Tang H, Wang X, Paterson AH. PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res. 2013;41(D1):D1152–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Gupta S, Garg V, Kant C, Bhatia S. Genome-wide survey and expression analysis of F-box genes in chickpea. BMC Genomics. 2015;16(1):67. doi:10.1186/s12864-015-1293-y.View ArticlePubMedPubMed CentralGoogle Scholar
- Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Libault M, Farmer A, Joshi T, Takahashi K, Langley RJ, Franklin LD, et al. An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants. Plant J. 2010;63(1):86–99.PubMedGoogle Scholar
- Liang C, Pineros MA, Tian J, Yao Z, Sun L, Liu J, et al. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol. 2013;161(3):1347–61.View ArticlePubMedPubMed CentralGoogle Scholar
- Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 2001;29(9):e45.View ArticlePubMedPubMed CentralGoogle Scholar
- Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001;25(4):402–8.View ArticlePubMedGoogle Scholar
- Liu J, Li Y. Supporting data for soybean MATE family. LabArchives. 2016. http://www.labarchives.com/. doi: 10.6070/H47M05ZFGoogle Scholar