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Genome-wide identification and characterization of the metal tolerance protein (MTP) family in grape (Vitis vinifera L.)

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Abstract

Metal tolerance proteins (MTPs) play an important role in the transport of metals at the cellular, tissue and whole plant levels. In the present study, 11 MTP genes were identified and these clustered in three major sub-families Fe/Zn-MTP, Zn-MTP, and Mn-MTP, and seven groups, which are similar to the grou** of MTP genes in both Arabidopsis and rice. Vitis vinifera metal tolerance proteins (VvMTP) ranged from 366 to 1092 amino acids, were predicted to be located in the cell vacuole, and had four to six putative TMDs, except for VvtMTP12 and VvMTP1. The VvMTPs had putative cation diffusion facilitator (CDF) domains and the putative Mn-MTPs also had zinc transporter dimerization domains (ZD-domains). V. vinifera Mn-MTPs had gene structures and motif distributions similar to those of the Fe/Zn-MTP and Zn-MTP sub-families. The upstream regions of VvMTP genes had variable frequencies of cis-regulatory elements that could indicate regulation at different developmental stages and/or differential regulation in response to stress. Comparison of the VvMTP coding sequences with known miRNAs found in various plant species indicated the presence of 13 putative miRNAs, with 7 of these associated with VvMTPs. Temporal and spatial expression profiling indicates a potential role for VvMTP genes during growth and development in grape plants, as well as the involvement of these genes in plant responses to environmental stress, especially osmotic stress. The data generated from this study provides a basis for further investigation of the roles of MTP genes in grapes.

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References

  • Ahmad P (2016) Water stress and crop plants: a sustainable approach. Wiley-Blackwell, New York

    Google Scholar 

  • Arrivault S, Senger T, Krämer U (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J 46:861–879

    CAS  PubMed  Google Scholar 

  • Bae S-H, Han HW, Moon J (2015) Functional analysis of the molecular interactions of TATA box-containing genes and essential genes. PLoS One 10:e0120848

    PubMed  PubMed Central  Google Scholar 

  • Bailey TL et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    CAS  PubMed  Google Scholar 

  • Blaudez D, Kohler A, Martin F, Sanders D, Chalot M (2003) Poplar metal tolerance protein 1 confers zinc tolerance and is an oligomeric vacuolar zinc transporter with an essential leucine zipper motif. Plant Cell 15:2911–2928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burklew CE, Ashlock J, Winfrey WB, Zhang B (2012) Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum). PLoS One 7:e34783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cambrollé J, García J, Figueroa M, Cantos M (2015) Evaluating wild grapevine tolerance to copper toxicity. Chemosphere 120:171–178

    PubMed  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

    CAS  PubMed  Google Scholar 

  • Chattopadhyay S, Puente P, Deng XW, Wei N (1998) Combinatorial interaction of light-responsive elements plays a critical role in determining the response characteristics of light-regulated promoters in Arabidopsis. Plant J 15:69–77

    CAS  PubMed  Google Scholar 

  • Chen Z et al (2013) Mn tolerance in rice is mediated by MTP8. 1, a member of the cation diffusion facilitator family. J Exp Bot 64:4375–4387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    CAS  Google Scholar 

  • Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–315

    CAS  PubMed  Google Scholar 

  • Delhaize E, Kataoka T, Hebb DM, White RG, Ryan PR (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15:1131–1142

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eroglu S, Meier B, von Wirén N, Peiter E (2016) The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiol 170:1030–1045

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Fu X-Z et al (2017) Genome-wide identification of sweet orange (Citrus sinensis) metal tolerance proteins and analysis of their expression patterns under zinc, manganese, copper, and cadmium toxicity. Gene 629:1–8

    CAS  PubMed  Google Scholar 

  • Fujiwara T, Kawachi M, Sato Y, Mori H, Kutsuna N, Hasezawa S, Maeshima M (2015) A high molecular mass zinc transporter MTP12 forms a functional heteromeric complex with MTP5 in the Golgi in Arabidopsis thaliana. FEBS J 282:1965–1979

    CAS  PubMed  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. The proteomics protocols handbook. Springer, Berlin, pp 571–607

    Google Scholar 

  • Gielen H, Remans T, Vangronsveld J, Cuypers A (2012) MicroRNAs in metal stress: specific roles or secondary responses? Int J Mol Sci 13:15826–15847

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261

    CAS  PubMed  Google Scholar 

  • Goodstein DM et al (2011) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    PubMed  PubMed Central  Google Scholar 

  • Guo J et al (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genom 35:105–118

    CAS  Google Scholar 

  • Gustin JL, Zanis MJ, Salt DE (2011) Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11:76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    CAS  PubMed  Google Scholar 

  • Haney CJ, Grass G, Franke S, Rensing C (2005) New developments in the understanding of the cation diffusion facilitator family. J Ind Microbiol Biotechnol 32:215–226

    CAS  PubMed  Google Scholar 

  • Hayat S, Khalique G, Irfan M, Wani AS, Tripathi BN, Ahmad A (2012) Physiological changes induced by chromium stress in plants: an overview. Protoplasma 249:599–611

    CAS  PubMed  Google Scholar 

  • Huang SQ, **ang AL, Che LL, Chen S, Li H, Song JB, Yang ZM (2010) A set of miRNAs from Brassica napus in response to sulfate deficiency and cadmium stress. Plant Biotechnol J 8:887–899

    CAS  PubMed  Google Scholar 

  • Jaillon O et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463

    CAS  PubMed  Google Scholar 

  • Jiang S-Y, Ma Z, Ramachandran S (2010) Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol 10:79

    PubMed  PubMed Central  Google Scholar 

  • Jiang H et al (2015) Genome-wide analysis of HD-Zip genes in grape (Vitis vinifera). Tree Genet Genomes 11:827

    Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    CAS  PubMed  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45:1749–1758

    CAS  PubMed  Google Scholar 

  • Kolaj-Robin O, Russell D, Hayes KA, Pembroke JT, Soulimane T (2015) Cation diffusion facilitator family: structure and function. FEBS Lett 589:1283–1295

    CAS  PubMed  Google Scholar 

  • Laloum T, De Mita S, Gamas P, Baudin M, Niebel A (2013) CCAAT-box binding transcription factors in plants: Y so many? Trends Plant Sci 18:157–166

    CAS  PubMed  Google Scholar 

  • Li Q, Cai S, Mo C, Chu B, Peng L, Yang F (2010) Toxic effects of heavy metals and their accumulation in vegetables grown in a saline soil. Ecotoxicol Environ Saf 73:84–88

    CAS  PubMed  Google Scholar 

  • Li X, Wu Y, Li B, He W, Yang Y, Yang Y (2018) Genome-wide identification and expression analysis of the cation diffusion facilitator gene family in turnip under diverse metal ion stresses. Front Genet 9:103

    PubMed  PubMed Central  Google Scholar 

  • Lima J, Arenhart R, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Res 10:2817–2832

    CAS  PubMed  Google Scholar 

  • Liu Z et al (2014) Genome-wide identification, phylogeny, duplication, and expression analyses of two-component system genes in Chinese cabbage (Brassica rapa ssp. pekinensis). DNA Res 21:379–396

    PubMed  PubMed Central  Google Scholar 

  • López-Ochoa L, Acevedo-Hernández G, Martínez-Hernández A, Argüello-Astorga G, Herrera-Estrella L (2007) Structural relationships between diverse cis-acting elements are critical for the functional properties of a rbcS minimal light regulatory unit. J Exp Bot 58:4397–4406

    PubMed  Google Scholar 

  • Lu M, Fu D (2007) Structure of the zinc transporter YiiP. Science 317:1746–1748

    CAS  PubMed  Google Scholar 

  • Lu M, Chai J, Fu D (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nat Struct Mol Biol 16:1063

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lv S, Nie X, Wang L, Du X, Biradar SS, Jia X, Weining S (2012) Identification and characterization of microRNAs from barley (Hordeum vulgare L.) by high-throughput sequencing. Int J Mol Sci 13:2973–2984

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marschner H (2011) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic, Cambridge

    Google Scholar 

  • Menguer PK, Farthing E, Peaston KA, Ricachenevsky FK, Fett JP, Williams LE (2013) Functional analysis of the rice vacuolar zinc transporter OsMTP1. J Exp Bot 64:2871–2883

    CAS  PubMed  PubMed Central  Google Scholar 

  • Migocka M et al (2015) Cucumber metal tolerance protein CsMTP9 is a plasma membrane H+-coupled antiporter involved in the Mn2+ and Cd2+ efflux from root cells. Plant J 84:1045–1058

    CAS  PubMed  Google Scholar 

  • Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the cation diffusion facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genom 8:107

    Google Scholar 

  • Omasits U, Ahrens CH, Müller S, Wollscheid B (2013) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30:884–886

    PubMed  Google Scholar 

  • Ozyigit II, Filiz E, Vatansever R, Kurtoglu KY, Koc I, Öztürk MX, Anjum NA (2016) Identification and comparative analysis of H2O2-scavenging enzymes (ascorbate peroxidase and glutathione peroxidase) in selected plants employing bioinformatics approaches. Front Plant Sci 7:301

    PubMed  PubMed Central  Google Scholar 

  • Pedas P, Stokholm MS, Hegelund JN, Ladegård AH, Schjoerring JK, Husted S (2014) Golgi localized barley MTP8 proteins facilitate Mn transport. PLoS One 9:e113759

    PubMed  PubMed Central  Google Scholar 

  • Peiter E et al (2007) A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proc Natl Acad Sci 104:8532–8537

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puente P, Wei N, Deng XW (1996) Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J 15:3732–3743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ricachenevsky FK, Menguer PK, Sperotto RA, Williams LE, Fett JP (2013) Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front Plant Sci 4:144

    PubMed  PubMed Central  Google Scholar 

  • Saeed AI et al (2006) TM4 microarray software suite. Methods Enzymol 411:134–193

    CAS  PubMed  Google Scholar 

  • Satheesh V, Jagannadham PTK, Chidambaranathan P, Jain P, Srinivasan R (2014) NAC transcription factor genes: genome-wide identification, phylogenetic, motif and cis-regulatory element analysis in pigeonpea (Cajanus cajan (L.) Millsp.). Mol Biol Rep 41:7763–7773

    CAS  PubMed  Google Scholar 

  • Shahzad Z, Gosti F, Frérot H, Lacombe E, Roosens N, Saumitou-Laprade P, Berthomieu P (2010) The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet 6:e1000911

    PubMed  PubMed Central  Google Scholar 

  • Sharp PA (1981) Speculations on RNA splicing. Cell 23:643–646

    CAS  PubMed  Google Scholar 

  • Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    CAS  PubMed  Google Scholar 

  • Shuai P, Liang D, Zhang Z, Yin W, **a X (2013) Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genom 14:233

    CAS  Google Scholar 

  • Singh RK, Anandhan S, Singh S, Patade VY, Ahmed Z, Pande V (2011) Metallothionein-like gene from Cicer microphyllum is regulated by multiple abiotic stresses. Protoplasma 248:839–847

    CAS  PubMed  Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143

    PubMed  PubMed Central  Google Scholar 

  • Srivastava S, Srivastava AK, Suprasanna P, D’souza S (2012) Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. J Exp Bot 64:303–315

    PubMed  Google Scholar 

  • Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Buchner P, Yoshimoto N, Hawkesford MJ, Shiu S-H (2012) Evolutionary relationships and functional diversity of plant sulfate transporters. Front Plant Sci 2:119

    PubMed  PubMed Central  Google Scholar 

  • Thomine S, Vert G (2013) Iron transport in plants: better be safe than sorry. Curr Opin Plant Biol 16:322–327

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno D et al (2015) A polarly localized transporter for efficient manganese uptake in rice. Nat Plants 1:15170

    CAS  PubMed  Google Scholar 

  • Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187:805–818

    PubMed  Google Scholar 

  • Vatansever R, Filiz E, Eroglu S (2017) Genome-wide exploration of metal tolerance protein (MTP) genes in common wheat (Triticum aestivum): insights into metal homeostasis and biofortification. Biometals 30:217–235

    CAS  PubMed  Google Scholar 

  • Wan P et al (2011) Computational analysis of drought stress-associated miRNAs and miRNA co-regulation network in Physcomitrella patens. Genom Proteomics Bioinform 9:37–44

    CAS  Google Scholar 

  • Wang C-Q, Tao W, ** M, Z-c Li, Ling Y (2013) Quantitative trait loci for mercury tolerance in rice seedlings. Rice Sci 20:238–242

    Google Scholar 

  • Wang M et al (2014) Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Hortic Res 1:14016

    PubMed  PubMed Central  Google Scholar 

  • **e FL, Huang SQ, Guo K, **ang AL, Zhu YY, Nie L, Yang ZM (2007) Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett 581:1464–1474

    CAS  PubMed  Google Scholar 

  • Yang X, Feng Y, He Z, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353

    CAS  PubMed  Google Scholar 

  • Yu LJ et al (2012) Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol 195:97–112

    CAS  PubMed  Google Scholar 

  • Yuan L, Yang S, Liu B, Zhang M, Wu K (2012) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep 31:67–79

    PubMed  Google Scholar 

  • Zeng Q-Y, Yang C-Y, Ma Q-B, Li X-P, Dong W-W, Nian H (2012) Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biol 12:182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Liu B (2017) Identification of a rice metal tolerance protein OsMTP11 as a manganese transporter. PLoS One 12:e0174987

    PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X (2012) Genome-wide identification and analysis of the TIFY gene family in grape. PLoS One 7:e44465

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao T, Liang D, Wang P, Liu J, Ma F (2012) Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol Genet Genom 287:423–436

    CAS  Google Scholar 

  • Zhou ZS, Huang SQ, Yang ZM (2008a) Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 374:538–542

    CAS  PubMed  Google Scholar 

  • Zhou ZS, Wang SJ, Yang ZM (2008b) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70:1500–1509

    CAS  PubMed  Google Scholar 

  • Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012) Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35:86–99

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Malayer University, P.O. Box: 65719-95863, Malayer, Iran

    Zahra Shirazi

  2. Department of Biotechnology, Faculty of Agricultural Sciences, University of Guilan, P.O. Box: 41635-1314, Rasht, Iran

    Amin Abedi & Mojtaba Kordrostami

  3. Rice Research Institute of Iran, Agricultural Research, Education and Extension Organization (AREEO), Rasht, Iran

    Mojtaba Kordrostami

  4. Department of Botany, University of Otago, Dunedin, New Zealand

    David J. Burritt

  5. Department of Genetics and Plant Breeding, Bangladesh Agricultural University, Mymensingh, 2202, Bangladesh

    Mohammad Anwar Hossain

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  1. Zahra Shirazi
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Shirazi, Z., Abedi, A., Kordrostami, M. et al. Genome-wide identification and characterization of the metal tolerance protein (MTP) family in grape (Vitis vinifera L.). 3 Biotech 9, 199 (2019). https://doi.org/10.1007/s13205-019-1728-2

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