Genome-wide mining and characterization of MATE transporters in Coriandrum sativum L.

Document Type : Original article

Authors

Bioinformatics Centre, Kerala Agricultural University, Thrissur-680 656, India

Abstract

Multidrug and Toxic Compound Extrusion (MATE) proteins are responsible for the transport of a wide range of metabolites out of plant cells. This helps to protect the cells from toxins and other harmful compounds. MATE proteins also play a role in plant development, by regulating the transport of hormones and other signalling molecules. They transport a wide variety of substances, including organic acids, plant hormones, flavonoids, alkaloids, terpenes and other secondary metabolites. MATE proteins are thought to play similar roles in Coriander, in addition to stress responses. The MATE genes in the coriander genome have been identified and characterized. Detailed genome homology search and domain identification analysis have identified 91 MATE proteins in the genome assembly of coriander. A phylogenetic analysis of the identified proteins divided them into five major clades. The functions of the transporters in each cluster were predicted based on the clustering pattern of the functionally characterized proteins. The amino acid sequences, exon-intron structures and motif details of all the 91 proteins are identified and described. This is the first work on the MATE transporters in coriander and the results deliver clues for the molecular mechanisms behind the stress responses and secondary metabolite transport in coriander.

Keywords

References

  1. Song X, Wang J, Li N, Yu J, Meng F, Wei C, Liu C, Chen W, Nie F, Zhang Z, Gong K, Li X, Hu J, Yang Q, Li Y, Li C, Feng S, Guo H, Yuan J, Pri Q, Yu T, Kang X, Zhao W, Lei T, Sun P, Wang L, Ge W, Guo D, Duan X,Shen S, Cui C, Yu Y, Xie Y, Zhang J, Hou Y, Wang J, Li XQ, Paterson AH, Wang X. Deciphering the high‐quality genome sequence of coriander that causes controversial feelings. Plant Biotechnol J 2020;18:1444-1456.
  2. Ewase AE-Din SS, Omran S, El-Sherif S, Tawfik N. Effect of salinity stress on coriander (Coriandrum sativum) seeds germination and plant growth. Egypt Acad J Biol Sci H. Bot 2013;4:1-7.
  3. Fattahi B, Arzani K, Souri MK, Barzegar M. Morphophysiological and phytochemical responses to cadmium and lead stress in coriander (Coriandrum sativum L.). Ind Crops Prod 2021;171:113979.
  4. Kuroda T, Tsuchiya T. Multidrug efflux transporters in the MATE family. Biochim Biophys Acta 2009;1794:763-768.
  5. Morita Y, Kodama K, Shiota S, Mine T, Kataoka A, Mizushima T, Tsuchiya T. NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother 1998;42:1778-1782.
  6. Brown MH, Paulsen IT, Skurray RA. The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 1999;31:394-395.
  7. 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;27:587-593.
  8. He X, Szewczyk P, Karyakin A, Evin M, Hong WX, Zhang Q, Chang G. Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature 2010;467:991-994.
  9. Radchenko M, Nie R, Lu M. Disulfide cross-linking of a multidrug and toxic compound extrusion transporter impacts multidrug efflux. J Biol Chem 2016;291:9818-9826.
  10. Kusakizako T, Miyauchi H, Ishitani R, Nureki O. Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochim Biophys Acta Biomembr 2020;1862:183154.
  11. Li L, He Z, 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: 5360-5368.
  12. 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;309:303-346.
  13. Ullrich KJ. Specificity of transporters for ‘organic anions’ and ‘organic cations’ in the kidney. Biochim Biophys Acta 1994;1197:45-62.
  14. Terada T, Inui KI. Physiological and pharmacokinetic roles of H+/organic cation antiporters (MATE/SLC47A). Biochem Pharmacol 2008;75:1689-1696.
  15. Upadhyay N, Kar D, Deepak Mahajan B, Nanda S, Rahiman R, Panchakshari N, Bhagavatula L, Datta S. The multitasking abilities of MATE transporters in plants. J Exp Bot 2019;70:4643-4656.
  16. Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier Jr MH. The multidrug/oligosaccharidyl‐lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 2003;270:799-813.
  17. Zhang W, Liao L, Xu J, Han Y, Li L. Genome-wide identification, characterization and expression analysis of MATE family genes in apple (Malus × domestica Borkh). BMC Genomics 2021;22:632.
  18. Zhang X, Weir B, Wei H, Deng Z, Zhang X, Zhang Y, Xu X, Zhao C, Berger JD, Vance W, Bell R, Jia Y, Li C. Genome-wide identification and transcriptional analyses of MATE transporter genes in root tips of wild Cicer spp. under aluminium stress. BioRxiv 2020.
  19. Chen Q, Wang L, Liu D, Ma S, Dai Y, Zhang X, Wang Y, Hu T, Xiao M, Zhou Y, Qi H, Xiao S, Yu L. Identification and expression of the multidrug and toxic compound extrusion (MATE) gene family in Capsicum annuum and Solanum tuberosum. Plants (Basel) 2020; 9:1448.
  20. Santos AL, Chaves-Silva S, Yang L, Maia LGS, Chalfun-Júnior A, Sinharoy S, Zhao J, Benedito VA. Global analysis of the MATE gene family of metabolite transporters in tomato. BMC Plant Biol 2017;17:185.
  21. Duan W, Lu F, Cui Y, Zhang J, Du X, Hu Y, Yan Y. Genome-wide identification and characterisation of wheat MATE genes reveals their roles in aluminium tolerance. Int J Mol Sci 2022;23:4418.
  22. Zhu H, Wu J, Jiang Y, Jin J, Zhou WE, Wang Y, Han G, Zhao Y, Cheng B. Genomewide analysis of MATE-type gene family in maize reveals microsynteny and their expression patterns under aluminum treatment. J Genet 2016;95:691-704.
  23. Gani U, Sharma P, Tiwari H, Nautiyal AK, Kundan M, Wajid MA, Kesari R, Nargotra A, Misra P. Comprehensive genome-wide identification, characterization, and expression profiling of MATE gene family in Nicotiana tabacum. Gene 2021;783:145554.
  24. Shijili M, Valsalan R, Mathew D. Genome wide identification and characterization of MATE family genes in mangrove plants. Genetica 2023;151:241-249.
  25. 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;144:197-205.
  26. 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;149:297-305.
  27. Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, Sato K, Nakazono M, Ma JF. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun 2012;3:713.
  28. 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;7:1522-1532.
  29. Debeaujon I, Peeters AJ, Léon-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;13:853-871.
  30. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M. The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 2007;19:2023-2038.
  31. 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;21:2323-2340.
  32. Lu P, Magwanga RO, Kirungu JN, Hu Y, Dong Q, Cai X, Zhou Z, Wang X, Zhang Z, Hou Y, Wang K, Liu F. Overexpression of cotton a DTX/MATE gene enhances drought, salt, and cold stress tolerance in transgenic Arabidopsis. Front Plant Sci 2019;10:299.
  33. Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF. An aluminum-activated citrate transporter in barley. Plant Cell Physiol 2007;48:1081-1091.
  34. Stanke M, Diekhans M, Baertsch R, Haussler D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 2008;24:637-644.
  35. Takanashi K, Shitan N, Yazaki K. The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotech 2014;31:417-430.
  36. Pundir S, Martin MJ, O’Donovan C. UniProt protein knowledgebase. In: Wu, C.H.; Arighi, C.N.; Ross, K.E. (eds.), Protein Bioinformatics: From Protein Modifications and Networks to Proteomics, Methods Mol Biology 2017;1558:ISBN 978-1-4939-6781-0, Humana Press, Springer, New York, pp.41-55.
  37. Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol 2011;7;e1002195.
  38. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012;28:3150-3152.
  39. Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS, Thanki N, Yamashita RA, Yang M, Zhang D, Zheng C, Lanczycki CJ, Marchler-Bauer A. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 2020;48(D1):D265-D268.
  40. Letunic I, Khedkar S, Bork P. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res 2021;49:D458-D460.
  41. Möller S, Croning MD, Apweiler R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 2001;17:646-653.
  42. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 2019;20:1160-1166.
  43. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011;27:1164-1165.
  44. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312-1313.
  45. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 2015;31:1296-1297.
  46. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009;37:W202-W208.
  47. Thumuluri V, Almagro Armenteros JJ, Johansen AR, Nielsen H, Winther O. DeepLoc 2.0: multi-label subcellular localization prediction using protein language models. Nucleic Acids Res 2022;50(W1):W228-W234.
  48. Du Z, Su Q, Wu Z, Huang Z, Bao J, Li J, Tu H, Zeng C, Fu J, He H. Genome-wide characterization of MATE gene family and expression profiles in response to abiotic stresses in rice (Oryza sativa). BMC Ecol Evol 2021;21:141.
  49. Ku YS, Cheng SS, Cheung MY, Lam HM. The roles of Multidrug and Toxic Compound Extrusion (MATE) transporters in regulating agronomic traits. Agronomy 2022;12:878.
  50. Saad KR, Kumar G, Puthusseri B, Srinivasa SM, Giridhar P, Shetty NP. Genome-wide identification of MATE, functional analysis and molecular dynamics of DcMATE21 involved in anthocyanin accumulation in Daucus carota. Phytochemistry 2023;210:113676.
  51. Liu J, Li Y, Wang W, Gai J, Li Y. Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean. BMC Genomics 2016;17:223.
  52. Wang L, Bei X, Gao J, Li Y, Yan Y, Hu Y. The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana. BMC Plant Biol 2016; 16:207.
  53. Li Y, He H, He LF. Genome-wide analysis of the MATE gene family in potato. Mol Biol Rep 2019; 46:403-414.
  54. Ku YS, Lin X, Fan K, Cheng SS, Chan TF, Chung G, Lam HM. The identification of MATE antisense transcripts in soybean using strand-specific RNA-seq datasets. Genes (Basel) 2022;13:228.
  55. 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.
  56. Zhang J, Liu J, Zheng F, Yu M, Shabala S, Song WY. Comparative analysis of arsenic transport and tolerance mechanisms: Evolution from prokaryote to higher plants. Cells 2022;11:2741.
  57. Mondal S, Pramanik K, Ghosh SK, Pal P, Ghosh PK, Ghosh A, Maiti TK. Molecular insight into arsenic uptake, transport, phytotoxicity, and defense responses in plants: A critical review. Planta 2022;255:87.
  58. Kar D, Pradhan AA, Dutta A, Bhagavatula L, Datta S, Bhagavatula L, Datta S. The Multidrug and Toxic Compound Extrusion (MATE) family in plants and their significance in metal transport. In: Kumar, K.; Srivastava, S. (eds.) Plant Metal and Metalloid Transporters 2022;ISBN 978-981-19-6102-1, Springer Nature Singapore 2022;151-177.
  59. Bulasag AS, Camagna M, Kuroyanagi T, Ashida A, Ito K, Tanaka A, Sato I, Chiba S, Ojika M, Takemoto D. Botrytis cinerea tolerates phytoalexins produced by Solanaceae and Fabaceae plants through an efflux transporter BcatrB and metabolizing enzymes. Front Plant Sci 2023;14:1177060.
  60. Seo PJ, Park J, Park MJ, Kim YS, Kim SG, Jung JH, Park CM. A Golgi-localized MATE transporter mediates iron homoeostasis under osmotic stress in Arabidopsis. Biochem J 2012; 442:551-561.
  61. Burko Y, Geva Y, Refael-Cohen A, Shleizer-Burko S, Shani E, Berger Y, Halon E, Chuck G, Moshelion M, Ori N. From organelle to organ: ZRIZI MATE-type transporter is an organelle transporter that enhances organ initiation. Plant Cell Physiol 2011;52:518-527.
  62. Muhammad Aslam M, Waseem M, Jakada BH, Okal EJ, Lei Z, Saqib HSA, Yuan W, Xu W, Zhang Q. Mechanisms of abscisic acid-mediated drought stress responses in plants. Int J Mol Sci 2022;23:1084.
  63. Rogers EE, Wu X, Stacey G, Nguyen HT. Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol 2009;166:1453-1459.
  64. Takanashi K, Yokosho K, Saeki K, Sugiyama A, Sato S, Tabata S, Ma JF, Yazaki K. LjMATE1: a citrate transporter responsible for iron supply to the nodule infection zone of Lotus japonicus. Plant Cell Physiol 2013;54:585-594.
  65. Yamasaki K, Motomura Y, Yagi Y, Nomura H, Kikuchi S, Nakai M, Shiina T. Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana. Plant Signal Behav 2013;8:e23603.
  66. Yan L, Riaz M, Liu J, Yu M, Cuncang J. The aluminum tolerance and detoxification mechanisms in plants; recent advances and prospects. Crit Rev Env Sci Tech 2022; 52:1491-1527.
  67. Hajiboland R, Panda CK, Lastochkina O, Gavassi MA, Habermann G, Pereira JF. Aluminum toxicity in plants: Present and future. J Plant Growth Regul 2023;42:3967-3999.
  68. Shitan N, Yazaki K. Accumulation and membrane transport of plant alkaloids. Curr Pharm Biotechnol 2007;8:244-252.
  69. Frank S, Keck M, Sagasser M, Niehaus K, Weisshaar B, Stracke R. Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biol 2011;13:42-50.
  70. Pérez-Díaz R, Ryngajllo M, Pérez-Díaz J, Peña-Cortés H, Casaretto JA, González-Villanueva E, Ruiz-Lara S. VvMATE1 and VvMATE2 encode putative proanthocyanidin transporters expressed during berry development in Vitis vinifera L. Plant Cell Rep 2014; 33:1147-1159.
  71. Nimmy MS, Kumar V, Singh AK, Jain PK, Srinivasan R. Expression analysis of a MATE-type transporter gene of Arabidopsis and its orthologues in rice and chickpea under salt stress. Indian J Genet Plant Breed 2015;75:478-485.
  72. Huang Y, He G, Tian W, Li D, Meng L, Wu D, He T. Genome-wide identification of MATE gene family in potato (Solanum tuberosum L.) and expression analysis in heavy metal stress. Front Genet 2021;12:650500.
  73. Lu P, Magwanga RO, Guo X, Kirungu JN, Lu H, Cai X, Zhou Z, Wei Y, Wang X, Zhang Z, Peng R, Wang K, Liu F. Genome-wide analysis of multidrug and toxic compound extrusion (MATE) family in Gossypium raimondii and Gossypium arboreum and its expression analysis under salt, cadmium, and drought stress. G3 (Bethesda) 2018;8:2483-2500.

Files

Share

How to cite

Statistics