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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Identification and analysis of MATE protein family in Gleditsia sinensis

Zisiye Mu A , Zhun Liang A , Jing Yang A , Shixiang Wei A , Yang Zhao A and Heying Zhou https://orcid.org/0009-0005-3388-3326 A *
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- Author Affiliations

A College of Forestry, Guizhou University, Guiyang 550025, China.

* Correspondence to: zhydyx2019@163.com

Handling Editor: Nieves Fernandez-Garcia

Functional Plant Biology 51, FP23249 https://doi.org/10.1071/FP23249
Submitted: 21 October 2023  Accepted: 22 March 2024  Published: 15 April 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Many studies have shown that multidrug and toxic compound extrusion (MATE) is a new secondary transporter family that plays a key role in secondary metabolite transport, the transport of plant hormones and disease resistance in plants. However, detailed information on this family in Gleditsia sinensis has not yet been reported. In the present study, a total of 45 GsMATE protein members were identified and analysed in detail, including with gene classification, phylogenetic evaluation and conserved motif determination. Phylogenetic analysis showed that GsMATE proteins were divided into six subfamilies. Additionally, in order to understand these members’ regulatory roles in growth and development in G. sinensis, the GsMATEs expression profiles in different tissues and different developmental stages of thorn were examined in transcriptome data. The results of this study demonstrated that the expression of all MATE genes varies in roots, stems and leaves. Notably, the expression levels of GsMATE26, GsMATE32 and GsMATE43 differ most in the early stages of thorn development, peaking at higher levels than in later stages. Our results provide a foundation for further functional characterisation of this important class of transporter family in G. sinensis.

Keywords: bioinformatics, different tissues, expression profile, Gleditsia sinensis, MATE, RNA-seq, thorns, transcriptome.

References

Behrens CE, Smith KE, Iancu CV, Choe J-Y, Dean JV (2019) Transport of anthocyanins and other flavonoids by the Arabidopsis ATP-binding cassette transporter AtABCC2. Scientific Reports 9, 437.
| Crossref | Google Scholar |

Chen S-Y, Tang Y-M, Hu Y-Y, Wang Y, Sun B, Wang X-R, Tang H-R, Chen Q (2018) FaTT12-1, a multidrug and toxin extrusion (MATE) member involved in proanthocyanidin transport in strawberry fruits. Scientia Horticulturae 231, 158-165.
| Crossref | Google Scholar |

Chen G, Liang H, Zhao Q, Wu A-M, Wang B (2020a) Exploiting MATE efflux proteins to improve flavonoid accumulation in Camellia sinensis in silico. International Journal of Biological Macromolecules 143, 732-743.
| Crossref | Google Scholar |

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 (2020b) Identification and expression of the multidrug and toxic compound extrusion (MATE) gene family in Capsicum annuum and Solanum tuberosum. Plants 9, 1448.
| Crossref | Google Scholar |

Debeaujon I, Peeters AJM, Léon-Kloosterziel KM, Koornneef M (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. The Plant Cell 13, 853-871.
| Crossref | Google Scholar |

Dong B, Niu L, Meng D, et al. (2019) Genome-wide analysis of MATE transporters and response to metal stress in Cajanus cajan. Journal of Plant Interactions 14, 265-275.
| Crossref | Google Scholar |

Du Z, Su Q, Wu Z, et al. (2021) Genome-wide characterization of MATE gene family and expression profiles in response to abiotic stresses in rice (Oryza sativa). BMC Ecology and Evolution 21, 141.
| Crossref | Google Scholar |

Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology 144, 197-205.
| Crossref | Google Scholar |

Frank S, Keck M, Sagasser M, Niehaus K, Weisshaar B, Stracke R (2011) Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biology 13, 42-50.
| Crossref | Google Scholar |

Gao J-S, Wu N, Shen Z-L, Lv K, Qian S-H, Guo N, Sun X, Cai Y-P, Lin Y (2016) Molecular cloning, expression analysis and subcellular localization of a Transparent Testa 12 ortholog in brown cotton (Gossypium hirsutum L.). Gene 576, 763-769.
| Crossref | Google Scholar |

Gomez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, Verries C, Souquet J-M, Mazauric J-P, Klein M, Cheynier V, Ageorges A (2009) Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiology 150, 402-415.
| Crossref | Google Scholar |

Green LS, Rogers EE (2004) FRD3 controls iron localization in Arabidopsis. Plant Physiology 136, 2523-2531.
| Crossref | Google Scholar |

Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. The Plant Journal 61, 1041-1052.
| Crossref | Google Scholar |

Hoang MTT, Almeida D, Chay S, et al. (2021) AtDTX25, a member of the multidrug and toxic compound extrusion family, is a vacuolar ascorbate transporter that controls intracellular iron cycling in Arabidopsis. New Phytologist 231, 1956-1967.
| Crossref | Google Scholar |

Kaatz GW, DeMarco CE, Seo SM (2006) MepR, a repressor of the Staphylococcus aureus MATE family multidrug efflux pump MepA, is a substrate-responsive regulatory protein. Antimicrobial Agents and Chemotherapy 50, 1276-1281.
| Crossref | Google Scholar |

Kutchan TM (2001) Ecological arsenal and developmental dispatcher. The paradigm of secondary metabolism. Plant Physiology 125, 58-60.
| Crossref | Google Scholar |

Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. Journal of Biological Chemistry 277, 5360-5368.
| Crossref | Google Scholar |

Li R, Li J, Li S, et al. (2014) ADP1 affects plant architecture by regulating local auxin biosynthesis. PLoS Genetics 10, e1003954.
| Crossref | Google Scholar |

Li Y, He H, He L-F (2019) Genome-wide analysis of the MATE gene family in potato. Molecular Biology Reports 46, 403-414.
| Crossref | Google Scholar |

Liu W-J, Du G-J, Li J-H, Wang Y-Y, Liu Y-H, Zhao B, Hou X-D (2013) Prevention and treatment of total flavonoids from Gleditsiae Spina on lung cancer and its mechanisms. Chinese Traditional and Herbal Drugs 44, 2878-2883 [In Chinese].
| Google Scholar |

Liu J, Li Y, Wang W, Gai J, Li Y (2016) Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean. BMC Genomics 17, 223.
| Crossref | Google Scholar |

Lu M (2016) Structures of multidrug and toxic compound extrusion transporters and their mechanistic implications. Channels 10, 88-100.
| Crossref | Google Scholar |

Ma Q, Yi R, Li L, Liang Z, Zeng T, Zhang Y, Huang H, Zhang X, Yin X, Cai Z, Mu Y, Cheng Y, Zeng Q, Li X, Nian H (2018) GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana. BMC Plant Biology 18, 212.
| Crossref | Google Scholar |

Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul J-M, Debeaujon I, Klein M (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. The Plant Cell 19, 2023-2038.
| Crossref | Google Scholar |

Miyamae S, Ueda O, Yoshimura F, Hwang J, Tanaka Y, Nikaido H (2001) A MATE family multidrug efflux transporter pumps out fluoroquinolones in Bacteroides thetaiotaomicron. Antimicrobial Agents and Chemotherapy 45, 3341-3346.
| Crossref | Google Scholar |

Morita Y, Kodama K, Shiota S, Mine T, Kataoka A, Mizushima T, Tsuchiya T (1998) NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrobial Agents and Chemotherapy 42, 1778-1782.
| Crossref | Google Scholar |

Pineau C, Loubet S, Lefoulon C, et al. (2012) Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genetics 8, e1003120.
| Crossref | Google Scholar |

Qin P, Zhang G, Hu B, et al. (2021) Leaf-derived ABA regulates rice seed development via a transporter-mediated and temperature-sensitive mechanism. Science Advances 7, eabc8873.
| Crossref | Google Scholar |

Scheepers M, Spielmann J, Boulanger M, et al. (2020) Intertwined metal homeostasis, oxidative and biotic stress responses in the Arabidopsis frd3 mutant. The Plant Journal 102, 34-52.
| Crossref | Google Scholar |

Serrano M, Wang B, Aryal B, et al. (2013) Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiology 162, 1815-1821.
| Crossref | Google Scholar |

Shoji T (2014) ATP-binding cassette and multidrug and toxic compound extrusion transporters in plants: a common theme among diverse detoxification mechanisms. In ‘International review of cell and molecular biology. Vol. 309’. (Ed. KW Jeon) pp. 303–346. (Academic Press) doi:10.1016/B978-0-12-800255-1.00006-5

Sun X, Gilroy EM, Chini A, et al. (2011) ADS1 encodes a MATE-transporter that negatively regulates plant disease resistance. New Phytologist 192, 471-482.
| Crossref | Google Scholar |

Tegli S, Bini L, Calamai S, Cerboneschi M, Biancalani C (2020) A MATE transporter is involved in pathogenicity and IAA homeostasis in the hyperplastic plant pathogen Pseudomonas savastanoi pv. nerii. Microorganisms 8, 156.
| Crossref | Google Scholar |

Tiwari M, Sharma D, Singh M, Tripathi RD, Trivedi PK (2014) Expression of OsMATE1 and OsMATE2 alters development, stress responses and pathogen susceptibility in Arabidopsis. Scientific Reports 4, 3964.
| Crossref | Google Scholar |

Upadhyay N, Kar D, Deepak Mahajan B, Nanda S, Rahiman R, Panchakshari N, Bhagavatula L, Datta S (2019) The multitasking abilities of MATE transporters in plants. Journal of Experimental Botany 70, 4643-4656.
| Crossref | Google Scholar |

Upadhyay N, Kar D, Datta S (2020) A multidrug and toxic compound extrusion (MATE) transporter modulates auxin levels in root to regulate root development and promotes aluminium tolerance. Plant, Cell & Environment 43, 745-759.
| Crossref | Google Scholar |

Wang L, Bei X, Gao J, Li Y, Yan Y, Hu Y (2016) The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana. BMC Plant Biology 16, 207.
| Crossref | Google Scholar |

Wang J, Hou Q, Li P, Yang L, Sun X, Benedito VA, Wen J, Chen B, Mysore KS, Zhao J (2017) Diverse functions of multidrug and toxin extrusion (MATE) transporters in citric acid efflux and metal homeostasis in Medicago truncatula. The Plant Journal 90, 79-95.
| Crossref | Google Scholar |

Wang S, Jiang D-Q, Kang C-Z, Wan X-F, Wang R-S, Liang J-W, Wang H-Y, Li T, Wang T-L, Huang L-Q, Guo L-P (2020) Core position of secondary metabolism of medicinal plants in ecological planting of Chinese materia medica and its utilization. China Journal of Chinese materia Medica 45, 2002-2008.
| Crossref | Google Scholar |

Wang S, Chen K, Zhang J, et al. (2022) Genome-wide characterization of MATE family members in Cucumis melo L. and their expression profiles in response to abiotic and biotic stress. Horticultural Plant Journal 8, 474-488.
| Crossref | Google Scholar |

Wen W, Alseekh S, Fernie AR (2020) Conservation and diversification of flavonoid metabolism in the plant kingdom. Current Opinion in Plant Biology 55, 100-108.
| Crossref | Google Scholar |

Xiao F, Zhao Y, Wang X, Sun Y (2023) Comparative transcriptome analysis of Gleditsia sinensis thorns at different stages of development. Plants 12, 1456.
| Crossref | Google Scholar |

Yamasaki K, Motomura Y, Yagi Y, Nomura H, Kikuchi S, Nakai M, Shiina T (2013) Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana. Plant Signaling & Behavior 8, e23603.
| Crossref | Google Scholar |

Yang S, Jiang Y, Xu L, Shiratake K, Luo Z, Zhang Q (2016) Molecular cloning and functional characterization of DkMATE1 involved in proanthocyanidin precursor transport in persimmon (Diospyros kaki Thunb.) fruit. Plant Physiology and Biochemistry 108, 241-250.
| Crossref | Google Scholar |

Yazaki K, Sugiyama A, Morita M, Shitan N (2008) Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochemistry Reviews 7, 513-524.
| Crossref | Google Scholar |

Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiology 149, 297-305.
| Crossref | Google Scholar |

Yu L, Liu D, Chen S, Dai Y, Guo W, Zhang X, Wang L, Ma S, Xiao M, Qi H, Xiao S, Chen Q (2020) Evolution and expression of the membrane attack complex and perforin gene family in the Poaceae. International Journal of Molecular Sciences 21, 5736.
| Crossref | Google Scholar |

Zhang J, Xu H, Zhou X, Chen J, Wang Y, Peng X (2010) Expression analysis of OsMATE in rice under abiotic stresses. Journal of Tropical and Subtropical Botany 18, 435-439 [In Chinese].
| Google Scholar |

Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L (2014) A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Molecular Plant 7, 1522-1532.
| Crossref | Google Scholar |

Zhao J, Dixon RA (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. The Plant Cell 21, 2323-2340.
| Crossref | Google Scholar |

Zhao J, Dixon RA (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends in Plant Science 15, 72-80.
| Crossref | Google Scholar |

Zhao J, Huhman D, Shadle G, et al. (2011) MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. The Plant Cell 23, 1536-1555.
| Crossref | Google Scholar |