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Genome-wide identification and comparative analysis of MATE gene family in Cucurbitaceae species and their regulatory role in melon (Cucumis melo) under salt stress

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Abstract

The multidrug and toxic compound extrusion (MATE) protein family includes a primeval gene family of secondary transporters that export toxins, extrude metabolites, and participate in plant defense mechanisms. However, lack of information regarding the MATE gene family in Cucurbitaceae, a comprehensive genome-wide analysis of the MATE family was carried out in four Cucurbitaceae species (Cucumis melo, Cucumis sativus, Cucurbita pepo, and Lagenaria siceraria), and 174 MATE genes were identified. Phylogenetic and structural analysis revealed that the Cucurbitaceae MATE transporters family could be further classified into seven subgroups (A–G). GO annotation-based subcellular localization analysis predicted that most of the MATE gene family members localized on the plasma membrane. Moreover, conserved motifs and gene structure (intron/exon) analysis revealed the functional divergence between clades. Transposed duplication events have played a key role in the expansion and evolution of the MATE gene family in Cucumis melo. Cis-acting elements analysis of MATE family genes revealed that these could be targeted by a diverse set of trans-acting factors involving the MATE gene family to manage diverse stress conditions. The Chromosomal localization and molecular characteristics (weight, length, and pI) were performed using numerous bioinformatics tools. Intraspecies microsynteny analysis demonstrated that maximum orthologous genes were found between A. thaliana, C. pepo, C. lanatus, and L. siceraria. Further, functional analysis of microRNAs demonstrated miRNAs are involved in the growth and regulation of MATE genes. Finally, eleven candidates MATE genes were selected randomly, and their expression analysis was carried out via qRT-PCR at 0 h and after 24 h of salt stress. Furthermore, transient CmMATE expression in Arabidopsis thaliana protoplasts showed that protein localized on the plasma membrane. This study provides insights into the functional analysis of the MATE gene family in Cucurbitaceae species and laid down the basic knowledge to explore the role and mechanism of the MATE gene family to cope with severe salt stress conditions.

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References

  • Abdullah M, Cao Y, Cheng X, Meng D, Chen Y, Shakoor A, Gao J, Cai Y (2018) The sucrose synthase gene family in Chinese pear (Pyrus bretschneideri Rehd.): structure, expression, and evolution. Molecules 23:1144

    Article  PubMed Central  CAS  Google Scholar 

  • Ali E, Saand MA, Khan AR, Shah JM, Feng S, Ming C, Sun P, (2020) Genome‐wide identification and expression analysis of detoxification efflux carriers (DTX) genes family under abiotic stresses in flax. Physiol Plant 171(4):483–501

  • Arshad M, Gruber MY, Wall K, Hannoufa A (2017) An insight into microRNA156 role in salinity stress responses of alfalfa. Front Plant Sci 8:356

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattarai S, Biswas D, Fu Y-B, Biligetu B (2020) Morphological, physiological, and genetic responses to salt stress in alfalfa: a review. Agronomy 10:577

    Article  CAS  Google Scholar 

  • Cao Y, Han Y, Meng D, Li D, Jin Q, Lin Y, Cai Y (2016) Structural, evolutionary, and functional analysis of the class III peroxidase gene family in Chinese pear (Pyrus bretschneideri). Front Plant Sci 7:1874

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Wang L, Liu D, Ma S, Dai Y, Zhang X, Wang Y, Hu T, Xiao M, Zhou Y (2020b) Identification and expression of the multidrug and toxic compound extrusion (MATE) gene family in Capsicum annuum and Solanum tuberosum. Plants 9:1448

    Article  CAS  PubMed Central  Google Scholar 

  • da Silva FHA, de Morais PLD, da Silva Dias N, de Sousa Nunes GH, de Morais MB, Melo MF, de Albuquerque Nascimento MT (2021) Physiological aspects of melon (Cucumis melo L.) as a function of salinity. J Plant Growth Regul 40:1298–1314

    Article  CAS  Google Scholar 

  • Dobritzsch M, Lübken T, Eschen-Lippold L, Gorzolka K, Blum E, Matern A, Marillonnet S, Böttcher C, Dräger B, Rosahl S (2016) MATE transporter-dependent export of hydroxycinnamic acid amides. Plant Cell 28:583–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong B, Niu L, Meng D, Song Z, Wang L, Jian Y, Fan X, Dong M, Yang Q, Fu Y (2019) Genome-wide analysis of MATE transporters and response to metal stress in Cajanus cajan. J Plant Interact 14:265–275

    Article  CAS  Google Scholar 

  • Dos Santos AL, Chaves-Silva S, Yang L, Maia LGS, Chalfun-Júnior A, Sinharoy S, Zhao J, Benedito VA (2017) Global analysis of the MATE gene family of metabolite transporters in tomato. BMC Plant Biol 17:1–13

    Article  CAS  Google Scholar 

  • Fan K, Wang M, Miao Y, Ni M, Bibi N, Yuan S, Li F, Wang X (2014) Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. PLoS ONE 9:e111837

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Franzoni G, Cocetta G, Trivellini A, Ferrante A (2020) Transcriptional regulation in rocket leaves as affected by salinity. Plants 9:20

    Article  CAS  Google Scholar 

  • Gani U, Sharma P, Tiwari H, Nautiyal AK, Kundan M, Wajid MA, Kesari R, Nargotra A, Misra P (2021) Comprehensive genome-wide identification, characterization, and expression profiling of MATE gene family in Nicotiana tabacum. Gene 783: 145554

  • Gao L-W, Yang S-L, Wei S-W, Huang D-F, Zhang Y-D (2020a) Supportive role of the Na+ transporter CmHKT1; 1 from Cucumis melo in transgenic Arabidopsis salt tolerance through improved K+/Na+ balance. Plant Mol Biol 103:561–580

    Article  CAS  PubMed  Google Scholar 

  • Gao LW, Yang SL, Wei SW, Huang DF, Zhang YD (2020b) Supportive role of the Na+ transporter CmHKT1; 1 from Cucumis melo in transgenic Arabidopsis salt tolerance through improved K+/Na+ balance. Plant Mol Biol 103(4):561–580

  • Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci 109:11872–11877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geer LY, Domrachev M, Lipman DJ, Bryant SH (2002) CDART: protein homology by domain architecture. Genome Res 12:1619–1623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Ibeas D, Blanca J, Donaire L, Saladié M, Mascarell-Creus A, Cano-Delgado A, Garcia-Mas J, Llave C, Aranda MA (2011) Analysis of the melon (Cucumis melo) small RNAome by high-throughput pyrosequencing. BMC Genom 12:1–20

    Article  CAS  Google Scholar 

  • Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Huang J, An W, Wang K, Jiang T, Ren Q, Liang W, Wang H (2019) Expression profile analysis of MATE gene family in rice. Biol Plant 63:556–564

    CAS  Google Scholar 

  • Huang Y, He G, Tian W, Li D, Meng L, Wu D, He T (2021) Genome-wide identification of MATE gene family in potato (Solanum tuberosum L.) and expression analysis in heavy metal stress. Front Genet 12:672

  • Isayenkov SV, Maathuis FJ (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80

  • Jo B-S, Choi SS (2015) Introns: the functional benefits of introns in genomes. Genom Inform 13:112

    Article  Google Scholar 

  • Julião MH, Silva SR, Ferro JA, Varani AM (2020) A genomic and transcriptomic overview of MATE, ABC, and MFS transporters in Citrus sinensis interaction with Xanthomonas citri subsp. citri. Plants 9:794

    Article  PubMed Central  CAS  Google Scholar 

  • Kaur A, Pati PK, Pati AM, Nagpal AK (2017) In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS ONE 12:e0184523

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuroda T, Tsuchiya T (2009) Multidrug efflux transporters in the MATE family. Biochimica Biophysica Acta (BBA) Proteins Proteom 1794:763–768

    Article  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2019) Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43(D1):D257–D260

  • 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. J Biol Chem 277:5360–5368

    Article  CAS  PubMed  Google Scholar 

  • Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Meng H, Xing H, Liang L, Zhao X, Luo K (2017) Genome-wide analysis of MATE transporters and molecular characterization of aluminum resistance in Populus. J Exp Bot 68:5669–5683

    Article  CAS  PubMed  PubMed Central  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 Genom 17:223

    Article  CAS  Google Scholar 

  • Liu Y, Cui J, Zhou X, Luan Y, Luan F (2020) Genome-wide identification, characterization and expression analysis of the TLP gene family in melon (Cucumis melo L.). Genomics 112:2499–2509

    Article  CAS  PubMed  Google Scholar 

  • Long-Tang H, Li-Na Z, Li-Wei G, Anne-Aliénor V, Hervé S, Yi-Dong Z (2018) Constitutive expression of CmSKOR, an outward K+ channel gene from melon, in Arabidopsis thaliana involved in saline tolerance. Plant Sci 274:492–502

    Article  PubMed  CAS  Google Scholar 

  • Lu P, Magwanga RO, Guo X, Kirungu JN, Lu H, Cai X, Zhou Z, Wei Y, Wang X, Zhang Z (2018) 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 Genes Genomes Genet 8:2483–2500

    CAS  Google Scholar 

  • Lu P, Magwanga RO, Kirungu JN, Hu Y, Dong Q, Cai X, Zhou Z, Wang X, Zhang Z, Hou Y (2019) Overexpression of cotton a DTX/MATE gene enhances drought, salt, and cold stress tolerance in transgenic Arabidopsis. Front Plant Sci 10:299

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma Q, Yi R, Li L, Liang Z, Zeng T, Zhang Y, Huang H, Zhang X, Yin X, Cai Z (2018) GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana. BMC Plant Biol 18:1–10

    Article  CAS  Google Scholar 

  • Maathuis FJ (2006) The role of monovalent cation transporters in plant responses to salinity. J Exp Bot 57:1137–1147

    Article  CAS  PubMed  Google Scholar 

  • Magwanga RO, Lu P, Kirungu JN, Lu H, Wang X, Cai X, Zhou Z, Zhang Z, Salih H, Wang K (2018) Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton. BMC Genet 19:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manzoor MA, Cheng X, Li G, Su X, Abdullah M, Cai Y (2020) Gene structure, evolution and expression analysis of the P-ATPase gene family in Chinese pear (Pyrus bretschneideri). Comput Biol Chem 88:107346

  • Manzoor MA, Guohui L, Muhammad A, Han W, Wenlong H, Yang Z, Xinya W, Yu Z, Xiaofeng F, Qing J (2021) Genome‐wide investigation and comparative analysis of MATE gene family in Rosaceae species and their regulatory role in abiotic stress responses in Chinese pear (Pyrus bretschneideri). Physiol Plant 173(3):1163–1178

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) 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 34:137–148

    Article  CAS  PubMed  Google Scholar 

  • Nimmy M, Kumar V, Singh A, Jain P, Srinivasan R (2015) 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 75:478–485

    Article  CAS  Google Scholar 

  • Qiao X, Yin H, Li L, Wang R, Wu J, Wu J, Zhang S (2018) Different modes of gene duplication show divergent evolutionary patterns and contribute differently to the expansion of gene families involved in important fruit traits in pear (Pyrus bretschneideri). Front Plant Sci 9:161

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, Zhang S, Paterson AH (2019) Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Biol 20:1–23

    Article  Google Scholar 

  • Qiao C, Yang J, Wan Y, Xiang S, Guan M, Du H, Tang Z, Lu K, Li J, Qu C (2020) A genome-wide survey of MATE transporters in Brassicaceae and unveiling their expression profiles under abiotic stress in rapeseed. Plants 9:1072

    Article  CAS  PubMed Central  Google Scholar 

  • Riaz MW, Lu J, Shah L, Yang L, Chen C, Mei XD, Xue L, Manzoor MA, Abdullah M, Rehman S (2021) Expansion and molecular characterization of AP2/ERF gene family in wheat (Triticum aestivum L.). Front Genet 12:632155

  • Saier Jr MH, Paulsen IT (2001) Phylogeny of multidrug transporters. In: Seminars in cell & developmental biology, vol 12. Academic Press. Elsevier, pp 205–213

  • Sazegari S, Niazi A, Ahmadi FS (2015) A study on the regulatory network with promoter analysis for Arabidopsis DREB-genes. Bioinformation 11:101

    Article  PubMed  PubMed Central  Google Scholar 

  • Shahid SA, Zaman M, Heng L (2018) Soil salinity: historical perspectives and a world overview of the problem. In: Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. Springer. Cham, pp 43–53

  • Sharma A, Ruiz-Manriquez LM, Serrano-Cano FI, Reyes-Pérez PR, Tovar Alfaro CK, Barrón Andrade YE, Hernández Aros AK, Srivastava A, Paul S (2020) Identification of microRNAs and their expression in leaf tissues of Guava (Psidium guajava L.) under salinity stress. Agronomy 10:1920

    Article  CAS  Google Scholar 

  • Sheshadri S, Nishanth M, Simon B (2016) Stress-mediated cis-element transcription factor interactions interconnecting primary and specialized metabolism in planta. Front Plant Sci 7:1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Si W, Hang T, Guo M, Chen Z, Liang Q, Gu L, Ding T (2019) Whole-genome and transposed duplication contributes to the expansion and diversification of TLC genes in maize. Int J Mol Sci 20:5484

    Article  CAS  PubMed Central  Google Scholar 

  • Singroha G, Sharma P, Sunkur R (2021) Current status of microRNA‐mediated regulation of drought stress responses in cereals. Physiol Plant 172(3):1808–1821

  • Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643

    Article  CAS  PubMed  Google Scholar 

  • Tian W, Hou C, Ren Z, Pan Y, Jia J, Zhang H, Bai F, Zhang P, Zhu H, He Y (2015) A molecular pathway for CO2 response in Arabidopsis guard cells. Nat Commun 6:1–10

    Article  CAS  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. Sci Rep 4:3964

    Article  PubMed  PubMed Central  CAS  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. J Exp Bot 70:4643–4656

    Article  CAS  PubMed  Google Scholar 

  • Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117

    Article  CAS  PubMed  Google Scholar 

  • Wahl MC, Will CL, Lührmann R (2009) The spliceosome: design principles of a dynamic RNP machine. Cell 136:701–718

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee T-H, Jin H, Marler B, Guo H (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49–e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R, Liu X, Liang S, Ge Q, Li Y, Shao J, Qi Y, An L, Yu F (2015a) A subgroup of MATE transporter genes regulates hypocotyl cell elongation in Arabidopsis. J Exp Bot 66:6327–6343

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Feng L, Zhu Y, Li Y, Yan H, Xiang Y (2015b) Comparative genomic analysis of the WRKY III gene family in populus, grape, arabidopsis and rice. Biol Direct 10:1–27

    Article  CAS  Google Scholar 

  • Wang L, Bei X, Gao J, Li Y, Yan Y, Hu Y (2016a) The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana. BMC Plant Biol 16:207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang L, Bei X, Gao J, Li Y, Yan Y, Hu Y (2016b) The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana. BMC Plant Biol 16:1–19

    Article  CAS  Google Scholar 

  • Wang L, Zhang L, Chen J, Huang D, Zhang Y (2016c) Physiological analysis and transcriptome comparison of two muskmelon (Cucumis melo L.) cultivars in response to salt stress. Genet Mol Res 15:1–18

    Article  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. Plant J 90:79–95

    Article  CAS  PubMed  Google Scholar 

  • Wani SH, Kumar V, Khare T, Guddimalli R, Parveda M, Solymosi K, Suprasanna P, Kishor PK (2020) Engineering salinity tolerance in plants: progress and prospects. Planta 251:1–29

    Article  CAS  Google Scholar 

  • Wei H, Wang P, Chen J, Li C, Wang Y, Yuan Y, Fang J, Leng X (2020) Genome-wide identification and analysis of B-BOX gene family in grapevine reveal its potential functions in berry development. BMC Plant Biol 20:1–19

    Article  CAS  Google Scholar 

  • Wu F-H, Shen S-C, Lee L-Y, Lee S-H, Chan M-T, Lin C-S (2009) Tape-Arabidopsis Sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods 5:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu X, Li R, Shi J, Wang J, Sun Q, Zhang H, Xing Y, Qi Y, Zhang N, Guo Y-D (2014) Brassica oleracea MATE encodes a citrate transporter and enhances aluminum tolerance in Arabidopsis thaliana. Plant Cell Physiol 55:1426–1436

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Zhu P, Kang H, Liu L, Cao Q, Sun J, Dong T, Zhu M, Li Z, Xu T (2020b) High-throughput deep sequencing reveals the important role that microRNAs play in the salt response in sweet potato (Ipomoea batatas L.). BMC Genomics 21:1–16

    Article  Google Scholar 

  • Yang Y, Ahammed GJ, Wan C, Liu H, Chen R, Zhou Y (2019) Comprehensive analysis of TIFY transcription factors and their expression profiles under Jasmonic acid and abiotic stresses in Watermelon. Int J Genom 2019. https://doi.org/10.1155/2019/6813086

  • Yang S, Xiong X, Arif S, Gao L, Zhao L, Shah IH, Zhang Y (2020a) A calmodulin-like CmCML13 from Cucumis melo improved transgenic Arabidopsis salt tolerance through reduced shoot's Na+, and also improved drought resistance. Plant Physiol Biochem 155:271–283

  • Yokosho K, Yamaji N, Fujii-Kashino M, Ma JF (2016) Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice. Plant Cell Physiol 57:976–985

    Article  CAS  PubMed  Google Scholar 

  • Yu L, Liu D, Chen S, Dai Y, Guo W, Zhang X, Wang L, Ma S, Xiao M, Qi H (2020) Evolution and expression of the membrane attack complex and perforin gene family in the poaceae. Int J Mol Sci 21:5736

    Article  CAS  PubMed Central  Google Scholar 

  • Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Ann Rev Plant Biol 71:403–433

  • Zhang H, Zhao F-G, Tang R-J, Yu Y, Song J, Wang Y, Li L, Luan S (2017) Two tonoplast MATE proteins function as turgor-regulating chloride channels in Arabidopsis. Proc Natl Acad Sci 114:E2036–E2045

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Liu X, Yang X, Wu H, Zhu J, Zhang H (2020) miRNA–mRNA integrated analysis reveals roles for miRNAs in a typical halophyte, Reaumuria soongorica, during seed germination under salt stress. Plants 9:351

    Article  CAS  PubMed Central  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. Plant Cell 21:2323–2340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Zhang F, Liu B, Yang S, Xiong X, Hassani D, Zhang Y (2019) CmRAV1 shows differential expression in two melon (Cucumis melo L.) cultivars and enhances salt tolerance in transgenic Arabidopsis plants. Acta Biochim Biophys Sin 51:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Li Y, Qi X, Liu R, Dong J, Jing W, Guo M, Si Q, Xu Z, Li L (2020) Overexpression of V-type H+ pyrophosphatase gene EdVP1 from Elymus dahuricus increases yield and potassium uptake of transgenic wheat under low potassium conditions. Sci Rep 10:1–12

    CAS  Google Scholar 

  • Zhu H, Wu J, Jiang Y, Jin J, Zhou W, Wang Y, Han G, Zhao Y, Cheng B (2016) Genomewide analysis of MATE-type gene family in maize reveals microsynteny and their expression patterns under aluminum treatment. J Genet 95:691–704

    Article  CAS  PubMed  Google Scholar 

  • Zotos P, Papachristoudis G, Roubelakis MG, Michalopoulos I, Pappa KI, Anagnou NP, Kossida S (2008) GOmir: a stand-alone application for human microRNA target analysis and gene ontology clustering. In: 2008 8th IEEE international conference on bioinformatics and bioengineering. IEEE, pp 1–6

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Acknowledgements

We are thankful to Essa Ali for his help and guidance in result analysis. We thank Qamar Zaman and Ali Raza Khan for their help to analyze the data from q RT PCR.

Funding

The study was financial supported by Shanghai Agriculture Applied Technology Development Program (No. 20180203).

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Authors and Affiliations

  1. School of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, 200240, People’s Republic of China

    Iftikhar Hussain Shah, Irfan Ali Sabir, Fazal Haq, Samiah Arif, Qingliang Niu & Yidong Zhang

  2. School of Life Sciences, Anhui Agricultural University, Hefei, 230036, People’s Republic of China

    Muhammad Aamir Manzoor

  3. Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, People’s Republic of China

    Muhammad Ashraf

  4. Queensland Alliance for Agriculture and Food Innovation, University of Queensland, Brisbane, 4072, Australia

    Muhammad Abdullah

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  1. Iftikhar Hussain Shah
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Contributions

Y.Z supervised and designed the research, I.H.S designed and performed most of the experiments, M.A.M, I.A.S, M.A and M.A contributed to analysis tool, F.H, S.A and Y.S.L assisted in RNA extraction, qRT-PCR and data analysis, Q.N and Y.Z revised, discussed, and finalized the manuscript.

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Correspondence to Yidong Zhang.

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Supplementary Fig.1 Phylogenetic analysis of MATE genes in Cucurbit genome. The tree divided MATE proteins into 7 subgroups (A-G).

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Supplementary Fig.2 Exon-intron structure analyses in Cucurbit Genome. The yellow boxes indicate exons and the black lines indicate introns.

Supplementary Fig.3 Phylogenetic tree with bootstrap values.

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Shah, I.H., Manzoor, M.A., Sabir, I.A. et al. Genome-wide identification and comparative analysis of MATE gene family in Cucurbitaceae species and their regulatory role in melon (Cucumis melo) under salt stress. Hortic. Environ. Biotechnol. 63, 595–612 (2022). https://doi.org/10.1007/s13580-021-00413-3

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  • DOI: https://doi.org/10.1007/s13580-021-00413-3

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