Abstract
A defense-inducible maize gene was discovered through global mRNA profiling analysis. Its mRNA expression is induced by pathogens and defense-related conditions in various tissues involving both resistant and susceptible interactions. These include Cochliobolus heterostrophus and Cochliobolus carbonum infection, ultraviolet light treatment, the Les9 disease lesion mimic background, and plant tissues engineered to express flavonoids or the avirulence gene avrRxv. The gene was named Zm-mfs1 after it was found to encode a protein related to the major facilitator superfamily (MFS) of intregral membrane permeases. It is most closely related to the bacterial multidrug efflux protein family, typified by the Escherichia coli TetA, which are proton motive force antiporters that export antimicrobial drugs and other compounds, but which can be also involved in potassium export/proton import or potassium re-uptake. Other related plant gene sequences in maize, rice, and Arabidopsis were identified, three of which are introduced here. Among this new plant MFS subfamily, the characteristic MFS motif in cytoplasmic TM2-TM3 loop, and the antiporter family motif in transmembrane domain TM5 are both conserved, however the TM7 and the cytoplasmic TM8-TM9 loop are divergent from those of the bacterial multidrug transporters. We hypothesize that Zm-Mfs1 is a prototype of a new class of plant defense-related proteins that could be involved in either of three nonexclusive roles: (1) export of antimicrobial compounds produced by plant pathogens; (2) export of plant-generated antimicrobial compounds; and (3) potassium export and/or re-uptake, as can occur in plant defense reactions.
Similar content being viewed by others
References
Agrios, G.N. 1997. Plant Pathology, 4th ed. Academic Press, San Diego, CA, pp. 635.
Atkinson, M.M., Huang, J.S. and Knopp, J.A. 1985. The hypersensitive reaction of tobacco to Pseudomonas syringae pv. pisi. Activation of a plasmalemma K+/H+ exchange mechanism. Plant Physiol. 79: 843–847.
Alexander, N.J., McCormick, S.P. and Hohn, T.M. 1999. TRI12, a trichothecene efflux pump from Fusarium sporotrichioides: gene isolation and expression in yeast. Mol. Gen. Genet. 261: 977–984.
Brederode, F.T., Linthorst, H.J.M. and Bol, J.F. 1991. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light, and wounding. Plant Mol. Biol. 17: 1117–1126.
Briggs, S.P., Simmons, C.R. and Tossberg, J.T. 1999. Methods for enhancing disease resistance in plants. PCT patent application WO99/43823.
Bruce, W., Folkerts, O., Garnaat, C., Crasta, O., Roth, B. and Bowen, B. 2000. Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. Plant Cell 12: 65–80.
Callahan, T.M., Rose, M.S., Meade, M.J., Ehrenshaft, M. and Upchurch, R.G. 1999. CFP, the putative cercosporin transporter of Cercospora kikuchii, is required for wild type cercosporin production, resistance, and virulence on soybean. Mol. Plant-Microbe Interact. 12: 901–910.
Carrasco, N., Püttner, I.B., Antes, L.M., Lee, J.A., Larigan, J.D., Lolkema, J.S., Roepe, P.D. and Kaback, H.R. 1989. Characterization of site-directed mutants in the lac permease of Escherichia coli. 2. Glutamate-325 replacements. Biochemistry 28: 2533–2539.
Chen, W.P., Chen, P.D., Liu, D.J., Kynast, R., Friebe, B., Velazhahan, R., Muthukrishnan, S. and Gill, B.S. 1999. Development of wheat scab symptoms is delayed in transgenic wheat plants that constitutively express a rice thaumatin-like protein gene. Theor. Appl. Genet. 99: 755–760.
Cheng, J., Hicks, D.B. and Krulwich, T.A. 1996. The purified Bacillus subtilis tetracycline efflux protein TetA(L) reconstitutes both tetracycline-cobalt/H+ and Na+(K+)/H+ exchange. Proc. Natl. Acad. Sci. USA 93: 14446–14451.
Clough, S.J., Fengler, K.A., Yu, I., Lippok, B., Smith, R.K. Jr. and Bent, A.F. 2000. The Arabidopsis dnd1 ‘defense, no death’ gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl. Acad. Sci. USA 97: 9323–9328.
Clarke, J.D., Liu, Y., Klessig, D.F. and Dong, X. 1998. Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant arabidopsis cpr6–1 mutant. Plant Cell 10: 557–569.
Del Sorbo, G., Schoonbeek, H.-J. and De Waard, M.A. 2000. Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet. Biol. 30: 1–15.
Didierjean, L., Frendo, P., Nasser, W., Genot, G., Burkhard, J. and Marivet, G. 1996. Heavy-metal-responsive genes in maize: Identification and comparison of their expression upon various forms of abiotic stress. Planta 199: 1–8.
Diener, A.C., Gaxiola, R.A. and Fink, G.R. 2001. Arabidopsis ALF5, a multidrug efflux transporter family member, confers resistance to toxins. Plant Cell 13: 1625–1637.
Ditty, J.L. and Harwood, C.S. 1999. Conserved cytoplasmic loops are important for both the transport and chemotaxis functions of PcaK, a protein from Pseudomonas putida with 12 membranespanning regions. J. Bact. 181: 5068–5074.
Eckert, B. and Beck, C.F. 1989. Overproduction of transposon Tn10-encoded tetracycline resistance protein results in cell death and loss of membrane potential. J. Bact. 171: 3557–3559.
Esnault, R., Buffard, D., Breda, C., Sallaud, C., El-Turk, J. and Kondorosi, A. 1993. Pathological and molecular characterizations of alfalfa interactions with compatible and incompatible bacteria, Xanthomonas campestris pv. alfalfae and Pseudomonas syringae pv. pisi. Mol. Plant-Microbe Interact. 6: 655–664.
Frey, M., Chomet, P., Glawischnig, E., Stettner, C., Gruen, S., Winklmair, A., Eisenriech, W., Bacher, A., Meeley, R.B., Briggs, S.P., Simcox, K. and Gierl, A. 1997. Analysis of a chemical plant defense mechanism in grasses. Science 277: 696–699.
Grotewold, E., Chamberlin, M., Snook, M., Siame, B., Butler, L., Swenson, J., Maddock, S., St. Clair, G. and Bowen, B. 1998. Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10: 721–740.
Guffanti, A.A., Cheng, J. and Krulwich, T.A. 1998. Electrogenic antiport activities of the gram-positive Tet proteins include a Na+(K+)/K+ mode that mediates net K+ uptake. J. Biol. Chem. 272: 26447–26454.
Hammond-Kosack, K. and Jones, J.D.G. 2000. Responses to plant pathogens. In: B. Buchanan, W. Guissem and R. Jones (Eds.) Biochemistry and Molecular Biology of Plants, American Society of Plant Physiologists, Rockville, MD, pp. 1102–1156.
Hofmann, K. and Stoffel, W. 1993. TMbase: a database of membrane spanning proteins segments. Biol. Chem. 374: 166.
Hoisington, D.A. 1986. An update on lesion mutants. Maize Genet. Coop. News Lett. 60: 50–51.
Jabs, T., Tschöpe, M., Colling, C., Hahlbrock, K. and Scheel, D. 1997. Elicitor-stimulated ion fluxes and O2-from the oxidative burst are essential counterparts in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA 94: 4800–4805.
Johal G.S. and Briggs, S.P. 1992. Reductase activity encoded by the HM1 disease resistance gene in maize. Science 258: 985–987.
Kimura, T. and Yamaguchi, A. 1996. Asp-285 of the metaltetracycline/H+ antiporter of Escherichia coli is essential for substrate binding. FEBS Lett. 388: 50–52.
Kochian, L.V. 2000. Molecular physiology of mineral nutrient acquisition, transport and utilization. In: B. Buchanan, W. Guissem, R. Jones (Eds.) Biochemistry and Molecular Biology of Plants, American Society of Plant Physiologists, Rockville, MD, pp. 1204–1249.
Koes, R.E., Quattrocchio, F. and Mol, J.N.M. 1994. The flavonoid biosynthetic pathway in plants: function and evolution. Bioessays 16: 123–132.
Lee, E.A., Byrne, P.F., McMullen, M.D., Snook, M.E., Wiseman, B.R., Widstrom, N.W. and Coe, E.H. 1998. Genetic mechanisms underlying apimaysin and maysin synthesis and corn earworm antibiosis in maize (Zea mays L.). Genetics 149: 1997–2006.
Lee, J.A., Püttner, I.B. and Kaback, H.R. 1989. Effect of distance and orientation between arginine-302, histidine-322, and glutamate-325 on the activity of lac permease from Escherichia coli. Biochemistry 28: 2540–2544.
Lemoine, R. 2000. Sucrose transporters in plants: update on function and structure. Biochim. Biophys. Acta 1465: 246–262.
Maiden, N.C.J., Davis, E.O., Baldwin, S.A., Moore, D.C.M. and Henderson, P.J.F. 1987. Mammalian and bacterial sugar transport proteins are homologous. Nature 325: 641–643.
Marger, M.D and Saier, M.H. Jr. 1993. A major superfamily of transmembrane facilitators that catalyse uniport, symport, and antiport. Trends Biochem. Sci. 18: 13–20.
Meeley, R.B., Johal, G.S., Briggs, S.P. and Walton, J.D. 1992. A biochemical phenotype for a disease resistance gene of maize. Plant Cell 4: 71–77.
Nadimpalli, R., Yalpani, N., Johal, G.S and Simmons, C.R. 2000. Prohibitins, stomatins, and a family of plant disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. J. Biol. Chem. 38: 29579–29586.
Nelissen, B., DeWachter, R. and Goffeau, A. 1997. Classification of all putative permeases and other membrane plurispanners of the major facilitator superfamily encoded by the complete genome of Saccharomyces cerevisiae. FEMS Microbiol. Rev. 21: 113–134.
Nishizawa, Y., Nishio, Z., Nakazono, K., Soma, M., Nakajima, E., Ugaki, M. and Hibi, T. 1999. Enhanced resistance to blast (Magnaporthe grisea) in transgenic Japonica rice by constitutive expression of rice chitinase. Theor. Appl. Genet. 99: 383–390.
Orth, K., Xu, Z., Mudgett, M.B., Bao, Z.Q., Palmer, L.E., Bliska, J.B., Mangel, W.F., Staskawicz, B. and Dixon, J.E. 2000. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594–1597.
Paulsen, I.T., Sliwinski, M.K. and Saier, M.H. Jr. 1998. Microbial genome analyses: global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities. J. Mol. Biol. 277: 673–592.
Pitkin, J.W., Panaccione, D.G. and Walton, J.D. 1996. A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology 142: 1557–1565.
Püttner, I.B., Sarkar, H.K., Padan, E., Lolkema, J.S. and Kaback, H.R. 1989. Characterization of site-directed mutants in the lac permease of Escherichia coli. 1. Replacement of histidine residues. Biochemistry 28: 2525–2533.
Quirino, B.F., Reiter, W.D. and Amasino, R.D. 2001. On of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol. Biol. 46: 447–457.
Rubin, R.A., Levy, S.B., Henrikson, R.L. and Kezdy, F.J. 1990. Gene duplication in the evolution of the two complementing domains of gram-negative bacterial tetracycline efflux proteins. Gene 87: 7–13.
Scheffer, R.P., Nelson, R.R. and Ullstrup, A.J. 1967. Inheritance of toxin production and pathogenicity in Cochliobolus carbonum and Cochliobolus victoriae. Phytopathology 57: 1288–1291.
Shimkets, R.A., Lowe, D.G., Tai, J.T., Sehl, P., Jin, H., Yang, R., Predki, P.F., Rothberg, B.E., Murtha, M. T., Roth, M.E., Shenoy, S.G., Windemuth, A., Simpson, J.W., Simons, J.F., Daley, M.P., Gold, S.A., McKenna, M.P., Hillan, K., Went, G.T. and Rothberg, J.M. 1999. Gene expression analysis by transcript profiling coupled to a gene database query. Nature Biotechnology 17: 798–803.
Simmons, C.R., Grant, S., Hantke, S., Johal, G.S. and Briggs, S.P. 1998. The maize lethal leaf spot1 mutant has elevated resistance to fungal infection at the leaf epidermis. Mol. Plant-Microbe Interact. 11: 1110–1118.
Simmons, C.R., Grant, S., Altier, D.J, Dowd, P.F., Crasta, O., Folkerts, O. and Yalpani, N. 2001. Maize rhm1 resists Bipolaris maydis by a discrete mechanism involving few differences in PR protein and global mRNA profiles. Mol. Plant-Microbe Interact. 14: 947–54.
Simmons, C.R., Tossberg, J.T., Sandahl, G.A., Marsh, W.A., Dowd, P.F., Duvick, J.P. and Briggs, S.P. 2002. Maize pathogen defense activated by avirulence gene avrRxv. Maize Genet. Coop. Newsl. 76: 40–41.
Smalla, K., Gebhard, F. and Heuer, H. 2000. Antibiotic resistance genes as markers in transgenic plants: risk of horizontal gene transfer? NachrBl. Deut. PflSchutzd. 52: 62–68.
Stapleton, A.E. and Walbot, V. 1994. Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiol. 105: 881–889.
Stravropoulos, T.A. and Strathdee, C.A. 2000. Expression of the tetA(C) tetracycline efflux pump in Escherichia coli confers osmotic sensitivity. FEMS Microbiol. Lett. 190: 147–150.
Sundin, G.W. 2001. Antibiotic resistance affects plant pathogens. Science 291: 2551.
Takemoto, D., Hayashi, M., Doke, N., Nishimura, M. and Kawakita, K. 1999. Molecular cloning of a defense-response-related cytochrome P450 gene from tobacco. Plant Cell Physiol. 40: 1232–1242.
Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.
Trueman, L.J., Richardson, A. and Forde, B.G. 1996. Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Clamydomonas reinhardtii and Aspergillus nidulans. Gene 175: 223–231.
Vad, K., De-Neergaard, E., Madriz-Ordenana, K., Mikkelsen, J.D. and Collinge, D. 1993. Accumulation of defence-related transcripts and cloning of a chitinase mRNA from pea leaves (Pisum sativum L.) inoculated with Ascochyta pisi Lib. Plant Sci. 92: 69–79.
Van Bambeke, F., Balzi, E. and Tulkens, P.M. 2000. Antibiotic efflux pumps. Biochem. Pharmacol. 60: 457–470.
Varela, M.F., Sansom, C.E. and Griffith, J.K. 1995. Mutational analysis and molecular modeling of an amino acid sequence motif conserved in antiporters but not symporters in a transporter superfamily. Mol. Membr. Biol. 12: 313–319.
Wang,W., Guffanti, A.A., Wei, Y., Ito, M. and Krulwich, T.A. 2000. Two types of Bacillus subtilis tetA(L) deletion strains reveal the physiological importance of TetA(L) in K+ acquisition as well as in Na+, alkali, and tetracycline resistance. J. Bact. 182: 2088–2095.
Wang, W., Takezawa, D. and Poovaiah, B.W. 1996. A potato cDNA encoding a homologue of mammalian multidrug-resistant P-glycoprotein. Plant Mol. Biol. 31: 683–687.
Whalen, M.C., Stall, R.E. and Staskawicz, B.J. 1988. Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc. Natl. Acad. Sci. USA 85: 6743–6747.
White, D.G. 1999. Compendium of Corn Diseases, 3rd ed. American Phytopathological Society Press, St. Paul, MN.
Yamaguchi, A., Someya, Y. and Sawai, T. 1992. Metal-tetracyclineproton antiporter of Escherichia coli encoded by transposon TN10. The role of a conserved sequence motif GXXXXRXGRR in a putative cytoplasmic loop between helices 2 and 3. J. Biol. Chem. 267: 19155–19162.
Yamaguchi, A., Kimura, T., Someya, Y. and Sawai, T. 1993. Metaltetracycline proton antiporter of Escherichia coli encoded by transposon Tn10: the structural resemblance and functional difference in the role of the duplicated sequence motif between hydrophobic segments 2 and 3 and segments 8 and 9. J. Biol. Chem. 268: 6496–6504.
Yamaguchi, A., Samejima, T., Kimura, T. and Sawai, T. 1996. His257 is a uniquely important histidine residue for tetracycline/H+ antiport function but not mandatory for full-activity of the transposon Tn10-encoded meta-tetracycline/H+ antiporter. Biochemistry 35: 4359–4364.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Simmons, C.R., Fridlender, M., Navarro, P.A. et al. A maize defense-inducible gene is a major facilitator superfamily member related to bacterial multidrug resistance efflux antiporters. Plant Mol Biol 52, 433–446 (2003). https://doi.org/10.1023/A:1023982704901
Issue Date:
DOI: https://doi.org/10.1023/A:1023982704901