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Expression of a tomato sugar transporter is increased in leaves of mycorrhizal or Phytophthora parasitica-infected plants

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Abstract

A full-length cDNA clone (LeST3), encoding a putative tomato sugar transporter, was isolated from mycorrhizal roots by using a PCR-based approach. Based on sequence similarity, conserved motifs and predicted membrane topology, LeST3 was classified as a putative monosaccharide transporter of the sugar transporter subgroup of the major facilitator superfamily. Southern blot analysis showed that LeST3 represents a single-copy gene in tomato. To investigate its function, LeST3 was expressed in a hexose transport-deficient mutant of Saccharomyces cerevisiae. Although LeST3 was correctly transcribed in yeast, it did not restore growth on hexoses of the S. cerevisiae mutant. LeST3 gene expression was increased in the leaves of plants colonised by the arbuscular mycorrhizal (AM) fungi Glomus mosseae or Glomus intraradices and in those of plants infected with the root pathogen Phytophthora parasitica. These data suggest that LeST3 plays a role in the transport of sugars into the sink tissues and responds to the increased demand for carbohydrates exerted by two AM fungi and by a root pathogen to cope with the increased metabolic activity of the colonised/infected tissues or to supply carbohydrates to the AM fungus.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Baker CJ, Orlandi EW, Deahl KL (2000) Oxygen metabolism in plant/bacteria interactions: characterization of oxygen uptake response of plant suspension cells. Physiol Mol Plant Pathol 57:159–167

    Google Scholar 

  • Barker L, Kühn C, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153–1164

    Article  CAS  PubMed  Google Scholar 

  • Benabdellah K, Azcón-Aguilar C, Ferrol N (1999) Plasma membrane ATPase and H+ transport activities in microsomal membranes from mycorrhizal tomato roots. J Exp Bot 337:1343–1349

    Google Scholar 

  • Blee KA, Anderson AJ (2002) Transcripts for genes encoding soluble acid invertase and sucrose synthase accumulate in root tip and cortical cells containing mycorrhizal arbuscules. Plant Mol Biol 50:197–211

    Google Scholar 

  • Büttner M, Sauer N (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465:263–274

    PubMed  Google Scholar 

  • Chiou T-J, Bush DR (1996) Molecular cloning, immunochemical localization to the vacuole, and expression in transgenic yeast and tobacco of a putative sugar transporter from sugar beet. Plant Physiol 110:511–520

    Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci U S A 81:1991–1995

    Google Scholar 

  • Douds DD Jr, Johnson CR, Koch KE (1988) Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol 86:491–496

    Google Scholar 

  • Felstein J (1993) PHYLIP, Version 3.5. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Ferrol N, Gianinazzi S, Gianinazzi-Pearson V (2002a) Arbuscular mycorrhiza induced ATPases and membrane nutrient transport mechanisms. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture: from genes to bioproducts. Birkhäuser, Basel, pp 113–122

    Google Scholar 

  • Ferrol N, Pozo MJ, Antelo M, Azcón-Aguilar C (2002b) Arbuscular mycorrhizal symbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants. J Exp Bot 53:1683–1687

    Google Scholar 

  • Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829

    Google Scholar 

  • Gear ML, McPhillips ML, Patrick JW, McCurdy DW (2000) Hexose transporters of tomato: molecular cloning, expression analysis and functional characterization. Plant Mol Biol 44:687–697

    Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular infection in roots. New Phytol 84:489–500

    Google Scholar 

  • Graham JH (2000) Assessing costs of arbuscular mycorrhizal symbiosis agroecosystems fungi. In: Podila GK, Douds DD Jr (eds) Current advances in mycorrhizae research. APS, St. Paul, pp 127–140

    Google Scholar 

  • Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular–arbuscular (VA) mycorrhizal associations. Plant J 9:491–503

    Article  CAS  PubMed  Google Scholar 

  • Heiland S, Radovanovic N, Höfer M, Winderickx J, Lichtenberg H (2000) Multiple hexose transporters of Schizosaccharomyces pombe. J Bacteriol 182:2153–2162

    Google Scholar 

  • Herbers K, Meuwly P, Frommer WB, Metraux JP, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803

    Google Scholar 

  • Hewitt EJ (1952) Sand and water culture methods used in the study of plant nutrition. In: Technical communication, vol. 22. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, UK

    Google Scholar 

  • Ho I, Trappe JM (1973) Translocation of 14C from Festuca plants to their endomycorrhizal fungi. Nature 244:311–327

    Google Scholar 

  • Hohnjec N, Perlick AM, Pühler A, Küster H (2003) The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in infected regions of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol Plant-Microb Interact 16:903–915

    Google Scholar 

  • Jennings DH (1995) The physiology of fungal nutrition. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Kiyosue T, Abe H, Yamaguchi-Shinozake K, Shinozaki K (1998) ERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter. Biochim Biophys Acta 1370:187–191

    Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Google Scholar 

  • Kyte J, Doolitle RF (1982) A simple method for displaying the hydrophobic character of a protein. J Mol Biol 157:105–132

    CAS  PubMed  Google Scholar 

  • Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372

    Article  CAS  PubMed  Google Scholar 

  • Lemoine R (2000) Sucrose transporters in plants: update on function and structure. Biochim Biophys Acta 1465:246–262

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \( 2^{{ - \Delta \Delta c_{{\text{t}}} }} \)method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20

    CAS  PubMed  Google Scholar 

  • Madi L, McBride SA, Bailey LA, Ebbole DJ (1997) rco-3, a gene involved in glucose transport and conidation in Neurospora crassa. Genetics 146:499–508

    Google Scholar 

  • Minet M, Dufour M-E, Lacroute F (1992) Complementation of Sacharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J 2:417–422

    Google Scholar 

  • Moerschbacher B, Mendgen K (2000) Structural aspects of defense. In: Slusarenko AJ, Fraser RS, van Loon LC (eds) Mechanisms of resistance to plant diseases. Kluwer, Dordrecht, pp 231–277

    Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    CAS  PubMed  Google Scholar 

  • Nehls U, Wiese J, Guttengerger M, Hampp R (1998) Carbon allocation in ectomycorrhizas: identification and expression analysis of an Amanita muscaria monosaccharide transporter. Mol Plant-Microb Interact 11:167–176

    Google Scholar 

  • Page RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85:2444–2448

    Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–160

    Google Scholar 

  • Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1998) Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophthora parasitica. J Exp Bot 49:1729–1739

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1999) β-1,3 glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141:149–157

    Article  CAS  Google Scholar 

  • Pozo MJ, Slezack-Deschaumes S, Dumas-Gaudot E, Gianinazzi S, Azcón-Aguilar C (2002) Plant defense responses induced by arbuscular mycorrhizal fungi. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture: from genes to bioproducts. Birkhäuser, Basel, pp 103–112

    Google Scholar 

  • Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jahn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279

    Google Scholar 

  • Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediate carbon metabolism in vesicular–arbuscular leek. Plant Physiol 108:2979–2995

    Google Scholar 

  • Smith SE, Dickson S, Smith FA (2001) Nutrient transfer in arbuscular mycorrhizas: how are fungal and plant processes integrated? Aust J Plant Physiol 28:683–694

    Google Scholar 

  • Solaiman MD, Saito M (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol 136:533–538

    Google Scholar 

  • Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–497

    Article  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  Google Scholar 

  • Tinker PB, Durall DM, Jones MD (1994) Carbon use in mycorrhizas: theory and sample calculations. New Phytol 128:115–122

    CAS  Google Scholar 

  • Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8:2169–2182

    Article  CAS  PubMed  Google Scholar 

  • Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci U S A 98:8133–8138

    Google Scholar 

  • Wieczorke R, Krampe S, Weierstall T, Friedel K, Hollenberg CP, Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464:123–128

    Article  CAS  PubMed  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    Article  Google Scholar 

  • Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891

    Article  Google Scholar 

  • Yu J, Chang P-K, Bhatnagar D, Cleveland TE (2000) Cloning of a sugar utilization gene cluster in Aspergillus parasiticus. Biochim Biophys Acta 1493:211–214

    Google Scholar 

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Acknowledgements

We thank Dr. Boles (University of Heinrich-Heine, Düsseldorf, Germany) for providing the S. cerevisiae strain EBY.VW4000 and Dr. Barea for helpful comments. We are grateful to Ms. Custodia Cano for excellent technical assistance. This research was supported by CICyT (AGL2003-01551), Spain.

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Correspondence to N. Ferrol.

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García-Rodríguez, S., Pozo, M.J., Azcón-Aguilar, C. et al. Expression of a tomato sugar transporter is increased in leaves of mycorrhizal or Phytophthora parasitica-infected plants. Mycorrhiza 15, 489–496 (2005). https://doi.org/10.1007/s00572-005-0354-5

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  • DOI: https://doi.org/10.1007/s00572-005-0354-5

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