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Tomato sugar transporter genes associated with mycorrhiza and phosphate

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Abstract

In arbuscular mycorrhizal (AM) symbiosis, there is a reciprocal nutrient exchange between symbiotic partners. AM fungi assist the plants with uptake of mineral nutrients from the soil, especially phosphate (Pi). The host plants, in return, provide the fungi with sugar. In contrast to the studies on the symbiotic transport of Pi in arbuscular mycorrhiza, there have been few investigations devoted specifically to sugar transport in AM symbiosis. Using reverse transcriptase PCR (RT-PCR), we analyzed the effects of mycorrhiza and Pi on the expression of seven putative sugar transporter genes in tomato plants. The expression of LeSUT1 and LeHT2, classified, respectively, as putative sucrose and hexose transporter genes, were down-regulated in the roots inoculated with AM fungi Glomus caledonium or Glomus intraradices. Unexpectedly, the expression of LeST3, a putative monosaccharide transporter gene, was decreased by inoculation of Glomus caledonium, but was enhanced by inoculation of Glomus intraradices in both the roots and leaves. High-Pi in the tomato decreased the expression of LeHT2 and LeST3 in the roots, and enhanced that of LeHT2 in the leaves. The contradictory regulation of the expression of LeST3 in the AM symbiosis indicates that different interaction may take place during mycorrhizal colonization, and a quite complicated regulation of expression of the sugar transporter genes exist in mycorrhizal tomato.

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Abbreviations

G. caledonium :

Glomus caledonium

G. intraradices :

Glomus intraradices

AM:

Arbuscular mycorrhiza

AMF:

Arbuscular mycorrhiza fungi

SUT:

Sucrose transporter

HT:

Hexose transporter

ST:

Sugar transporter

FW:

Fresh weight

References

  • Aoki N, Scofield GN, Wang XD, Patrick JW, Offler CE, Furbank RT (2004) Expression and localisation analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues. Planta 219:176–184

    Article  PubMed  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    Article  PubMed  CAS  Google Scholar 

  • Balestrini R, Lanfranco L (2006) Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16:509–524

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26

    Article  PubMed  CAS  Google Scholar 

  • Chen A, Hu J, Sun S, Xu G (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol 173:817–831

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Rodriguez S, Pozo MJ, Azcon-Aguilar C (2005) Expression of a tomato sugar transporter is increased in leaves of mycorhizal or Phytophthora parasitica-infected plants. Mycorrhiza 15:489–496

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Glassop D, Smith S, Smith F (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698

    Article  PubMed  CAS  Google Scholar 

  • Gogarten JP, Bentrup FW (1989) Substrate specificity of the hexose carrier in the plasma membrane of chenopodium suspension cells probes by transmembrane exchange diffusion. Planta 178:52–60

    Article  CAS  Google Scholar 

  • Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kuhn C (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45:180–192

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provides insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Pumplin N, Harrison MJ (2007a) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007b) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725

    Article  PubMed  CAS  Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    Article  PubMed  CAS  Google Scholar 

  • Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Localization and turnover of sucrose transporters in enucleate sieve elements indicate macromolecular trafficking. Science 275:1298–1300

    Article  PubMed  Google Scholar 

  • Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of the arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123

    Article  PubMed  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250

    Article  PubMed  CAS  Google Scholar 

  • Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37

    Article  PubMed  CAS  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  PubMed  CAS  Google Scholar 

  • Riesmeier JW, Willmitzer L, Frommer WB (1992) Isolation and characterization of a sucrose carrier cDNA from spinach by function expression in yeast. EMBO J 11:4705–4713

    PubMed  CAS  Google Scholar 

  • Sauer N, Tanner W (1989) The hexose carrier from Chlorella cDNA cloning of a eukaryotic H+-cotransporter. FEBS Lett 259:43–46

    Article  PubMed  CAS  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Sherson SM, Hemmann G, Wallace G, Forbes S, Germain V, Stadler R, Bechtold N, Sauer N, Smith SM (2000) Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. Plant J 24:849–857

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Truernit E, Stadler R, Baier K, Sauer N (1999) A male gametophyte-specific monosaccharide transporter in Arabidopsis. Plant J 17:191–201

    Article  PubMed  CAS  Google Scholar 

  • Tubbe A, Buckhout TJ (1992) In vitro analysis of the H+-hexose symporter on the plasma membrane of sugar beets (Beta vulgaris L). Plant Physiol 99:945–951

    Article  PubMed  CAS  Google Scholar 

  • Versaw WK, Chiou TJ, Harrison MJ (2002) Phosphate transporters of Medicago truncatula and arbuscular mycorrhizal fungi. Plant Soil 244:239–245

    Article  CAS  Google Scholar 

  • Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer WB (2000) A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell 12:1345–1355

    Article  PubMed  CAS  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  PubMed  CAS  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 

  • Wright DP, Scholes JD, Read DJ, Rolfe SA (2005) European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. New Phytol 167:881–896

    Article  PubMed  CAS  Google Scholar 

  • Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, Raghothama KG, Levy AA, Silber A (2007) Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J Exp Bot 58:2491–501

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work is supported by the National Science Foundation of China (30471037; 30571108), the 863 project (2006AA10Z134) and the Basic Research Program of Jiangsu province in China (BK2006136).

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Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Lei Ge, Shubin Sun, Aiqun Chen & Guohua Xu

  2. Institute of Plant Sciences, The Agricultural Research Organization of Israel, Volcani Center, P.O. Box 6, Bet Dagan, 50250, Israel

    Yoram Kapulnik

Authors
  1. Lei Ge
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  2. Shubin Sun
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  3. Aiqun Chen
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  4. Yoram Kapulnik
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  5. Guohua Xu
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Correspondence to Shubin Sun or Guohua Xu.

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Ge, L., Sun, S., Chen, A. et al. Tomato sugar transporter genes associated with mycorrhiza and phosphate. Plant Growth Regul 55, 115–123 (2008). https://doi.org/10.1007/s10725-008-9266-7

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