[go: up one dir, main page]
More Web Proxy on the site http://driver.im/
Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Sugar transporters for intercellular exchange and nutrition of pathogens

Nature volume 468, pages 527–532 (2010)Cite this article

Subjects

Abstract

Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Despite broad biological importance, the identity of sugar efflux transporters has remained elusive. Using optical glucose sensors, we identified a new class of sugar transporters, named SWEETs, and show that at least six out of seventeen Arabidopsis, two out of over twenty rice and two out of seven homologues in Caenorhabditis elegans, and the single copy human protein, mediate glucose transport. Arabidopsis SWEET8 is essential for pollen viability, and the rice homologues SWEET11 and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter. Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is probably targeted by pathogens and symbionts for nutritional gain. The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Characterization of SWEET transporters.
Figure 2: Biotrophic bacteria or fungi induce mRNA levels of different SWEET genes.
Figure 3: Type-III-effector-specific induction of OsSWEET genes in rice disease.
Figure 4: Model for the function of SWEET transporters in plant pathogenesis.
Figure 5: Metazoan SWEET transporters.

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  2. Thorens, B., Guillam, M. T., Beermann, F., Burcelin, R. & Jaquet, M. Transgenic reexpression of GLUT1 or GLUT2 in pancreatic β cells rescues GLUT2-null mice from early death and restores normal glucose-stimulated insulin secretion. J. Biol. Chem. 275, 23751–23758 (2000)

    Article  CAS  Google Scholar 

  3. Stümpel, F., Burcelin, R., Jungermann, K. & Thorens, B. Normal kinetics of intestinal glucose absorption in the absence of GLUT2: evidence for a transport pathway requiring glucose phosphorylation and transfer into the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 98, 11330–11335 (2001)

    Article  ADS  Google Scholar 

  4. Hosokawa, M. & Thorens, B. Glucose release from GLUT2-null hepatocytes: characterization of a major and a minor pathway. Am. J. Physiol. Enocriol. Metab. E794–E801 (2002)

  5. Hesse, M., Pacini, E. & Willemse, M. The Tapetum: Cytology, Function, Biochemistry and Evolution 1–152 (Springer, 2004)

    Google Scholar 

  6. Bisseling, T., Dangl, J. L. & Schulze-Lefert, P. Next-generation communication. Science 324, 691 (2009)

    Article  ADS  CAS  Google Scholar 

  7. Zhou, Y., Qu, H., Dibley, K. E., Offler, C. E. & Patrick, J. W. A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators. Plant J. 49, 750–764 (2007)

    Article  CAS  Google Scholar 

  8. Tang, D. J. et al. Xanthomonas campestris pv. campestris possesses a single gluconeogenic pathway that is required for virulence. J. Bacteriol. 187, 6231–6237 (2005)

    Article  CAS  Google Scholar 

  9. Patrick, J. W. Solute efflux from the host at plant microorganism interfaces. Aust. J. Plant Physiol. 16, 53–67 (1989)

    CAS  Google Scholar 

  10. Aked, J. & Hall, J. L. The uptake of glucose, fructose and sucrose into the lower epidermis of leaf discs of pea (Pisum sativum L. cv. Argenteum). New Phytol. 123, 271–276 (1993)

    Article  CAS  Google Scholar 

  11. Sutton, P. N., Henry, M. J. & Hall, J. L. Glucose, and not sucrose, is transported from wheat to wheat powdery mildew. Planta 208, 426–430 (1999)

    Article  CAS  Google Scholar 

  12. Sutton, P. N., Gilbert, M. J., Williams, L. E. & Hall, J. L. Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol. Plant. 129, 787–795 (2007)

    Article  CAS  Google Scholar 

  13. Voegele, R. T., Struck, C., Hahn, M. & Mendgen, K. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae . Proc. Natl Acad. Sci. USA 98, 8133–8138 (2001)

    Article  ADS  CAS  Google Scholar 

  14. Aramemnon. Plant membrane protein database 〈http://aramemnon.botanik.uni-koeln.de〉 (2010)

  15. Takanaga, H. & Frommer, W. B. Facilitative plasma membrane transporters function during ER transit. FASEB J. 24, 2849–2858 (2010)

    Article  CAS  Google Scholar 

  16. Takanaga, H., Chaudhuri, B. & Frommer, W. B. GLUT1 and GLUT9 as major contributors to glucose influx in HepG2 cells identified by a high sensitivity intramolecular FRET glucose sensor. Biochim. Biophys. Acta 1778, 1091–1099 (2008)

    Article  CAS  Google Scholar 

  17. Wieczorke, R. et al. Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae . FEBS Lett. 464, 123–128 (1999)

    Article  CAS  Google Scholar 

  18. Bermejo, C., Haerizadeh, F., Takanaga, H., Chermak, D. & Frommer, W. B. Dynamic analysis of cytosolic glucose and ATP levels in yeast with optical sensors. Biochem. J. 10.1042/BJ20100946 (20 September 2010)

  19. Chaudhuri, B. et al. Protonophore- and pH-insensitive glucose and sucrose accumulation detected by FRET nanosensors in Arabidopsis root tips. Plant J. 56, 948–962 (2008)

    Article  CAS  Google Scholar 

  20. Guan, Y. F. et al. RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis . Plant Physiol. 147, 852–863 (2008)

    Article  CAS  Google Scholar 

  21. Yang, B., Sugio, A. & White, F. F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc. Natl Acad. Sci. USA 103, 10503–10508 (2006)

    Article  ADS  CAS  Google Scholar 

  22. Song, L. F., Zou, J. J., Zhang, W. Z., Wu, W. H. & Wang, Y. Ion transporters involved in pollen germination and pollen tube tip-growth. Plant Signal. Behav. 4, 1193–1195 (2009)

    Article  Google Scholar 

  23. Engel, M. L., Holmes-Davis, R. & McCormick, S. Green sperm. Identification of male gamete promoters in Arabidopsis . Plant Physiol. 138, 2124–2133 (2005)

    Article  CAS  Google Scholar 

  24. Ge, Y. X. et al. Partial silencing of the NEC1 gene results in early opening of anthers in Petunia hybrida . Mol. Genet. Genomics 265, 414–423 (2001)

    Article  CAS  Google Scholar 

  25. Ge, Y. X. et al. NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida . Plant J. 24, 725–734 (2000)

    Article  CAS  Google Scholar 

  26. Quirino, B. F., Reiter, W. D. & Amasino, R. D. One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol. Biol. 46, 447–457 (2001)

    Article  CAS  Google Scholar 

  27. Quirino, B. F., Normanly, J. & Amasino, R. M. Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol. Biol. 40, 267–278 (1999)

    Article  CAS  Google Scholar 

  28. Ferrari, S. et al. Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol. 144, 367–379 (2007)

    Article  CAS  Google Scholar 

  29. Yuan, M., Chu, Z., Li, X., Xu, C. & Wang, S. Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant Cell Physiol. 50, 947–955 (2009)

    Article  CAS  Google Scholar 

  30. Chu, Z. et al. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev. 20, 1250–1255 (2006)

    Article  CAS  Google Scholar 

  31. Chu, Z. et al. Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor. Appl. Genet. 112, 455–461 (2006)

    Article  CAS  Google Scholar 

  32. Boch, J. et al. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509–1512 (2009)

    Article  ADS  CAS  Google Scholar 

  33. Antony, G. et al. xa13 recessive resistance to bacterial blight is defeated by the induction of disease susceptibility gene Os11N3 . Plant Cell (in the press)

  34. Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M. & Dangl, J. L. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60, 425–449 (2006)

    Article  CAS  Google Scholar 

  35. Mansfield, J. W. From bacterial avirulence genes to effector functions via the hrp delivery system: an overview of 25 years of progress in our understanding of plant innate immunity. Mol. Plant Pathol. 10, 721–734 (2009)

    Article  CAS  Google Scholar 

  36. Ashrafi, K. et al. Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421, 268–272 (2003)

    Article  ADS  CAS  Google Scholar 

  37. Hamada, M., Wada, S., Kobayashi, K. & Satoh, N. Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis . Differentiation 73, 364–376 (2005)

    Article  CAS  Google Scholar 

  38. Ibberson, M., Uldry, M. & Thorens, B. GLUTX1, a novel mammalian glucose transporter expressed in the central nervous system and insulin-sensitive tissues. J. Biol. Chem. 275, 4607–4612 (2000)

    Article  CAS  Google Scholar 

  39. Berglund, L. et al. A genecentric Human Protein Atlas for expression profiles based on antibodies. Mol. Cell. Proteomics 7, 2019–2027 (2008)

    Article  CAS  Google Scholar 

  40. Human Protein Atlas. Small intestine [RAG1AP1] 〈http://www.proteinatlas.org/normal_unit.php?antibody_id=18095&mainannotation_id=1747049〉 (2010)

  41. Anderson, S. M., Rudolph, M. C., McManaman, J. L. & Neville, M. C. Key stages in mammary gland development. Secretory activation in the mammary gland: it's not just about milk protein synthesis! Breast Cancer Res . 9, 204 (2007)

  42. Bioparadigms. SLC Tables 〈http://www.bioparadigms.org/slc/intro.htm〉 (2010)

  43. Santer, R. et al. Mutations in GLUT2, the gene for the liver-type glucose transporter, in patients with Fanconi-Bickel syndrome. Nature Genet. 17, 324–326 (1997)

    Article  CAS  Google Scholar 

  44. Manz, F. et al. Fanconi-Bickel syndrome. Pediatr. Nephrol. 1, 509–518 (1987)

    Article  CAS  Google Scholar 

  45. Udvardi, M. K., Yang, L.-J. O., Young, S. & Day, D. A. Sugar and amino acid transport across symbiotic membranes from soybean nodules. Mol. Plant Micr. Int. 3, 334–340 (1990)

    Article  CAS  Google Scholar 

  46. Oerke, E. C. Crop losses to pests. J. Agric. Sci. 144, 31–43 (2006)

    Article  Google Scholar 

  47. Hediger, M. A., Coady, M. J., Ikeda, T. S. & Wright, E. M. Expression cloning and cDNA sequencing of the Na+/glucose co-transporter. Nature 330, 379–381 (1987)

    Article  ADS  CAS  Google Scholar 

  48. Fehr, M., Takanaga, H., Ehrhardt, D. W. & Frommer, W. B. Evidence for high-capacity bidirectional glucose transport across the endoplasmic reticulum membrane by genetically encoded fluorescence resonance energy transfer nanosensors. Mol. Cell. Biol. 25, 11102–11112 (2005)

    Article  CAS  Google Scholar 

  49. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ CT method. Methods 25, 402–408 (2001)

    Article  CAS  Google Scholar 

  50. Hruz, T. et al. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 420747 (2008)

    Article  Google Scholar 

  51. Lalonde, S. et al. A membrane protein/signaling protein interaction network for Arabidopsis version AMPv2. Front. Physiol. 10.3389/fphys.2010.00024 (22 September 2010)

  52. Loqué, D., Lalonde, S., Looger, L. L., von Wiren, N. & Frommer, W. B. A cytosolic trans-activation domain essential for ammonium uptake. Nature 446, 195–198 (2007)

    Article  ADS  Google Scholar 

  53. Riesmeier, J. W., Willmitzer, L. & Frommer, W. B. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11, 4705–4713 (1992)

    Article  CAS  Google Scholar 

  54. Kunkel, T. A., Bebenek, K. & McClary, J. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204, 125–139 (1991)

    Article  CAS  Google Scholar 

  55. Hou, B. H., Takanaga, H., Griesbeck, O. & Frommer, W. B. Osmotic induction of calcium accumulation in human embryonic kidney cells detected with a high sensitivity FRET calcium sensor. Cell Calcium 46, 130–135 (2009)

    Article  CAS  Google Scholar 

  56. Ballatori, N., Wang, W., Li, L. & Truong, A. T. An endogenous ATP-sensitive glutathione S-conjugate efflux mechanism in Xenopus laevis oocytes. Am. J. Physiol. 270, R1156–R1162 (1996)

    CAS  PubMed  Google Scholar 

  57. Detaille, D., Wiernsperger, N. & Devos, P. Metformin interaction with insulin-regulated glucose uptake, using the Xenopus laevis oocyte model expressing the mammalian transporter GLUT4. Eur. J. Pharmacol. 377, 127–136 (1999)

    Article  CAS  Google Scholar 

  58. Chernova, M. N. et al. Electrogenic sulfate/chloride exchange in Xenopus oocytes mediated by murine AE1 E699Q. J. Gen. Physiol. 109, 345–360 (1997)

    Article  CAS  Google Scholar 

  59. Vogel, J. & Somerville, S. Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proc. Natl Acad. Sci. USA 97, 1897–1902 (2000)

    Article  ADS  CAS  Google Scholar 

  60. Haring, M. et al. Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods 3, 11 (2007)

    Article  Google Scholar 

  61. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 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 (1994)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was made possible by grants from the Department of Energy (DE-FG02-04ER15542) and NIH (NIDDK; 1RO1DK079109) to W.B.F., X.-Q.Q. was supported by The Carnegie Institution and the National Natural Science Foundation of China (NSFC; 30771288). NSF (IOS-0821801) and NIH (ZRO1GM06886-06A1) to M.B.M. and J.-G.K. was supported 50% by NIH and 50% by NSF. W.U. was supported in part by an NIH postdoctoral fellowship (F32GM083439-02). G.A. and F.F.W. were supported by grants from USDA NIFA (2007-35319-18103) and NSF Plant Genome (DBI-0820831).

Author information

Authors and Affiliations

  1. Department of Plant Biology, Carnegie Institution for Science, 260 Panama St, Stanford, 94305, California, USA

    Li-Qing Chen, Bi-Huei Hou, Sylvie Lalonde, Hitomi Takanaga, Mara L. Hartung, Xiao-Qing Qu, Woei-Jiun Guo, Bhavna Chaudhuri, Diane Chermak & Wolf B. Frommer

  2. Department of Biology, Stanford University, 228A Gilbert Bioscience Building, 371 Serra Mall, Stanford, California 94305, USA,

    Jung-Gun Kim & Mary Beth Mudgett

  3. Department of Plant Pathology, Kansas State University, Manhattan, 66506, Kansas, USA

    Ginny Antony & Frank F. White

  4. Energy Bioscience Institute, 130 Calvin Hall, MC 5230, Berkeley, 94720, California, USA

    William Underwood & Shauna C. Somerville

Authors
  1. Li-Qing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bi-Huei Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sylvie Lalonde
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hitomi Takanaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mara L. Hartung
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiao-Qing Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Woei-Jiun Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jung-Gun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. William Underwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bhavna Chaudhuri
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Diane Chermak
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ginny Antony
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Frank F. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Shauna C. Somerville
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Mary Beth Mudgett
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Wolf B. Frommer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

W.B.F., S.L., M.B.M. and S.C.S. conceived and designed the experiments. L.-Q.C., B.-H.H., H.T., M.L.H., J.-G.K., X.-Q.Q., W.-J.G., W.U., B.C., G.A. and D.C. performed the experiments. W.B.F., S.L., M.B.M., G.A., F.F.W. and S.S. analysed the data. L.-Q.C. and W.B.F. wrote the manuscript.

Corresponding author

Correspondence to Wolf B. Frommer.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-22 with legends, Supplementary Tables 1-3 and additional references. (PDF 9227 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, LQ., Hou, BH., Lalonde, S. et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532 (2010). https://doi.org/10.1038/nature09606

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09606

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology