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Sugar transporters for intercellular exchange and nutrition of pathogens

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.

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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.

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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).

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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.

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Correspondence to Wolf B. Frommer.

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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

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