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Oomycete pathogens encode RNA silencing suppressors

Abstract

Effectors are essential virulence proteins produced by a broad range of parasites, including viruses, bacteria, fungi, oomycetes, protozoa, insects and nematodes. Upon entry into host cells, pathogen effectors manipulate specific physiological processes or signaling pathways to subvert host immunity. Most effectors, especially those of eukaryotic pathogens, remain functionally uncharacterized. Here, we show that two effectors from the oomycete plant pathogen Phytophthora sojae suppress RNA silencing in plants by inhibiting the biogenesis of small RNAs. Ectopic expression of these Phytophthora suppressors of RNA silencing enhances plant susceptibility to both a virus and Phytophthora, showing that some eukaryotic pathogens have evolved virulence proteins that target host RNA silencing processes to promote infection. These findings identify RNA silencing suppression as a common strategy used by pathogens across kingdoms to cause disease and are consistent with RNA silencing having key roles in host defense.

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Figure 1: P. sojae RXLR effectors PSR1 and PSR2 suppress transgene-mediated GFP silencing in GFP-transgenic N. benthamiana 16c plants.
Figure 2: Effects of PSR1 and PSR2 on small RNA biogenesis in Arabidopsis.
Figure 3: PSR1 promotes the infection of N. benthamiana by PVX.
Figure 4: Expression of RNA silencing suppressors in N. benthamiana enhances infection by P. infestans.
Figure 5: Silencing of PSR2 in P. sojae impairs virulence in soybean.

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Acknowledgements

We thank B. Tyler (Oregon State University) for providing soybean seeds and ten effector clones. S. Kamoun (The Sainsbury Laboratory) and M. Coffey (University of California, Riverside) kindly provided pGR106 and P. sojae strain P6497, respectively. We are indebted to S.-W. Ding for sharing viral suppressor constructs and thoughtful input. This work was supported by funds from the University of California, Riverside, to W.M. and X.C., National Science Foundation (NSF) grant IOS-0847870 to W.M. and US Department of Agriculture–National Institute of Food and Agriculture (USDA-NIFA) grants 2010-04209 and 2008-00694 to X.C. and H.S.J., respectively. L.L. was supported by a fellowship from the China Scholarship Council.

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Authors and Affiliations

Authors

Contributions

W.M. and X.C. developed the concept. W.M., X.C., Y.Q., Y.W. and H.S.J. designed the experiments. Y.Q., L.L., Q. Xiong, C.F., J.W., J.S., X.W., X.L., Q. Xiang, S.J. and F.Z. performed the experiments. W.M., X.C. and Y.W. analyzed the data. W.M., X.C., H.S.J., Y.Q., L.L. and Y.W. wrote the manuscript. W.M. conceived, directed and coordinated the project.

Corresponding author

Correspondence to Wenbo Ma.

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The authors declare no competing financial interests.

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Supplementary Figures 1–14 and Supplementary Tables 1–3 (PDF 9930 kb)

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Qiao, Y., Liu, L., Xiong, Q. et al. Oomycete pathogens encode RNA silencing suppressors. Nat Genet 45, 330–333 (2013). https://doi.org/10.1038/ng.2525

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