Skip to main content

Thank you for visiting 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.

A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases


Plant innate immunity is activated on the detection of pathogen-associated molecular patterns (PAMPs) at the cell surface, or of pathogen effector proteins inside the plant cell1,2,3,4. Together, PAMP-triggered immunity and effector-triggered immunity constitute powerful defences against various phytopathogens. Pathogenic bacteria inject a variety of effector proteins into the host cell to assist infection or propagation. A number of effector proteins have been shown to inhibit plant immunity5, but the biochemical basis remains unknown for the vast majority of these effectors. Here we show that the Xanthomonas campestris pathovar campestris type III effector AvrAC enhances virulence and inhibits plant immunity by specifically targeting Arabidopsis BIK1 and RIPK, two receptor-like cytoplasmic kinases known to mediate immune signalling6,7,8. AvrAC is a uridylyl transferase that adds uridine 5′-monophosphate to and conceals conserved phosphorylation sites in the activation loop of BIK1 and RIPK, reducing their kinase activity and consequently inhibiting downstream signalling.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: AvrAC inhibits plant immunity.
Figure 2: AvrAC targets BIK1 and inhibits early PTI signalling events.
Figure 3: AvrAC uridylylates BIK1 and RIPK.
Figure 4: AvrAC uridylyl transferase activity and BIK1 are required for AvrAC virulence in plants.


  1. 1

    Ausubel, F. M. Are innate immune signaling pathways in plants and animals conserved? Nature Immunol. 6, 973–979 (2005)

    CAS  Article  Google Scholar 

  2. 2

    Chisholm, S. T., Coaker, G., Day, B. & Staskawicz, B. J. Host microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814 (2006)

    CAS  Article  Google Scholar 

  3. 3

    Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Boller, T. & Felix, G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406 (2009)

    CAS  Article  Google Scholar 

  5. 5

    Block, A. & Alfano, J. R. Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr. Opin. Microbiol. 14, 39–46 (2011)

    CAS  Article  Google Scholar 

  6. 6

    Lu, D. et al. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl Acad. Sci. USA 107, 496–501 (2010)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Zhang, J. et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7, 290–301 (2010)

    CAS  Article  Google Scholar 

  8. 8

    Liu, J., Elmore, J. M., Lin, Z.-J. D. & Coaker, G. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9, 137–146 (2011)

    CAS  Article  Google Scholar 

  9. 9

    Xu, R.-Q. et al. AvrACXcc8004, a type III effector with a leucine-rich-repeat domain from Xanthomonas campestris pathovar campestris confers avirulence in vascular tissues of Arabidopsis thaliana ecotype Col-0. J. Bacteriol. 190, 343–355 (2008)

    CAS  Article  Google Scholar 

  10. 10

    He, P. et al. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563–575 (2006)

    CAS  Article  Google Scholar 

  11. 11

    Segonzac, C. & Zipfel, C. Activation of plant pattern-recognition receptors by bacteria. Curr. Opin. Microbiol. 14, 54–61 (2011)

    CAS  Article  Google Scholar 

  12. 12

    Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Heese, A. et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl Acad. Sci. USA 104, 12217–12222 (2007)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Chung, E.-H. et al. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9, 125–136 (2011)

    CAS  Article  Google Scholar 

  15. 15

    Woolery, A. R., Luong, P., Broberg, C. A. & Orth, K. AMPylation: something old is new again. Front. Microbiol. 1, 113 (2010)

    CAS  Article  Google Scholar 

  16. 16

    Mattoo, S. et al. Comparative analysis of Histophilus Somni IbpA with other FIC enzymes reveals differences in substrate and nucleotide specificities. J. Biol. Chem. 286, 32834–32842 (2011)

    CAS  Article  Google Scholar 

  17. 17

    Yarbrough, M. L. et al. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323, 269–272 (2009)

    CAS  Article  Google Scholar 

  18. 18

    Worby, C. A. et al. The Fic domain: regulation of cell signaling by adenylylation. Mol. Cell 34, 93–103 (2009)

    CAS  Article  Google Scholar 

  19. 19

    Muller, M. P. et al. The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science 329, 946–949 (2010)

    ADS  Article  Google Scholar 

  20. 20

    Mukherjee, S. et al. Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature 477, 103–106 (2011)

    ADS  CAS  Article  Google Scholar 

  21. 21

    Laluk, K. et al. Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 23, 2831–2849 (2011)

    CAS  Article  Google Scholar 

  22. 22

    Luong, P. et al. Kinetic and structural insights into the mechanism of AMPylation by VopS Fic domain. J. Biol. Chem. 285, 20155–20163 (2010)

    CAS  Article  Google Scholar 

  23. 23

    Xiao, J. et al. Structural basis of Fic mediated adenylylation. Nature Struct. Mol. Biol. 17, 1004–1010 (2010)

    CAS  Article  Google Scholar 

  24. 24

    Sun, W., Dunning, M. F., Pfund, C., Weingarten, R. & Bent, A. F. Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18, 764–779 (2006)

    CAS  Article  Google Scholar 

  25. 25

    Veronese, P. et al. The membrane-anchored BOTRYTIS-INDUCED KINASE1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell 18, 257–273 (2006)

    CAS  Article  Google Scholar 

  26. 26

    White, F. F., Potnis, N., Jones J. B & Koebnik, R. The type III effectors of Xanthomonas. Mol. Plant Pathol. 10, 749–766 (2009)

    CAS  Article  Google Scholar 

  27. 27

    Kinch, L. N., Yarbrough, M. L., Orth, K. & Grishin, N. V. Fido, a novel AMPylation domain common to Fic, Doc, and AvrB. PLoS ONE 4, e5818 (2009)

    ADS  Article  Google Scholar 

  28. 28

    Mukherjee, S. et al. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312, 1211–1214 (2006)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Wang, L. F., Tang, X. Y. & He, C. Z. The bifunctional effector AvrXccC of Xanthomonas campestris pv. campestris requires plasma membrane-anchoring for host recognition. Mol. Plant Pathol. 8, 491–501 (2007)

    Article  Google Scholar 

  30. 30

    Yuan, J. & He, S. Y. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J. Bacteriol. 178, 6399–6402 (1996)

    CAS  Article  Google Scholar 

  31. 31

    Li, X. et al. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc. Natl Acad. Sci. USA 102, 12990–12995 (2005)

    ADS  CAS  Article  Google Scholar 

  32. 32

    Schäfer, A. et al. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69–73 (1994)

    Article  Google Scholar 

  33. 33

    Zuo, J., Niu, Q. W. & Chua, N. H. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265–273 (2000)

    CAS  Article  Google Scholar 

  34. 34

    Zhang, J. et al. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1, 175–185 (2007)

    CAS  Article  Google Scholar 

  35. 35

    Schwessinger, B. et al. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046 (2011)

    CAS  Article  Google Scholar 

  36. 36

    Macho, A. P. et al. Competitive index in mixed infections: a sensitive and accurate assay for the genetic analysis of Pseudomonas syringae–plant interactions. Mol. Plant Pathol. 8, 437–450 (2007)

    Article  Google Scholar 

  37. 37

    Dow, J. M. et al. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc. Natl Acad. Sci. USA 100, 10995–11000 (2003)

    ADS  CAS  Article  Google Scholar 

  38. 38

    Schechter, L. M. et al. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol. 186, 543–555 (2004)

    CAS  Article  Google Scholar 

  39. 39

    Cheng, W. et al. The AvrPtoB-BAK1 complex reveals two structurally similar kinase-interacting domains in a single type III effector. Cell Host Microbe 10, 616–626 (2011)

    CAS  Article  Google Scholar 

Download references


The authors thank J. Chai for sharing plasmids before publication, A. Bent for the XccB186 strain, S. Y. He and F. White for helpful comments. J.-M.Z. was supported by grants from the Chinese Ministry of Science and Technology (2011CB100700; 2010CB835301). S.C. was supported by a grant from the Chinese Ministry of Science and Technology (2010CB835204) C.H. was supported by Funds from Hainan University.

Author information




S.C., C.H. and J.-M.Z. conceived and designed the experiments. F.F., F.Y., W.R., X.W. and J.Z. performed the experiments. F.F., F.Y., S.C., C.H. and J.-M.Z. analysed the data. F.F., S.C., C.H. and J.-M.Z. wrote the paper.

Corresponding authors

Correspondence to Chaozu He or Jian-Min Zhou.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-16. (PDF 1597 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Feng, F., Yang, F., Rong, W. et al. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485, 114–118 (2012).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links