A secreted effector protein of Ustilago maydis guides maize leaf cells to form tumors

Plant Cell

Volumn 27, Issue 4, 2015, Pages 1332-1351

  Redkar, Amey ^a,f   Hoser, Rafal ^b   Schilling, Lena ^a   Zechmann, Bernd ^c   Krzymowska, Magdalena ^b   Walbot, Virginia ^d   Doehlemann, Gunther ^a,e  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c BAYLOR UNIVERSITY   (United States)

^d STANFORD UNIVERSITY   (United States)

^e UNIVERSITY OF COLOGNE   (Germany)

^f NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; SACCHAROMYCES CEREVISIAE; USTILAGO MAYDIS; ZEA MAYS;

PLANT PROTEIN;

GENE EXPRESSION REGULATION; IMMUNOLOGY; MAIZE; METABOLISM; PLANT DISEASE; PLANT TUMOR;

GENE EXPRESSION REGULATION, PLANT; PLANT DISEASES; PLANT PROTEINS; PLANT TUMORS; ZEA MAYS;

EID: 84928940364     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.131086     Document Type: Article

References (68)

1. Austin, M.J., Muskett, P., Kahn, K., Feys, B.J., Jones, J.D., and Parker, J.E. (2002). Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295: 2077–2080.
2. Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., and Schulze-Lefert, P. (2002). The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295: 2073–2076.
3. Bao, Z., Yang, H., and Hua, J. (2013). Perturbation of cell cycle regulation triggers plant immune response via activation of disease resistance genes. Proc. Natl. Acad. Sci. USA 110: 2407–2412.
4. Bhavsar, A.P., et al. (2013). The Salmonella type III effector SspH2 specifically exploits the NLR co-chaperone activity of SGT1 to subvert immunity. PLoS Pathog. 9: e1003518.
5. Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei, A., and Kahmann, R. (2009). Ustilago maydis as a pathogen. Annu. Rev. Phytopathol. 47: 423–445.
6. Brefort, T., Tanaka, S., Neidig, N., Doehlemann, G., Vincon, V., and Kahmann, R. (2014). Characterization of the largest effector gene cluster of Ustilago maydis. PLoS Pathog. 10: e1003866.
7. Cohen, P. (2000). The regulation of protein function by multisite phos-phorylation—A 25 year update. Trends Biochem. Sci. 25: 596–601.
8. Conover, W.J. (1999). Practical Nonparametric Statistics, (New York: John Wiley & Sons).
9. Cui, H., Wang, Y., Xue, L., Chu, J., Yan, C., Fu, J., Chen, M., Innes, R.W., and Zhou, J.M. (2010). Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7: 164–175.
10. Cuzick, A., Maguire, K., and Hammond-Kosack, K.E. (2009). Lack of the plant signalling component SGT1b enhances disease resistance to Fusarium culmorum in Arabidopsis buds and flowers. New Phytol. 181: 901–912.
11. Djamei, A., and Kahmann, R. (2012). Ustilago maydis: Dissecting the molecular interface between pathogen and plant. PLoS Pathog. 8: e1002955.
12. Djamei, A., et al. (2011). Metabolic priming by a secreted fungal effector. Nature 478: 395–398.
13. Doehlemann, G., Reissmann, S., Assmann, D., Fleckenstein, M., and Kahmann, R. (2011). Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydis-induced tumour formation. Mol. Microbiol. 81: 751–766.
14. Doehlemann, G., Requena, N., Schaefer, P., Brunner, F., O’Connell, R., and Parker, J.E. (2014). Reprogramming of plant cells by filamentous plant-colonizing microbes. New Phytol. 204: 803–814.
15. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., and Kahmann, R. (2009). Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog. 5: e1000290.
16. Doehlemann, G., Wahl, R., Horst, R.J., Voll, L.M., Usadel, B., Poree, F., Stitt, M., Pons-Kühnemann, J., Sonnewald, U., Kahmann, R., and Kämper, J. (2008). Reprogramming a maize plant: Transcrip-tional and metabolic changes induced by the fungal biotroph Usti-lago maydis. Plant J. 56: 181–195.
17. Dubacq, C., Guerois, R., Courbeyrette, R., Kitagawa, K., and Mann, C. (2002). Sgt1p contributes to cyclic AMP pathway activity and physically interacts with the adenylyl cyclase Cyr1p/Cdc35p in budding yeast. Eukaryot. Cell 1: 568–582.
18. El Oirdi, M., and Bouarab, K. (2007). Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea. New Phytol. 175: 131–139.
19. Flowers, J.L., and Vaillancourt, L.J. (2005). Parameters affecting the efficiency of Agrobacterium tumefaciens-mediated transformation of Colletotrichum graminicola. Curr. Genet. 48: 380–388.
20. Gao, L., Kelliher, T., Nguyen, L., and Walbot, V. (2013). Ustilago maydis reprograms cell proliferation in maize anthers. Plant J. 75: 903–914.
21. Garcia-Ranea, J.A., Mirey, G., Camonis, J., and Valencia, A. (2002). p23 and HSP20/alpha-crystallin proteins define a conserved sequence domain present in other eukaryotic protein families. FEBS Lett. 529: 162–167.
22. Gratzner, H.G. (1982). Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218: 474–475.
23. Gray, W.M., Muskett, P.R., Chuang, H.W., and Parker, J.E. (2003). Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell 15: 1310–1319.
24. Hann, D.R., and Rathjen, J.P. (2007). Early events in the pathoge-nicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J. 49: 607–618.
25. Hemetsberger, C., Herrberger, C., Zechmann, B., Hillmer, M., and Doehlemann, G. (2012). The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog. 8: e1002684.
26. Heyneke, E., Luschin-Ebengreuth, N., Krajcer, I., Wolkinger, V., Müller, M., and Zechmann, B. (2013). Dynamic compartment specific changes in glutathione and ascorbate levels in Arabidopsis plants exposed to different light intensities. BMC Plant Biol. 13: 104.
27. Hogenhout, S.A., Van der Hoorn, R.A.L., Terauchi, R., and Kamoun, S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 22: 115–122.
28. Horst, R.J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kämper, J., Sonnewald, U., and Voll, L.M. (2010). Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152: 293–308.
29. Hoser, R., Zurczak, M., Lichocka, M., Zuzga, S., Dadlez, M., Samuel, M.A., Ellis, B.E., Stuttmann, J., Parker, J.E., Hennig, J., and Krzymowska, M. (2013). Nucleocytoplasmic partitioning of tobacco N receptor is modulated by SGT1. New Phytol. 200: 158–171.
30. Jelenska, J., van Hal, J.A., and Greenberg, J.T. (2010). Pseudo-monas syringae hijacks plant stress chaperone machinery for virulence. Proc. Natl. Acad. Sci. USA 107: 13177–13182.
31. Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323–329.
32. Kämper, J., et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101.
33. Kankanala, P., Czymmek, K., and Valent, B. (2007). Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19: 706–724.
34. Kelliher, T., and Walbot, V. (2011). Emergence and patterning of the five cell types of the Zea mays anther locule. Dev. Biol. 350: 32–49.
35. Khang, C.H., Berruyer, R., Giraldo, M.C., Kankanala, P., Park, S.Y., Czymmek, K., Kang, S., and Valent, B. (2010). Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22: 1388–1403.
36. Kim, N.H., Kim, D.S., Chung, E.H., and Hwang, B.K. (2014). Pepper suppressor of the G2 allele of skp1 interacts with the receptor-like cytoplasmic kinase1 and type III effector AvrBsT and promotes the hypersensitive cell death response in a phosphorylation-dependent manner. Plant Physiol. 165: 76–91.
37. Kitagawa, K., Skowyra, D., Elledge, S.J., Harper, J.W., and Hieter, P. (1999). SGT1 encodes an essential component of the yeast ki-netochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol. Cell 4: 21–33.
38. Kotogány, E., Dudits, D., Horváth, G.V., and Ayaydin, F. (2010). A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods 6: 5.
39. Li, P., et al. (2010). The developmental dynamics of the maize leaf transcriptome. Nat. Genet. 42: 1060–1067.
40. Loubradou, G., Brachmann, A., Feldbrügge, M., and Kahmann, R. (2001). A homologue of the transcriptional repressor Ssn6p antagonizes cAMP signalling in Ustilago maydis. Mol. Microbiol. 40: 719–730.
41. Mueller, A.N., Ziemann, S., Treitschke, S., Aßmann, D., and Doehlemann, G. (2013). Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog. 9: e1003177.
42. Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., and de Vries, R.P. (2008). The secretome of the maize pathogen Usti-lago maydis. Fungal Genet. Biol. 45 (suppl. 1): S63–S70.
43. Mukhtar, M.S., et al. (2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333: 596–601.
44. Noël, L.D., Cagna, G., Stuttmann, J., Wirthmüller, L., Betsuyaku, S., Witte, C.P., Bhat, R., Pochon, N., Colby, T., and Parker, J.E. (2007). Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19: 4061–4076.
45. Ökmen, B., and Doehlemann, G. (2014). Inside plant: Biotrophic strategies to modulate host immunity and metabolism. Curr. Opin. Plant Biol. 20: 19–25.
46. Peart, J.R., et al. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99: 10865–10869.
47. Salic, A., and Mitchison, T.J. (2008). A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl. Acad. Sci. USA 105: 2415–2420.
48. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
49. Schilling, L., Matei, A., Redkar, A., Walbot, V., and Doehlemann, G. (2014). Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors. Mol. Plant Pathol. 15: 780–789.
50. Schirawski, J., et al. (2010). Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330: 1546–1548.
51. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., Herskowitz, I., and Kahmann, R. (1990). The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60: 295–306.
52. Shirasu, K. (2009). The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu. Rev. Plant Biol. 60: 139–164.
53. Skibbe, D.S., Doehlemann, G., Fernandes, J., and Walbot, V. (2010). Maize tumors caused by Ustilago maydis require organ-specific genes in host and pathogen. Science 328: 89–92.
54. Song, J., Durrant, W.E., Wang, S., Yan, S., Tan, E.H., and Dong, X. (2011). DNA repair proteins are directly involved in regulation of gene expression during plant immune response. Cell Host Microbe 9: 115–124.
55. Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R.A., and Kamoun, S. (2009). Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc. Natl. Acad. Sci. USA 106: 1654–1659.
56. Sparkes, I.A., Runions, J., Kearns, A., and Hawes, C. (2006). Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1: 2019– 2025.
57. Takahashi, A., Casais, C., Ichimura, K., and Shirasu, K. (2003). HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 11777–11782.
58. Talarczyk, A., Krzymowska, M., Borucki, W., and Hennig, J. (2002). Effect of yeast CTA1 gene expression on response of tobacco plants to tobacco mosaic virus infection. Plant Physiol. 129: 1032–1044.
59. Tanaka, S., Brefort, T., Neidig, N., Djamei, A., Kahnt, J., Vermerris, W., Koenig, S., Feussner, K., Feussner, I., and Kahmann, R. (2014). A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize. eLife 3: e01355.
60. van der Linde, K., Hemetsberger, C., Kastner, C., Kaschani, F., van der Hoorn, R.A., Kumlehn, J., and Doehlemann, G. (2012). A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 24: 1285–1300.
61. Walbot, V., and Skibbe, D.S. (2010). Maize host requirements for Ustilago maydis tumor induction. Sex. Plant Reprod. 23: 1–13.
62. Wang, K., Uppalapati, S.R., Zhu, X., Dinesh-Kumar, S.P., and Mysore, K.S. (2010). SGT1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol. Plant Pathol. 11: 597–611.
63. Wen, W., Meinkoth, J.L., Tsien, R.Y., and Taylor, S.S. (1995). Identification of a signal for rapid export of proteins from the nucleus. Cell 82: 463–473.
64. Witte, C.P., Noël, L.D., Gielbert, J., Parker, J.E., and Romeis, T. (2004). Rapid one-step protein purification from plant material using the eight-amino acid StrepII epitope. Plant Mol. Biol. 55: 135–147.
65. Yan, S., Wang, W., Marqués, J., Mohan, R., Saleh, A., Durrant, W.E., Song, J., and Dong, X. (2013). Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol. Cell 52: 602–610.
66. Yang, K.Y., Liu, Y., and Zhang, S. (2001). Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98: 741–746.
67. Zhang, M., Kadota, Y., Prodromou, C., Shirasu, K., and Pearl, L.H. (2010). Structural basis for assembly of Hsp90-Sgt1-CHORD protein complexes: Implications for chaperoning of NLR innate immunity receptors. Mol. Cell 39: 269–281.
68. Zhang, S., and Liu, Y. (2001). Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell 13: 1877–1889.