The type III effector HsvG of the gall-forming Pantoea agglomerans mediates expression of the host gene HSVGT

Molecular Plant-Microbe Interactions

Volumn 25, Issue 2, 2012, Pages 231-240

  Nissan, Gal ^a   Manulis Sasson, Shulamit ^b   Chalupowicz, Laura ^b   Teper, Doron ^a   Yeheskel, Adva ^a   Pasmanik Chor, Metsada ^a   Sessa, Guido ^a   Barash, Isaac ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; HSVG PROTEIN, PANTOEA AGGLOMERANS; LEUCINE ZIPPER PROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARYOPHYLLACEAE; GENE EXPRESSION REGULATION; GENETICS; HOST RANGE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PANTOEA; PATHOGENICITY; PLANT DISEASE; PLANT GENE; PLANT TUMOR; PROMOTER REGION; TRANSCRIPTION INITIATION; UPREGULATION; VIRULENCE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CARYOPHYLLACEAE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HOST SPECIFICITY; LEUCINE ZIPPERS; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PANTOEA; PLANT DISEASES; PLANT TUMORS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION; VIRULENCE; ZINC FINGERS;

EUKARYOTA; GYPSOPHILA; GYPSOPHILA PANICULATA; PANTOEA AGGLOMERANS; PANTOEA AGGLOMERANS PV. GYPSOPHILAE;

EID: 84856189358     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-11-0173     Document Type: Article

References (74)

1. Ahmad, S., Gromiha, M. M., and Sarai, A. 2004. Analysis and prediction of DNA-binding proteins and their binding residues based on composition, sequence and structure information. Bioinformatics 20:477-486. (Pubitemid 38344327)
2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G, Smith, J. A., and Struhl, K. eds. 1995. Current Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
3. Baily, T. L., and Elkan, C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Pages 28-36 in: Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology, Vol 2. The Association for the Advancement of Artificial Intelligence (AAAI) Press, Menlo Park, CA, U.S.A.
4. Balaji, V., Jacob-Hirsh, J., Sherf, O., Eichenlaub, R., Iraki, N., Manulis- Sasson, S., Rechavi, G., Barash I., and Sessa, G. 2008. Tomato transcriptional changes in response to Clavibacter michiganensis subsp. Michiganensis reveal a role for ethylene in disease development. Plant Physiol. 146:1797-1809. (Pubitemid 352844081)
5. Barash, I., and Manulis-Sasson, S. 2007. Virulence mechanisms and host specificity of gall-forming Pantoea agglomerans. Trends Microbiol. 15:538-545. (Pubitemid 350137736)
6. Barash, I., and Manulis-Sasson, S. 2009. Recent evolution of bacterial pathogens: The gall-forming Pantoea agglomerans case. Annu. Rev. Phytopathol. 47:133-152.
7. Berezin, C., Glaser, F., Rosenberg, Y., Paz, I., Pupko, T., Fariselli, P., Casadio, R., and Ben-Tal, N. 2004. The identification of functionally and structurally important residues in protein sequences. Bioinformatics 20:1322-1324. (Pubitemid 38807587)
8. Biegert, A., and Soding, J. 2009. Sequence context-specific profiles for homology searching. Proc. Natl. Acad. Sci. U.S.A. 106:3770-3775.
9. Boch, J., and Bonas, U. 2010. Xanthomonas AvrBs3 family-type III effectors: Discovery and function. Annu. Rev. Phytopathol. 48:419-436.
10. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A., and Bonas, U. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509-1512.
11. Bogdanove, A. J., Schornack, S., and Lahaye, T. 2010. TAL effectors: Finding plant genes for disease and defense. Curr. Opin. Plant Biol. 13:394-401.
12. Buchanan, B. B., Gruissem, W., and Jones, R. L. 2000. Biochemistry and Molecular Biology of Plants. American Society of Plant Physiology, Rockville, MD, U.S.A.
13. Burr, T. J., Katz, B. H., Abawi, G. S., and Crosier, D. C. 1991. Comparison of tumorigenic strains of Erwinia herbicola isolated from table beet with E. herbicola pv. gypsophilae. Plant Dis. 75:855-858.
14. Cheetham, M. E., and Caplan, A. J. 1998. Structure, function and evolution of DnaJ: Conservation and adaptation of chaperon function. Cell Stress Chaperon. 3:28-36. (Pubitemid 28159676)
15. Ciftci-Yilmaza, S., and Mittlera, R. 2008. The zinc finger network of plants. Cell. Mol. Life Sci. 65:1150-1160.
16. Clark, E., Manulis, S., Ophir, Y., Barash, I, and Gafni, Y. 1993. Cloning and characterization of iaaM and iaaH from Erwinia herbicola pathovar gypsophilae. Phytopathology 83:234-240.
17. Cole, C., Barber, J. D., and Barton, G. J. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36 (Suppl. 2):W197-W201.
18. Cooksey, D. A. 1986. Galls of Gypsophila paniculata caused by Erwinia herbicola. Plant Dis. 70:464-468.
19. Dong, X. 2004. NPR1, all things considered. Curr. Opin. Plant Biol. 7:547-552. (Pubitemid 39175152)
20. Enninga, J., Mounier, J., Sansonetti, P., and Tran Van Nhieu, G. 2005. Secretion of type III effectors into host cells in real time. Nat. Methods 2:959-965. (Pubitemid 43108733)
21. Ezra, D., Barash I., Valinsky L., and Manulis, S. 2000. The dual function in virulence and host range restriction of a gene isolated from the pPATHEhg plasmid of Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 13:683-692. (Pubitemid 30322809)
22. Frohman, M. A. 1993. Rapid amplification of complementary DNA ends for generation of full-length complementary DNAs: Thermal RACE. Methods Enzymol. 218:340-356.
23. Ginalski, K., Elofsson, A., and Fischer, D. L. R. 2002. 3D-Jury: A simple approach to improve protein structure predictions. Bioinformatics 19:1015-1018.
24. Gurlebeck, D., Thieme, F., and Bonas, U. 2006. Type III effector proteins from the plant pathogen Xanthomonas and their role in interaction with the host plant. J. Plant Physiol. 163:233-255. (Pubitemid 43112080)
25. Hennessy, F., Nicoll, W. S., Zimmermann, R., Cheetham, M. E., and Blatch, G. L. 2005. Not all J domains are created equal: Implications for the specificity of Hsp40-Hsp70 interactions. Prot. Sci. 17:1697-1709. (Pubitemid 41001413)
26. Hwang, S., Gou, Z., and Kuznetsov, I. B. 2007. DP-Bind: A web server for sequence-based prediction of DNA-binding residues in DNA-binding proteins. Bioinformatics 23:634-636. (Pubitemid 46522600)
27. Jakoby, M., Weisshaar, B., Droge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., and Parcy, F. 2002. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7:106-111. (Pubitemid 36726435)
28. Jaroszewski, L., Rychlewski, L., Li, Z., Li, W., and Godzik, A. 2005. FFAS03: A server for profile-profile sequence alignments. Nucleic Acids Res. 33:W284-W288. (Pubitemid 44529927)
29. Jelenska, J., van Hal, J. A., and Greenberg, J. T. 2010. Pseudomonas syringae hijacks plant stress chaperon machinery for virulence. Proc. Natl. Acad. Sci. U.S.A. 107:13177-13182.
30. Jones, D. T. 1999. Protein secondary structure prediction based on position- specific scoring matrices. J. Mol. Biol. 292:195-202. (Pubitemid 29435759)
31. Katho, K., Misawa, K., Kuma, K.-I., and Miyata, T. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066. (Pubitemid 34851225)
32. Kay, S., Hahn, S., Marois, E., Hause, G., and Bonas, U. 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648-651. (Pubitemid 350014839)
33. Kay, S., Hahn, S., Marois, E., Wieduwild, R., and Bonas, U. 2009. Detailed analysis of DNA recognition motifs of Xanthomonas type III effectors AvrBs3 and AvrBs3 rep16. Plant J. 59:859-871.
34. Kelly, W. L. 1998. The J-domain family and the recruitment of chaperone power. Trends Biochem. Sci. 23:222-227.
35. Latchman, D. S. 2008. Eukaryotic Transcription Factors. Academic Press. New York.
36. Lichter, A., Barash, I., Valinsky, L., and Manulis, S. 1995. The genes involved in cytokinin biosynthesis in Erwinia herbicola pv. gypsophilae: Characterization and role in gall formation. J. Bacteriol. 177:4457-4465.
37. Manulis, M., and Barash, I. 2003. The molecular basis for transformation of an epiphyte into a gall-forming pathogen as exemplified by Erwinia herbicola pv. gypsophilae. Pages 19-52 in: Plant-Microbe Interactions, vol. 6. G. Stacey and N. Keen, eds. American Phytopathological Society, St. Paul, MN, U.S.A.
38. Manulis, S., Gafni, Y., Clark, E., Zutra, D., Ophir, Y., and Barash, I. 1991. Identification of a plasmid DNA probe for detection of Erwinia herbicola pathogenic on Gypsophila paniculata. Phytopathology 81:54-57.
39. Marois, E., Van den Ackerveken, G., and Bonas, U. 2002. The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol. Plant-Microbe Interact. 15:637-646. (Pubitemid 34780473)
40. Mayrose, M., Ekengren, S. K., Melech-Bonfil, S., Martin, G. B., and Sessa, G. 2006. A novel link between tomato GRAS genes, plant disease resistance and mechanical stress response. Mol. Plant Pathol. 6:593-604. (Pubitemid 44607179)
41. Milanesi, L., Muselli, M., and Arrigo, P. 1996. Hamming-Clustering method for signals prediction in 5′ and 3′ regions of eukaryotic genes. Comput. Appl. Biosci. 12:399-404.
42. Miura, P. M. K., Jin, J. B., and Hasegawaa, P. M. 2007. Sumoylation, a post-translational regulatory process in plants. Curr. Opin. Plant Biol. 10:495-502. (Pubitemid 47503877)
43. Mor, H., Manulis, S., Zuc, M., Nizan, R., Coplin, D. L., and Barash I. 2001. Genetic organization of the hrp gene cluster and dspAE/BF operon in Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 14:431-436. (Pubitemid 32176740)
44. Moscou, M. J., and Bogdanove, A. J. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326:1501.
45. Nguyen Ba, A. N., Pogoutse, A., Provart, N., and Moses, A. M. 2009. NLStradamus: A simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:202.
46. Nissan, G., Manulis, S., Weinthal, D., Sessa, G., and Barash, I. 2005. Analysis of promoters recognized by HrpL, an alternative sigma-factor protein from Pantoea agglomerans pv. gypsophilae. Mol. Plant-Microbe Interact. 18:634-643. (Pubitemid 40832030)
47. Nissan, G., Manulis-Sasson, S., Weinthal, D. M., Mor, H., Sessa, G., and Barash, I. 2006. The type III effectors HsvG and HsvB of gall-forming Pantoea determine host specificity and function as transcriptional activators. Mol. Microbiol. 61:1118-1131. (Pubitemid 44215417)
48. Nizan, R., Barash, I., Valinsky, L., Lichter, A., and Manulis, S. 1997. The presence of hrp genes on the pathogenicity-associated plasmid of the tumorigenic bacterium Erwinia herbicola pv. gypsophilae. Mol. Plant- Microbe Interact. 10:677-682.
49. Nizan-Koren, R., Manulis, S., Mor, H., Iraki, N. M., and Barash, I. 2003. The regulatory cascade that activates the Hrp regulon in Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 16:249-260. (Pubitemid 36229940)
50. Okuno, M., Arimoto, E., Ikenobu, Y., Nishiara, T., and Imagawa, M. 2001. Dual DNA binding specificity of peroxisome-proliferator-activated receptor gamma controlled by heterodimer formation with retinoid X receptor alpha. Biochem. J. 353:241-249.
51. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
52. Pollastri, G., and McLysaght, A. 2005. Porter: A new, accurate server for protein secondary structure prediction. Bioinformatics 21:1719-1720. (Pubitemid 40542742)
53. Ren, J., Gao, X., Jin, C., Zhul, M., Wang, X., Shaw, A., Wen, L., Yao, X., and Xue, Y. 2009. Systematic study of protein sumoylation: Development of a site-specific predictor of SUMOsp 2.0. Proteomics 9:3409-3412.
54. Römer, P., Strauss, T., Hahn, S., Scholze, H., Morbitzer, R., Grau, J., Bonas, U., and Lahaye, T. 2009. Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 alleles. Plant Physiol. 150:1697-1712.
55. Sibéril, Y., Doireau, P., and Gantet, P. 2001. Plant bZIP G-box binding factors. Eur. J. Biochem. 268:5655-5666.
56. Söding, J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960. (Pubitemid 40467915)
57. Staskawicz, B., Dahlbeck, D., Keen, N., and Napoli, C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
58. Sugio, A., Yang, B., Zhu, T., and White, F. F. 2007. Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFAg1 and OsTFX1 during bacterial blight of rice. Proc. Natl. Acad. Sci. U.S.A. 104:10720-10725. (Pubitemid 47185731)
59. 2- type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biol. 12:689-697.
60. Valinsky, L., Manulis, S., Nizan, R., Ezra, D., and Barash, I. 1998. A pathogenicity gene isolated from the pPATH of Erwinia herbicola pv. gypsophila determines host specificity. Mol. Plant-Microbe Interact. 11:753-762. (Pubitemid 28338709)
61. Weinthal, D., Barash, I., Tzfira, T., Gaba, V., Teper, D., Sessa, G., and Manulis-Sasson, S. 2011. Characterization of nuclear localization signals in the type III effectors HsvG and HsvB of the gall-forming bacterium Pantoea agglomerans. Microbiology 157:1500-1508.
62. Zhou, J.-M., Trifa, Y., Silva, H., Pontier, D., Lam, E., Shah, J., and Klessig, D. F. 2000. NPR1 differentially interacts with members of the TGA/ OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol. Plant-Microbe Interact. 13:191-202. (Pubitemid 30061602)
63. Carnegie Institution for Science Department of Biology website: www-ciwdpb.stanford.edu/publications/methods/aflp.html
64. Conseq server: conseq.tau.ac.il
65. DBS-PRED prediction server: gibk26.bio.kyutech.ac.jp/jouhou/shandar/ netasa/dbs-pred
66. EMBOSS Explorer helixturnhelix server: bioinformatica.cecalc.ula.ve/ cgibin/emboss/helixturnhelix
67. GYM 2.0 helix-turn-helix detection program: http://users.cis.fiu.edu/ ~giri/bioinf/GYM2/welcome.html
68. MEME Suite analysis tools: meme.nbcr.net/meme/intro.html
69. Pôle BioInformatique Lyonnais helix-turn-helix motif prediction server: npsa-pbil.ibcp.fr/cgi-bin/npsa-automat.pl?page=/NPSA/npsa-hth.html
70. Prediction of or helix-loop-helix SUMOsp server: sumosp.biocuckoo.org/ online.php
71. UniProt database: www.uniprot.org
72. University of Albany DB-Bind server: lcg.rit.albany.edu/dp-bind/
73. University of Toronto NLStradamus webpage: www.moseslab.csb.utoronto.ca/ NLStradamus
74. Webgene Zeus 2 analysis tool: zeus2.itb.cnr.it/~webgene/wwwHC-tata.html