Recent evolution of bacterial pathogens: The gall-forming pantoea agglomerans case

Annual Review of Phytopathology

Volumn 47, Issue , 2009, Pages 133-152

  Barash, Isaac ^a   Manulis Sasson, Shulamit ^b  

^a TEL AVIV UNIVERSITY   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

Auxin; Cytokinins; Host specificity; Hrp hrc gene cluster; Pathogenicity island; Quorum sensing regulation

Indexed keywords

ARTICLE; EVOLUTION; GENETICS; GENOMIC ISLAND; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PANTOEA; PATHOGENICITY; PLANT TUMOR;

EVOLUTION; GENE TRANSFER, HORIZONTAL; GENOMIC ISLANDS; HOST-PATHOGEN INTERACTIONS; PANTOEA; PLANT TUMORS;

BACTERIA (MICROORGANISMS); PANTOEA; PANTOEA AGGLOMERANS;

EID: 69549121269     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080508-081803     Document Type: Article

References (114)

1. Abeles FB, Morgan PW, Saitveit ME. 1992. Ethylene in Plant Biology. San Diego, CA: Academic
2. Allano JR, Colimer A. 2004. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42:385414
3. 3. Arnold DL, Pitman A, Jackson RW. 2003. Pathogenicity and other genomic islands in plant pathogenic bacteria. Md. Plant Pathol. 4:404-420 (Pubitemid 37144131)
4. Barash I, Manulis-Sasson S. 2007. Virulence mechanisms and host specificity of gall-forming Pantoea agglomerans. Trends Microbiol. 15:53845
5. Barash I, Panijei M, Gurel F, Chalupowicz L, Manulis S. 2005. Transformation of Pantoea agglomerans into a tumorigenic pathogen. In Proceedings of the 1st International Conference on Plant-Microbe Interactions: Endophytes and Biocontrol Agents, ed. S Sorvari, O Toldi, pp. 10-19. Lapland, Finland: Saariselka
6. 6. Beji A, Mergaert J, Gavini F, Izard D, Kersters K, et al. 1988. Subjective synonymy of Erwinia herbicola, Erwinia milletiae, and Enterobacter agglomerant and redefinition of the taxon by genotypic and phenotypic data. Int. J. Syst. Bacteriol. 38:77-88 (Pubitemid 18029016)
7. 7. Best VM, Vasanthakumar A, McManus PC. 2004. Anatomy of cranberry stem gall and localization of bacteria in galls. Phytopathology 94:1172-1177 (Pubitemid 39448194)
8. Binns AN, Costantino P. 1998. The Agrobacterium oncogenes. In The Rhizobiaceae, Molecular Biology of Model Plant-Associated Bacteria, ed. ITP Spaink, A Kondorosi, PJJ Hooykaas. pp. 251-266 Dordrecht/Boston/London: Kluwer Academic
9. Boucher CA, Martinel A, Barberis P, Alloing G, Zischek C. 1986. Virulence genes are carried, by a megaplasmid of the plant pathogen Pseudomonas solanacearum. Mol. Gen. Genet. 205:270-275
10. Brady CL, Venter SN, Cleenwerck I, Vancanney M, Swings J, Coutinho TA. 2006. Examining the taxonomy of the genus Pantoea. Proc. Int. Conf Plant Pathog. Bact., 11th, Edinburgh, pp. 23-24
11. Brandi MT, Lindow SE. 1996. Cloning and characterization of a locus encoding an indolepyruvate decarboxylase involved in indole-3-acetic acid synthesis in Erwinia herbicola. Appl. Environ. Microbiol. 62:4121-4128
12. Brandi MT, Lindow SE. 1997. Environmental signals modulate the expression of anindole-3-acetic acid biosynthetic gene in Erwinia herbicola. Mol. Plant-Microbe Interact. 10:499-505
13. 13. Brandi MT, Quinones B, Lindow SE. 2001. Heterogenous transcription of an indole-3-acetic acid biosynthetic gene in Erwinia herbicola on plant surfaces. Proc. Natl. Acad. Sci. USA. 98:3454-3459 (Pubitemid 32220866)
14. BrussowH, Canchaya C, Hardt WD. 2004. Phages and evolution of bacterial pathogens: from genomic rearrangement to lysogenic conversion. Microbiol. Mol, Biol, Rev. 68:560-602
15. Buchanan BB, Gruissem W, Jones RL. 2000. Biochemistry and Molecular Biology of Plants. Rockville, MD: Am. Soc. Plant Physiol. 1367 pp.
16. Burr TJ, Katz BIT, Abawi GS, Crosier DC. 1991. Comparison of tumorigenic strains ofErwinia herbicola isolated from table beet with E. herbicola gypsophilae. Plant Dis. 75:855-858
17. Chalupowicz L, Barash I, Panijei M, Sessa G, Manulis-Sasson S. 2009. Regulatory interactions between quorum-sensing, auxin, cytokinin and hrp-regulatory genes in relation to gall formation and epiphytic fitness of Pantoea agghmerans pv. gypsophilae. Mol, Plant-Microbe Interact. 22:in press
18. 18. Chalupowicz L, Barash I, Schwartz M, Aloni R, Manulis S. 2006. Comparative anatomy of gall development on Gypsophila paniculata induced by bacteria with different mechanisms of pathogenicity. Planta 224:429-437 (Pubitemid 43946060)
19. Chalupowicz L, Manulis-Sasson M, Itkin M, Sacher A, Sessa G, Barash I. 2008. Quorum sensing system affects gall development incited by Pantoea agglomerans pv. gypsophilae. Mol. Plant-Microbe Interact. 21:1094-1105
20. Christie PJ. 2004. The Agrobacterium Ti plasmids. In Plasmid Biology, ed. BE Funnel, G-J Philips, pp. 455-572. Washington, DC: ASM Press.
21. Clark E, Manulis S, Ophir Y, Barash I, Gafni Y. 1993. Cloning and characterization of iaaM and iaa H from Erwinia herbicola pathovar gypsophilae. Phytopathology 83:23440
22. Cooksey DA. 1986. Galls of Gypsophila paniculata caused by Erwinia herbicola. Plant Dis. 70:464-468
23. CostacurtaA, VanderleydenJ. 1995. Synthesis ofphytohormones by plant-associated bacteria. Crit. Rev. Microbiol. 21:1-18
24. Couturier M, Bex F, Bergquist PL, Maas WK. 1988. Identification and classification of bacterial plasmids. Microbiol. Rev. 52:375-395
25. Crespi M, Messens E, Capiau AB, van Montagu M, Desomer J. 1992. Fasciation induction by the phytopatliogen Rhodococcus fasdans depends upon a linear plasmid encoding a cytokinin synthase gene. EMBOJ. 11:795-804
26. Cruz AT, Cazacu AC, Al CH. 2007. Pantoea agglomerans, a plant pathogen causing human disease. J Clin. Microbiol. 45:1989-92
27. Day WAJr, Fernandez RE, Maureili AT. 2001. Patlioadaptive mutations that enhance virulence: genetic organization of the cadA. region of Shigella spp. Infect. Immune. 69:7471-7480
28. 28. Ehrbar K, Hardt WD. 2005. Bacteriophage-encoded type III effectors in Salmonella entérica subspecies I. serovar typhimurium. Infect. Genet. Evol. 5:1-9 (Pubitemid 39619012)
29. Ehg plasmid of Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 13:693-698
30. 30. Ezra D, Barash I, Weinthal DM, Ciaba V, Manulis S. 2004. pthG from Pantoea agglomerans pv. gypsophilae encodes an avirulence effector that determines incompatibility in multiple beet species. Mol. Plant Pathol. 5:105-114 (Pubitemid 38370325)
31. 31. Gafni Y, Manulis S, Kunik T, Lichter A, Barash I, Ophir Y. 1997. Characterization of the auxin synthesis genes of Erwinia herbicoola pv. gypsophilae. Israel J. Plant Sci. 45:279-284 (Pubitemid 28195170)
32. 32. Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, et al. 1989. Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov. Int. J. Syst. Bacterial. 39:33745 (Pubitemid 19175054)
33. 33. Geldner N, Firml J, Stierhof YD, Jurgens G, Palme K. 2001. Auxin transport inhibitors block PINl and vesicle trafficking. Nature 413:425-428 (Pubitemid 32928597)
34. Genin S, Boucher C. 2004. Lessons learned from the genome analysis of Ralstonia solanacearum. Annu. Rev. Phytopathol. 42:107-134
35. Gibbon MJ, Sesma A, Canal A, Wood JR, Hidalgo E, et al. 1999. Replication regions from plantpadiogenic Pseudomonassyringae plasmids are similar to ColE2-reiated replicons. Microbiology 145:3 2 5-34
36. 36. Giladi H, Gottesman M, Oppenheim AB. 1990. Integration host factor stimulates the phage lambda pL promoter. J. Mol. Biol. 213:109-121 (Pubitemid 20171100)
37. Goto M, Nakano M. 1978. Effects of mechanical injuries on wound-induced gall formation at different growth stages of kidney bean (Phaseolm vulgaris L.).Jpn. Soc. Hort. Sci. 47:365-369
38. Grant SR, Fisher EJ, Chag JH, Mole BM, Dangl JL. 2006. Subterfuge and manipulation: type III effector proteins of phytopadiogenic bacteria. Annu. Rev. Microbiol. 60:42549
39. 39. Guo M, Manulis S, Barash I, Lichter A. 2001. The operon for cytokinin biosynthesis of Erwinia herbicola pv. gypsophilae contains two promoters and is plant-induced. Can. J. Microbiol. 47:1126-1131 (Pubitemid 34194276)
40. 40. Guo M, Manulis S, Mor H, Barash I. 2002. The presence of diverse IS elements and an avrPphD homologue that acts as a virulence factor on the pathogenicity plasmid of Erwinia herbicola pv. gypsophilae. Mol, Plant-Microbe Interact. 15:709-716 (Pubitemid 34780480)
41. 41. Gurlebeck D, Thieme F, Bonas U. 2006. Type III effector proteins from the plant padiogenXanthomonas and their role in interaction with the host plant. J. Plant Physiol. 163:23 3-55 (Pubitemid 43112080)
42. Hacker J, Kaper JB. 1999. The concept of pathogenicity islands. See Ref. 50, pp. 1-11
43. Hacker J, Kaper JB. 2000. Padiogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54:641-679
44. Herbers K, Conrads-Strauch J, Bonas U. 1992. Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356:172-174
45. Iacobellis NS, Sisto A, Surico G, Evidente A, DiMaio E. 1994. Pathogenicity of Pseudomonas syringa-e subsp. savastanoi mutants defective in phytohormone production. J. Phytopathol. 140:23848
46. IchikawaT, Syono K. 1991. Tobacco genetic tumors. Plant Cell Physiol. 32:1123-1128
47. 47. Jackson JF, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, et al. 1999. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean padiogen Pseudomonas syringae patliovar phaseolicola. Proc. Natl. Acad. Sci. USA 96:10875-10880 (Pubitemid 29442237)
48. Janda J. 2006. New members of the family Enterobacteriaceae. in Prokaryotes, ed. M Dworkin, S Falkow, E Rosenberg, K-H Schleifer, E Stackebrandt, pp. 540. New York: Springer
49. Kamiunten IT. 1999. Isolation and characterization of virulence gene psvA on a plasmid of Pseudomonas syringae pv. eriobotryae. Ann. Phytopathol. Soc.Jpn. 65:501-509
50. Kaper JB, Hacker J, eds. 1999. "Pathogenicity Islands and Other Mobile Viruleme Elements." WashingtǒDC: ASM Press. 352 pp.
51. 51. Kay S, Halin S, Marois E, Hause G, Bonas U. 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 31.8:648-651 (Pubitemid 350014839)
52. Kelly WL. 1998. The j-domain family and the recruitment of chaperone power. Trends Biochem. Sci. 23:222-227
53. Kobayashi DY, Palumbo JD. 2000. Bacterial endophytes and their effects on plants and uses in agriculture. In Microbial Endophytes, ed. CW Bacon, JF White Jr, pp. 199-233. Basel, Switzerland: Marcel Dekker.
54. Krishnan BR, Iyer LM. 1988. Host range of the IncN group plasmid pCUl and its minireplicon in gram negative purple bacteria. Appl. Environ. Microbiol. 54:2273-2276
55. Kues U, Stahl U. 1989. Replication of plasmids in gram-negative bacteria. Microbiol. Rev. 53:491-513
56. 56. Lawrence JG. 1999. Gene transfer, speciation, and the evolution of bacterial genomes. Curr. Opin. Microbiol. 5:519-523 (Pubitemid 29477180)
57. Le Gail T, Mavris M, Martino MC, Bernardini ML, Denamur E, Parsot C. 2005. Analysis of virulence plasmid gene expression defines diree classes of effectors in the type III system of Shigella flexneri. Microbiology 151:951-962
58. Lichter A, Barash I, Valinsky L, Manulis S. 1995. The genes involved in cytokinin biosynthesis in Erwinia herbicola pv. gypsophilae: characterization and role in gall formation. J. Bacterial. 177:4457-4465
59. Lichter A, Manulis S, Sagee O, Gafni Y, Gray J, et al. 1995. Production of cytokinins by Erwinia herbicola pv. gypsophilae and isolation of a locus conferring cytokinin biosynthesis. Mol. Plant-Microbe Interact. 8:114. 4-21.
60. 60. Lichter A, Manulis S, Valinsky I., Karniol B, Barash I. 1996. IS1327, a new insertion-like element in the pathogenicity-associated plasmid of Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 9:98-104 (Pubitemid 2623836)
61. Lindeberg M, Stavrinides J, Change JH, Alfano JR, Collmer A, et al. 2005. Proposed guidelines for unified nomenclature and phylogenetic analysis of type III hop effector proteins in the plant pathogen Pseudomonas syringae. Mol. Plant-Microbe Interact. 18:275-282
62. Lindow SE, Brandi M. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875-1883
63. MahillonJ, Chandler M. 1998. Insertion sequences. Microbiol. Mol. Biol, Rev. 62:725-774
64. 64. Malathum K, Singh KV, Weinstock GM, Murray BE. 1998. Repetitive sequence-based PCR versus pulsed-field gel electrophoresis for typing of Enterococcus faecalis at subspecies level. J. Clin. Microbiol. 36:21.1-15 (Pubitemid 28047461)
65. Manulis M, Barash I. 2003. The molecular basis for transformation of an. epiphyte into a gall-forming pathogen as exemplified by Erwinia herbicola pv. gypsophilae. In Plant-Microbe Interactions, ed. G Stacey, N Keen, pp. 19-52. St. Paul, MN: American Phytopathological Society
66. Manulis S, Gafni Y, Clark E, Zutra D, OpMr Y, Barash I. 1991. Identification of a plasmid DNA probe for detection of Erwinia herbicola pathogenic on Gypsophila paniculata. Phytopathology 81:54-57
67. 67. Manulis S, Haviv-Cliesner A, Brandi MT, Lindow SE, Barash I. 1998. Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol, Plant-Microbe Interact. 11:634-642 (Pubitemid 28417753)
68. Manulis S, Valinsky L, Gafni Y, Hershenhom J. 1991. Indole-3-acetic acid biosynthetic pathways in Erwinia herbicola in relation to padiogenicity on Gypsophila paniculata. Physiol. Mol. Plant Pathol. 39:161-171
69. Mecsas J, Strauss EJ. 1996. Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg. Infect. Dis. 2:271-288
70. 70. Montesano M, Brader G, Paiva ET. 2003. Pathogen derived elicitors: searching for receptors in plants. Mol. Plant Pathol. 4:73-79 (Pubitemid 36093361)
71. 71. Mor IT, Manulis S, Zuc M, Nizan R, Coplin DL, Barash I. 2001. Genetic organization of die hrp gene cluster and dspAE/BF operon in Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 14:431-436 (Pubitemid 32176740)
72. Morris RO. 1986. Genes specifying auxin and cytokinin biosynthesis in phytopatliogens. Annu. Rev. Plant Physiol. 37:509-538
73. 73. Mudgett M. 2005. New insights to the function of phytopadiogenic bacterial type III effectors in plants. Annu. Rev. Plant Biol. 56:509-531 (Pubitemid 40802420)
74. Nissan G, Manulis S, Barash I. 2003. Molecular determinants affecting activity of the virulence effectors, PtIiG and HsvG of Erwinia herbicola pv. gypsophilae. Int. Congr. Molec. Plant-Microbe Interact., 11th, St. Petersburg, Russia, p. 152
75. Nissan G, Manulis S, Weintlial D, Sessa. G, Barash I. 2005. Analysis of promoters recognized by HrpL, an alternative sigma-factor protein from Pantoea agglomerans pv. gypsophilae. Mol, Plant-Microbe Interact. 18:63443
76. Nissan G. 2005. Elucidating the mode of action and regulation of type III virulence effectors in the tumorigenic bacterium Pantoea agglomerans. Ph.D. Thesis, Tel-Aviv University, 107 pp.
77. 76. Nissan G, Manulis-Sasson S, Weintlial DM, Mor H, Sessa G, 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)
78. Nizan R, Barash I, Valinsky L, Lichter A, Manulis S. 1997. The presence of hrp genes on the padiogenicity-associated plasmid of the tumorigenic bacterium Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 10:677-682
79. Nizan-Koren R, Manulis S, Mor IT, Iraki N, Barash I. 2003. The regulatory cascade that activates the Hrp regulon in Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 15:1249-1260
80. Ochman IT, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and die nature of bacterial innovation. Nature 405:299-304
81. Okuno M, Arimoto E, Ikenobu Y, Nishiara T, Imagawa M. 2001. Dual DNA binding specificity of peroxisome-proliferator-activated receptor gamma controlled by heterodimer formation with retinoid Xreceptor alpha. Biochem. J. 353:241-249
82. OttenL, Schmidt J. 1998. AT-DNA from the Agrobacterium tumefacienslimked-host-range strain A.B2/73 contains a single oncogene. MoI. Plant-Microbe Interact. 11:33 5-42
83. Patten CL, Click BR. 1996. Bacterial biosynthesis of indole-3-acetic acid. Can. J. Microbiol. 42:207-20
84. SalanoubatM, Genin S, Artiguenave F, Gouzy J, Mangenot S, et al. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502
85. 83. Sauer F, Tjian R. 1997. Mechanisms of transcriptional activation: differences and similarities between yeast, Drosophila and man. Curr. Opin. Genet. Dev. 7:176-181 (Pubitemid 27206755)
86. 84. Sisto A, Cipriani MG, Morea M. 2004. Knot formation caused by Pseudomonas syringae subsp. savastanoi on olive plants is hrp-dependent. Phytopathology 94:484-489 (Pubitemid 38522275)
87. 85. Small PL, Falkow S. 1988. Identification of regions on a 230-kilobase plasmid from enteroinvasive Escherichia coli that are required for entry into HEp-2 cells. Infect. Immun. 56:225-229 (Pubitemid 18032155)
88. Snyder L, Champness W. 1997. Molecular Genetics of Bacteria. Washington, DC: ASM Press. 504 pp.
89. Sokurenko EV, Hasty DL, Dykhuizen DE. 1999. Pathoadaptive mutations: gene loss and variation in bacterial padiogens. Trends Microbiol. 7:191-195
90. Sota M, Top EM. 2008. Horizontal gene transfer mediated by plasmids. In Plasmids, ed. G Lipps. Norfolk, UK: Caister Academic
91. 89. Spaepen S, Vanderleyden J, Remans R. 2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMSMicrobiol. Rev. 31:42548 (Pubitemid 46920250)
92. Spooner BM, Bowdery JP. 1993. Check list of British gall causing organisms: progress report 1992. Cecidology 8:31-35
93. Stahl EA, Bishop JG. 2000. Plant-pathogen anus races at the molecular level. Curr. Opin. Plant Biol. 3:299-304
94. Starr MP. 1981. The genus Erwinia. In The Prokaryotes, ed. MP Star, HG Truper, A Balows, HG Schlegel, pp. 1260-1271 Berlin: Springer-Verlag
95. Starvinides J, McCann HC, Guttman DS. 2008. Host-pathogen interplay and the evolution of bacterial effectors. Cell. Microbiol. 10:285-292
96. Stukenbrock IT, McDonald BA. 2008. The origins of plant pathogens in agro-ecosystems. Annu, Rev. Phytopathol. 46:75-100
97. Sundin GW. 2007. Genomic insights into the contribution of phytopadiogenic bacterial plasmids to the evolutionary history of their hosts. Annu. Rev. Phytopathol. 45:129-151
98. 96. Tang X, Xiao Y, Zhou J-M. 2006. Regulation of the type III secretion system in phytopadiogenic bacteria. Mol. Plant-Microbe Interact. 19:1159-1166 (Pubitemid 44607328)
99. 97. Taniguehi T, O'Neill M, de Crombrugghe B. 1979. Interaction site of Escherichia coli AMP receptor protein on DNA galactose operon promoters. Proc. Natl. Acad. Sci, USA 76:5090-5094 (Pubitemid 10231827)
100. 98. Valinsky L, Manulis S, Nizan R, Ezra D, Barash I. 1998. A padiogenicity gene isolated from the pPATH of Erwinia herbicola pv. gypsophilae determines host specificity. Mol. Plant-Microbe Interact. 11:753-762 (Pubitemid 28338709)
101. 99. Valinsky L, Nisan I, Tu X, Nisan G, Rosenshine I, et al. 2002. A host-specific virulence protein of Erwinia herbicola pv. gypsophilae is translocated into human epithelial cells by the type III secretion system. of enteropatliogenic Escherichia coli. Mol. Plant Pathol. 3:97-101 (Pubitemid 34231429)
102. 100. Vandeputte O, Oden S, Mol A, Vereecke D, Goethals K, et al. 2005. Biosynthesis of auxin by grampositive phytopatliogen Rhodococcus fascians is controlled by compounds specific to infected, plant tissues. Appl. Environ. Microbiol. 7.1:1169-1177 (Pubitemid 40396652)
103. 101. Vasanthakumar A, McManus PC. 2004. Indole-3-acetic acid-producing bacteria are associated with cranberry stem. gall. Phytopathology 94:1164-1171 (Pubitemid 39448193)
104. 102. Vivian A, Murillo J, Jackson RW. 2001. The role of plasmids in phytopadiogenic bacteria: mobile arsenals? Microbiology 147:763-780 (Pubitemid 32401317)
105. Volcani Z. 1985. Bacterial Diseases of Plana in Israel. Bet Dagan, Israel: Agricultural Research Organization, the Volcani Center. 388 pp.
106. von. Bodman SB, Bauer WD, Coplin DL. 2003. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41:455-482
107. Weintlial DM. 2008. Plasmid-borne pathogenidty determinants in Pantoea agglomerans pv. gypsophilae and betae: mechanism of virulence and their distribution. Ph.D. thesis, Tel-Aviv University, 120 pp.
108. Weinthal DM, Barash I, Panijei M, Valinsky L, Gaba V, Manulis-Sasson S. 2007. Distribution and replication of the pathogenicity plasmid pPATH in diverse populations of the gall-forming Pantoea agglomerans. Appl. Environ. Microbiol. 73:7552-7561
109. Weinthal DM, Manulis-Sasson S, Nissan G, Tzfira T, Sessa G, Barash I. 2008. Identification of NLS signals and a DNA binding domain in the host specificity determinants HsvG and HsvB of the gallforming Pantoea agglomerans. Phytopathology 98:S169
110. Williams MAJ. 2004. Plant galls: a perspective, in Plant Galls, ed. MAJ Williams, pp. 1-7. Oxford: Clarendon Press
111. 109. Yamada T, Palm CJ, Brook B, Kosuge T. 1985. Nucleotide sequence of the Pseudomonas savastanoi indole acetic acid genes show homology with Agrobacterium tumefadens T-DNA. Proc. Natl. Acad. Sci. USA 82:6522-6526 (Pubitemid 16230546)
112. Yamada Y. 1993. The role of auxin in plant-disease development. Annu. Rev. Phytopathol. 31:253-273
113. 111. Yang SF, Zhang Q, Guo J, Charkowski AO, Click BR, et al. 2007. Global effect of indole-3-acetic acid (IAA) biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl, Environ. Microbiol. 73:1079-1088 (Pubitemid 46303223)
114. Yang Y, Gabriel DW. 1995. Intragenic recombination of a single plant pathogen, gene provides a mechanism for the evolution of new host specificities. J. Bacterial. 177:4963-4968