the bacterium Pantoea stewartii uses two different type III secretion systems to colonize its plant host and insect vector

Applied and Environmental Microbiology

Volumn 78, Issue 17, 2012, Pages 6327-6336

  Correa, Valdir R ^a   Majerczak, Doris R ^b   Ammar, El Desouky ^a,d   Merighi, Massimo ^b,e   Pratt, Richard C ^a,f   Hogenhout, Saskia A ^c   Coplin, David L ^b   Redinbaugh, Margaret G ^b,d  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c JOHN INNES CENTRE   (United Kingdom)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e Glycosyn Inc   (United States)

^f NEW MEXICO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL PATHOGENS; BACTERIAL WILT; CAUSATIVE AGENTS; ECTOPIC EXPRESSIONS; FLEA BEETLES; HOST CELLS; LEAF BLIGHTS; NEEDLE-LIKE; PANTOEA; PLANT HOSTS; TYPE III SECRETION SYSTEM;

ANIMALS; BACTERIA; PHYSIOLOGY; TISSUE;

GENE EXPRESSION;

BACTERIAL DNA; BACTERIAL PROTEIN; VIRULENCE FACTOR;

BACTERIAL DISEASE; BACTERIUM; BEETLE; COLONIZATION; HOST PLANT; LIFE CYCLE; MAIZE; PATHOGEN; PATHOGENICITY; PERSISTENCE; PHENOTYPE; PHYLOGENETICS; PROTEIN; SECRETION;

ANIMAL; ARTICLE; BACTERIAL SECRETION SYSTEM; BEETLE; CHEMISTRY; DISEASE CARRIER; DNA SEQUENCE; GENE DELETION; GENETIC COMPLEMENTATION; GENETICS; MAIZE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PANTOEA; PATHOGENICITY; PLANT DISEASE; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BEETLES; DNA, BACTERIAL; GENE DELETION; GENETIC COMPLEMENTATION TEST; INSECT VECTORS; MOLECULAR SEQUENCE DATA; PANTOEA; PLANT DISEASES; SEQUENCE ANALYSIS, DNA; VIRULENCE; VIRULENCE FACTORS; ZEA MAYS;

ALTICINI; ANIMALIA; BACTERIA (MICROORGANISMS); CHAETOCNEMA PULICARIA; COLEOPTERA; HEXAPODA; PANTOEA; PANTOEA STEWARTII; PANTOEA STEWARTII SUBSP. STEWARTII; ZEA MAYS;

EID: 84866150188     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00892-12     Document Type: Article

References (60)

1. Ammar ED, Hogenhout SA. 2008. A neurotropic route for Maize mosaic virus (Rhabdoviridae) in its planthopper vector Peregrinus maidis. Virus Res. 131:77-85.
2. Basset A, Tzou P, Lemaitre B, Boccard F. 2003. A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Rep. 4:205-209.
3. Beck von Bodman S, Farrand SK. 1995. Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J. Bacteriol. 177:5000-5008.
4. Blocker A, et al. 2001. Structure and composition of the Shigella flexneri "needle complex", a part of its type III secreton. Mol. Microbiol. 39:652-663.
5. Boyer HW, Roulland-Dussoix D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
6. Cesbron S, Paulin JP, Tharaud M, Barny MA, Brisset MN. 2006. The alternative sigma factor HrpL negatively modulates the flagellar system in the phytopathogenic bacterium Erwinia amylovora under hrp-inducing conditions. FEMS Microbiol. Lett. 257:221-227.
7. Claflin LE. 1999. Stewart's bacterial wilt, 3rd ed. American Phytopathological Society, St. Paul, MN.
8. Coplin DL, Frederick RD, Majerczak DR, Haas ES. 1986. Molecular cloning of virulence genes from Erwinia stewartii. J. Bacteriol. 168:619-623.
9. Coplin DL, Majerczak DR. 1990. Extracellular polysaccharide genes in Erwinia stewartii: directed mutagenesis and complementation analysis. Mol. Plant Microbe Interact. 3:286-292.
10. Coplin DL, et al. 2002. Identification of Pantoea stewartii subsp. stewartii by PCR and strain differentiation by PFGE. Plant Dis. 86:304-311.
11. Dale C, Young SA, Haydon DT, Welburn SC. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. U. S. A. 98:1883-1888.
12. Dale C, Jones T, Pontes M. 2005. Degenerative evolution and functional diversification of type-III secretion systems in the insect endosymbiont Sodalis glossinidius. Mol. Biol. Evol. 22:758-766.
13. Deiwick J, et al. 1998. Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J. Bacteriol. 180:4775-4780.
14. Dereeper A, et al. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469.
15. Elliot C, Poos FW. 1934. Overwintering of Aplanobacter stewartii. Science 80:289-290.
16. Elliott C, Poos FW. 1940. Seasonal development, insect vectors, and host range of bacterial wilt of sweet corn. J. Agric. Res. 60:645-686.
17. Epler CR, Dickenson NE, Olive AJ, Picking WL, Picking WD. 2009. Liposomes recruit IpaC to the Shigella type III secretion apparatus needle as a final step in secretion induction. Infect. Immun. 77:2754-2761.
18. Esker PD, Nutter FW. 2003. Temporal dynamics of corn flea beetle populations infested with Pantoea stewartii, causal agent of Stewart's disease of corn. Phytopathology 93:210-218.
19. Figurski DH, Helinski DR. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652.
20. Foultier B, Troisfontaines P, Muller S, Opperdoes FR, Cornelis GR. 2002. Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J. Mol. Evol. 55:37-51.
21. Foultier B, et al. 2003. Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system. Infect. Immun. 71:242-253.
22. Fouts DE, et al. 2002. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. U. S. A. 99:2275-2280.
23. Frederick RD, et al. 2001. Genetic organization of the Pantoea stewartii subsp. stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN, and wtsE operons. Mol. Plant Microbe Interact. 14:1213-1222.
24. Glasner JD, et al. 2003. ASAP, a systematic annotation package for community analysis of genomes. Nucleic Acids Res. 31:147-151.
25. Grenier AM, Duport G, Pages S, Condemine G, Rahbe Y. 2006. The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl. Environ. Microbiol. 72:1956-1965.
26. Guttman DS, Gropp SJ, Morgan RL, Wang PW. 2006. Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Mol. Biol. Evol. 23:2342-2354.
27. Ham JH, Majerczak DR, Arroyo-Rodriguez AL, Mackey DM, Coplin DL. 2006. WtsE, an AvrE-family effector protein from Pantoea stewartii subsp. stewartii, causes disease-associated cell death in maize and requires a chaperone protein for stability. Mol. Plant Microbe Interact. 19:1092-1102.
28. Harlow E, Lane D. 1998. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Huang Y, Suyemoto M, Garner CD, Cicconi KM, Altier C. 2008. Formate acts as a diffusible signal to induce Salmonella invasion. J. Bacteriol. 190:4233-4241.
30. Huson DH, et al. 2007. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8:460.
31. Ivanoff SS. 1933. Stewart's wilt disease of corn, with emphasis on the life history of Phytomonas stewartii in relation to pathogenesis. J. Agr. Res. 47:749-770.
32. Jin Q, He SY. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-2558.
33. Kane CD, Schuch R, Day WA, Jr, Maurelli AT. 2002. MxiE regulates intracellular expression of factors secreted by the Shigella flexneri 2a type III secretion system. J. Bacteriol. 184:4409-4419.
34. Keen NT, Tamaki S, Kobayashi D, Trollinger D. 1988. Improved broadhost-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70:191-197.
35. Keen NT, Ridgway D, Boyd C. 1992. Cloning and characterization of a phospholipase gene from Erwinia chrysanthemi EC16. Mol. Microbiol. 6:179-187.
36. Killiny N, Almeida RP. 2009. Xylella fastidiosa afimbrial adhesins mediate cell transmission to plants by leafhopper vectors. Appl. Environ. Microbiol. 75:521-528.
37. Kube M, et al. 2008. The genome of Erwinia tasmaniensis strain Et1/99, a non-pathogenic bacterium in the genus Erwinia. Environ. Microbiol. 10: 2211-2222.
38. Lorenz C, Buttner D. 2009. Functional characterization of the type III secretion ATPase HrcN from the plant pathogen Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 191:1414-1428.
39. Menard R, Sansonetti PJ, Parsot C. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
40. Merighi M, Majerczak DR, Stover EH, Coplin DL. 2003. The HrpX/HrpY two-component system activates hrpS expression, the first step in the regulatory cascade controlling the Hrp regulon in Pantoea stewartii subsp. stewartii. Mol. Plant Microbe Interact. 16:238-248.
41. Merighi M, Majerczak DR, Zianni M, Tessanne K, Coplin DL. 2006. Molecular characterization of Pantoea stewartii subsp. stewartii HrpY, a conserved response regulator of the Hrp type III secretion system, and its interaction with the hrpS promoter. J. Bacteriol. 188:5089-5100.
42. Metcalf WW, et al. 1996. Conditionally replicative and conjugative plasmids carrying lacZα for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35:1-13.
43. Mitchell RF, Hanks LM. 2009. Insect frass as a pathway for transmission of bacterial wilt of cucurbits. Environ. Entomol. 38:395-403.
44. Moraes TF, Spreter T, Strynadka NC. 2008. Piecing together the type III injectisome of bacterial pathogens. Curr. Opin. Struct. Biol. 18:258-266.
45. Mueller CA, Broz P, Cornelis GR. 2008. The type III secretion system tip complex and translocon. Mol. Microbiol. 68:1085-1095.
46. Nadarasah G, Stavrinides J. 2011. Insects as alternative hosts for phytopathogenic bacteria. FEMS Microbiol. Rev. 35:555-575.
47. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Shea JE, Hensel M, Gleeson C, Holden DW. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. U. S. A. 93:2593-2597.
49. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gramnegative bacteria. Biotechnology 1:784-794.
50. Stavrinides J, McCann HC, Guttman DS. 2008. Host-pathogen interplay and the evolution of bacterial effectors. Cell Microbiol. 10:285-292.
51. Stavrinides J, McCloskey JK, Ochman H. 2009. Pea aphid as both hostand vector for the phytopathogenic bacterium Pseudomonas syringae. Appl. Environ. Microbiol. 75:2230-2235.
52. Stavrinides J, No A, Ochman H. 2010. A single genetic locus in the phytopathogen Pantoea stewartii enables gut colonization and pathogenicity in an insect host. Environ. Microbiol. 12:147-155.
53. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
54. Troisfontaines P, Cornelis GR. 2005. Type III secretion: more systems than you think. Physiology (Bethesda) 20:326-339.
55. Tsuchiya K, d'Ursel CCM, Nozu YY. 2004. Production and preliminary characterization of monoclonal antibodies raised against Xanthomonas campestris pv. mangiferaeindicae. J. Gen. Plant Pathol. 70:27-33.
56. Venecia K, Young GM. 2005. Environmental regulation and virulence attributes of the Ysa type III secretion system of Yersinia enterocolitica biovar 1B. Infect. Immun. 73:5961-5977.
57. Young BM, Young GM. 2002. Evidence for targeting of Yop effectors by the chromosomally encoded Ysa type III secretion system of Yersinia enterocolitica. J. Bacteriol. 184:5563-5571.
58. Young BM, Young GM. 2002. YplA is exported by the Ysc, Ysa, and flagellar type III secretion systems of Yersinia enterocolitica. J. Bacteriol. 184:1324-1334.
59. Zandjanaku-Tachin M, Fanou A, Gall PL, Wydra K. 2007. Detection, survival and transmission of Xanthomonas axonopodis pv. manihotis and X. axonopodis pv. vignicola, causal agents of cassava and cowpea bacterial blight, respectively, in/by insect vectors. J. Phytopathol. 155: 159-169.
60. Zurawski DV, Mitsuhata C, Mumy KL, McCormick BA, Maurelli AT. 2006. OspF and OspC1 are Shigella flexneri type III secretion system effectors that are required for postinvasion aspects of virulence. Infect. Immun. 4:5964-5976.