Sequences essential for transmission of spiroplasma citri by Its leafhopper vector, circulifer haematoceps, revealed by plasmid curing and replacement based on incompatibility

Applied and Environmental Microbiology

Volumn 76, Issue 10, 2010, Pages 3198-3205

  Breton, Marc ^a   Duret, Sybille ^a   Danet, Jean Luc ^a   Dubrana, Marie Pierre ^a   Renaudin, Joël ^a  

^a Univ Bordeaux   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CODING SEQUENCES; HYDROPHILIC PROTEIN; LEAFHOPPER VECTOR; MEMBRANE PROTEINS; MUTANT STRAIN; REPLACEMENT STRATEGY; SPIROPLASMAS; WILD-TYPE STRAIN;

BIOLOGICAL MEMBRANES; ENCODING (SYMBOLS); MICROBIOLOGY;

PROTEINS;

BACTERIUM; DISEASE VECTOR; GENETICS; INCOMPATIBILITY; INSECT; PLASMID; PROTEIN;

ANIMAL; ARTICLE; DISEASE CARRIER; GENETICS; HEMIPTERA; METABOLISM; MICROBIOLOGY; MUTATION; PLASMID; SPIROPLASMA CITRI;

ANIMALS; HEMIPTERA; INSECT VECTORS; MUTATION; PLASMIDS; SPIROPLASMA CITRI;

CIRCULIFER HAEMATOCEPS; HEXAPODA; SPIROPLASMA; SPIROPLASMA CITRI;

EID: 77952253005     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00181-10     Document Type: Article

References (44)

1. André, A., W. Maccheroni, F. Doignon, M. Garnier, and J. Renaudin. 2003. Glucose and trehalose PTS permeases of Spiroplasma citri probably share a single IIA domain, enabling the spiroplasma to adapt quickly to carbohydrate changes in its environment. Microbiology 149:2687-2696.
2. Bai, X., T. Fazzolari, and S. A. Hogenhout. 2004. Identification and characterization of traE genes of Spiroplasma kunkelii. Gene 336:81-91.
3. Berg, M., U. Melcher, and J. Fletcher. 2001. Characterization of Spiroplasma citri adhesion related protein SARP1, which contains a domain of a novel family designated sarpin. Gene 275:57-64.
4. 4. Berho, N., S. Duret, J. L. Danet, and J. Renaudin. 2006. Plasmid pSci6 from Spiroplasma citri GII-3 confers insect transmissility to the non-transmissible S. citri strain 44. Microbiology 152:2703-2716. (Pubitemid 44405095)
5. Berho, N., S. Duret, and J. Renaudin. 2006. Absence of plasmids encoding adhesion-related proteins in non-insect-transmissible strains of Spiroplasma citri. Microbiology 152:873-886.
6. Bertaccini, A. 2007. Phytoplasmas: diversity, taxonomy, and epidemiology. Front. Biosci. 12:673-689.
7. 7. Boutareaud, A., J. L. Danet, M. Garnier, and C. Saillard. 2004. Disruption of a gene predicted to encode a solute binding protein of an ABC transporter reduces transmission of Spiroplasma citri by the leafhopper Circulifer haematoceps. Appl. Environ. Microbiol. 70:3960-3967. (Pubitemid 38969735)
8. Breton, M., S. Duret, N. Arricau-Bouvery, L. Béven, and J. Renaudin. 2008. Characterizing the replication and stability regions of Spiroplasma citri plasmids identifies a novel replication protein and expands the genetic toolbox for plant pathogenic spiroplasmas. Microbiology 154:3232-3244.
9. Carle, P., F. Laigret, J. G. Tully, and J. M. Bové. 1995. Heterogeneity of genome sizes within the genus Spiroplasma. Int. J. Syst. Bacteriol. 45:178-181.
10. Christensen, N. M., K. B. Axelsen, M. Nicolaisen, and A. Schulz. 2005. Phytoplasmas and their interactions with hosts. Trends Plant Sci. 10:526-535.
11. Duret, S., B. Batailler, J.-L. Danet, L. Béven, J. Renaudin, and N. Arricau-Bouvery. 2010. Infection of the Circulifer haematoceps cell line Ciha-1 by Spiroplasma citri: the non-insect-transmissible strain 44 is impaired in invasion. Microbiology 156:1097-1107.
12. 12. Duret, S., N. Berho, J. L. Danet, M. Garnier, and J. Renaudin. 2003. Spiralin is not essential for helicity, motility, or pathogenicity but is required for efficient transmission of Spiroplasma citri by its leafhopper vector Circulifer haematoceps. Appl. Environ. Microbiol. 69:6225-6234. (Pubitemid 37280348)
13. Fletcher, J., A. Wayadande, U. Melcher, and F. C. Ye. 1998. The phytopathogenic mollicute-insect vector interface: a closer look. Phytopathology 88: 1351-1358.
14. 14. Foissac, X., J. L. Danet, C. Saillard, P. Gaurivaud, F. Laigret, C. Pare, and J. M. Bové. 1997. Mutagenesis by insertion of Tn4001 into the genome of Spiroplasma citri: characterization of mutants affected in plant pathogenicity and transmission to the plant by the leafhopper vector Circulifer haematoceps. Mol. Plant Microbe Interact. 10:454-461. (Pubitemid 27204368)
15. Foissac, X., J. L. Danet, C. Saillard, R. F. Whitcomb, and J. M. Bové. 1996. Experimental infections of plant by spiroplasmas, p. 385-389. In S. Razin and J. G. Tully (ed.), Molecular and diagnostic procedures in mycoplasmology, vol.2. Academic Press, New York, NY.
16. Fos, A., J. M. Bové, J. Lallemand, C. Saillard, J. C. Vignault, Y. Ali, P. Brun, and R. Vogel. 1986. The leafhopper Neoaliturus haematoceps is a vector of Spiroplasma citri in the mediterranean area. Ann. Inst. Pasteur Microbiol. 137A:97-107.
17. Ghosh, A. K., and M. Jacobs-Lorena. 2009. Plasmodium sporozoite invasion of the mosquito salivary gland. Curr. Opin. Microbiol. 12:394-400.
18. Gibbon, M. J., A. Sesma, A. Canal, J. R. Wood, E. Hidalgo, J. Brown, A. Vivian, and J. Murillo. 1999. Replication regions from plant-pathogenic Pseudomonas syringae plasmids are similar to colE2-related replicons. Microbiology 145:325-334.
19. Hosseini Pour, A. 2000. Determination of some molecular and cellular characteristics of Spiroplasma citri, the causal agent of citrus stubborn disease in Kerman, Fars and Mazadaran provinces. Tarbiat Modares University, Tehran, Iran.
20. Jewett, M. W., K. A. Lawrence, A. Bestor, R. Byram, F. Gherardini, and P. A. Rosa. 2009. GuaA and GuaB are essential for Borrelia burgdorferi survival in the tick-mouse infection cycle. J. Bacteriol. 191:6231-6241.
21. Joshi, B. D., M. Berg, J. Rogers, J. Fletcher, and U. Melcher. 2005. Sequence comparisons of plasmids pBJS-O of Spiroplasma citri and pSKU146 of S. kunkelii: implications for plasmid evolution. BMC Genomics 6:175-185.
22. Killiny, N., B. Batailler, X. Foissac, and C. Saillard. 2006. Identification of a Spiroplasma citri hydrophilic protein associated with insect transmissibility. Microbiology 152:1221-1230.
23. 23. Killiny, N., M. Castroviejo, and C. Saillard. 2005. Spiroplasma citri spiralin acts in vitro as a lectin binding to glycoproteins from its insect vector Circulifer haematoceps. Phytopathology 95:541-548. (Pubitemid 40589236)
24. Kwon, M. O., A. C. Wayadande, and J. Fletcher. 1999. Spiroplasma citri movement into the intestines and salivary glands of its leafhopper vector, Circulifer tenellus. Phytopathology 89:1144-1151.
25. Labroussaa, F., N. Arricau-Bouvery, M.-P. Dubrana, and C. Saillard. 2010. Entry of Spiroplasma citri into Circulifer haematoceps cells involves interaction between spiroplasma phosphoglycerate kinase and leafhopper actin. Appl. Environ. Microbiol. 76:1879-1886.
26. Lee, I. M., R. E. Davis, and D. E. Gundersen-Rindal. 2000. Phytoplasma: phytopathogenic mollicutes. Annu. Rev. Microbiol. 54:221-255.
27. Liu, H. Y., D. J. Gumpf, G. N. Oldfield, and E. C. Calavan. 1983. The relationship of Spiroplasma citri and Circulifer tenellus. Phytopathology 73: 585-590.
28. Liu, H. Y., D. J. Gumpf, G. N. Oldfield, and E. C. Calavan. 1983. Transmission of Spiroplasma citri by Circulifer tenellus. Phytopathology 73:582-585.
29. Neelakanta, G., X. Li, U. Pal, X. Liu, D. S. Beck, K. DePonte, D. Fish, F. S. Kantor, and E. Fikrig. 2007. Outer surface protein B is critical for Borrelia burgdorferi adherence and survival within Ixodes ticks. PLoS Pathog. 3:e33.
30. Novick, R. P. 1987. Plasmid incompatibility. Microbiol. Rev. 51:381-395.
31. Purcell, A. H. 1983. Insect vector relationships with procaryotic plant pathogens. Annu. Rev. Phytopathol. 20:397-417.
32. Rogowsky, P. M., B. S. Powell, K. Shirasu, T. S. Lin, P. Morel, E. M. Zyprian, T. R. Steck, and C. I. Kado. 1990. Molecular characterization of the vir regulon of Agrobacterium tumefaciens: complete nucleotide sequence and gene organization of the 28.63-kbp regulon cloned as a single unit. Plasmid 23:85-106.
33. Saglio, P., M. Lhospital, D. Laflèche, G. Dupont, J. M. Bové, J. G. Tully, and E. A. Freundt. 1973. Spiroplasma citri gen. and sp. nov.: a mycoplasma-like organism associated with stubborn disease of citrus. Int. J. Syst. Bacteriol. 23:191-204.
34. Saillard, C., P. Carle, S. Duret-Nurbel, R. Henri, N. Killiny, S. Carrère, J. Gouzy, J. M. Bové, J. Renaudin, and X. Foissac. 2008. The abundant extra-chromosomal content of Spiroplasma citri strain GII3-3X. BMC Genomics 9:195-207.
35. Schröder, G., S. Krause, E. L. Zechner, B. Traxler, H. J. Yeo, R. Lurz, G. Waksman, and E. Lanka. 2002. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J. Bacteriol. 184:2767-2779.
36. Seemüller, E., M. Garnier, and B. Schneider. 2002. Mycoplasmas of plants and insects, p. 91-116. In S. Razin and R. Herrmann (ed.), Molecular biology and pathogenicity of mycoplasmas. Kluwer Academic/ Plenum, New York, NY.
37. Stamburski, C., J. Renaudin, and J. M. Bové. 1991. First step toward a virus-derived vector for gene cloning and expression in spiroplasmas, organisms which read UGA as a tryptophan codon: synthesis of chloramphenicol acetyltransferase in Spiroplasma citri. J. Bacteriol. 173:2225-2230.
38. Sundin, G. W. 2007. Genomic insights into the contribution of phytopathogenic bacterial plasmids to the evolutionary history of their hosts. Annu. Rev. Phytopathol. 45:129-151.
39. Suzuki, S., K. Oshima, S. Kakizawa, R. Arashida, H. Jung, Y. Yamaji, H. Nishigawa, M. Ugaki, and S. Namba. 2006. Interaction between the membrane protein of a pathogen and insect microfilament complex determines insect-vector specificity. Proc. Natl. Acad. Sci. U. S. A. 103:4252-4257.
40. Vignault, J. C., J. M. Bové, C. Saillard, R. Vogel, A. Farro, L. Venegas, W. Stemmer, S. Aoki, R. E. McCoy, A. S. Al-beldawi, M. Larue, O. Tuzco, M. Ozan, A. Nhami, M. Abassi, J. Bonfils, G. Moutous, A. Fos, F. Poutiers, and G. Viennot-Bourgin. 1980. Mise en culture de spiroplasmes à partir de matériel végétal et d'insectes provenant de pays circum méditerranéens et du Proche Orient. C. R. Acad. Sci. Ser. III 290:775-780.
41. Vivian, A., J. Murillo, and R. W. Jackson. 2001. The roles of plasmids in phytopathogenic bacteria: mobile arsenals? Microbiology 147:763-780.
42. Weintraub, P. G., and L. Beanland. 2006. Insect vectors of phytoplasmas. Annu. Rev. Entomol. 51:91-111.
43. Whitcomb, R. F. 1983. Culture media for spiroplasma, p. 147-158. In S. Razin and J. G. Tully (ed.), Methods in mycoplasmology, vol.I. Academic Press, New York, NY.
44. 44. Yu, J., A. C. Wayadande, and J. Fletcher. 2000. Spiroplasma citri surface protein P89 implicated in adhesion to cells of the vector Circulifer tenellus. Phytopathology 90:716-722. (Pubitemid 30400332)