Molecular and histological characterization of primary (betaproteobacteria) and secondary (gammaproteobacteria) endosymbionts of three mealybug species

Applied and Environmental Microbiology

Volumn 78, Issue 4, 2012, Pages 1187-1197

  Gatehouse, Laurence N ^a   Sutherland, Paul ^a   Forgie, Shaun A ^a,b   Kaji, Ryohei ^a   Christeller, John T ^a  

^a THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^b LANDCARE RESEARCH   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; 16S RRNA SEQUENCES; AMINO ACID SEQUENCE; BETAPROTEOBACTERIA; COAT PROTEINS; ENDOSYMBIONT; ENDOSYMBIOTIC BACTERIUM; GAMMAPROTEOBACTERIA; PLANT PATHOGEN; SEQUENCE DATA; VIRUS TRANSMISSION;

AMINO ACIDS; FRUITS; GENES; PROTEINS; RNA; VIRUSES;

BACTERIA;

BACTERIAL DNA; RIBOSOME DNA; RNA 16S;

BACTERIUM; DISEASE TRANSMISSION; DIVERGENCE; ENDOSYMBIONT; EVOLUTIONARY BIOLOGY; HISTOLOGY; HOMOLOGY; HOST-PATHOGEN INTERACTION; INSECT; MOLECULAR ANALYSIS; PROTEIN;

ANIMAL; ARTICLE; BETAPROTEOBACTERIA; CHEMISTRY; CLASSIFICATION; CLOSTEROVIRIDAE; CLUSTER ANALYSIS; CYTOCHEMISTRY; DNA SEQUENCE; GAMMAPROTEOBACTERIA; GENETICS; HEMIPTERA; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; SYMBIOSIS; VIROLOGY;

ANIMALS; BETAPROTEOBACTERIA; CLOSTEROVIRIDAE; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; GAMMAPROTEOBACTERIA; HEMIPTERA; HISTOCYTOCHEMISTRY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; CANDIDATUS TREMBLAYA PRINCEPS; GAMMAPROTEOBACTERIA; GRAPEVINE LEAFROLL-ASSOCIATED VIRUS 3; PSEUDOCOCCIDAE; PSEUDOCOCCUS CALCEOLARIAE; PSEUDOCOCCUS LONGISPINUS; PSEUDOCOCCUS VIBURNI; SODALIS GLOSSINIDIUS;

EID: 84857067691     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06340-11     Document Type: Article

References (46)

1. Akad F, Dotan N, Czosnek H. 2004. Trapping of Tomato yellow leaf curl virus (TYLCV) and other plant viruses with a GroEL homologue from the whitefly Bemisia tabaci. Arch. Virol. 149:1481-1497.
2. Aksoy S, Pourhosseini AA, Chow A. 1995. Mycetome endosymbionts of tsetse flies constitute a distinct lineage related to Enterobacteriaceae. Insect Mol. Biol. 4:15-22.
3. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ. 2005. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71:7724-7736.
4. Axe DD, Foster NW, Fersht AR. 1996. Active barnase variants with completely random hydrophobic cores. Proc. Natl. Acad. Sci. U. S. A. 93:5590-5594.
5. Baumann L, Baumann P. 2005. Cospeciation between the primary endosymbionts of mealybugs and their hosts. Curr. Microbiol. 50:84-87.
6. Baumann L, Thao ML, Hess JM, Johnson MW, Baumann P. 2002. The genetic properties of the primary endosymbionts of mealybugs differ from those of other endosymbionts of plant sap-sucking insects. Appl. Environ. Microbiol. 68:3198-3205.
7. Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155-189.
8. Baumann P. 2006. Diversity of procaryote-insect associations with the Sternorrhycha (psyllids, whiteflires, aphids, mealybugs), vol 2. CRC Press, Boca Raton, FL.
9. Bovey R, Gartel W, Hewitt WB, Martelli GP, Vuittenez A. 1980. Virus and virus-like diseases of grapevine. Payot Publishing Co., Lausanne, France.
10. Cabaleiro C, Segura A. 1997. Field transmission of grapevine leafroll associated virus 3 (GLRaV-3) by the mealybug Planococcus citri. Plant Dis. 81:283-287.
11. Charles JG, et al. 2006. A review of grapevine leafroll associated virus type 3 (GLRaV-3) for the New Zealand wine industry. HortResearch client report no. 18447. HortResearch, Palmerston North, New Zealand.
12. Charles JG, Froud KJ, van den Brink R, Allan DJ. 2009. Mealybugs and the spread of grapevine leafroll-associated virus 3 (GLRaV-3) in a New Zealand vineyard. Australasian Plant Pathol. 38:576-583.
13. Cid M, Pereira S, Cabaleiro C, Faoro F, Segura A. 2007. Presence of Grapevine leafroll-associated virus 3 in primary salivary glands of the mealybug vector Planococcus citri suggests a circulative transmission mechanism. Eur. J. Plant Pathol. 118:23-30.
14. Dale C, Moran NA. 2006. Molecular interactions between bacterial symbionts and their hosts. Cell 126:453-465.
15. Douglas A. 2007. Interactions between insects and their symbiotic microorganisms. Comp. Biochem. Physiol. A 146:S217. doi:10.1016/j.cbpa.2007.01.473 9.
16. Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43:17-37.
17. Duron O, et al. 2008. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 6:27.
18. Edelbaum D, Gorovits R, Sasaki S, Ikegami M, Czosnek H. 2009. Expressing a whitefly GroEL protein in Nicotiana benthamiana plants confers tolerance to tomato yellow leaf curl virus and cucumber mosaic virus, but not to grapevine virus A or tobacco mosaic virus. Arch. Virol. 154:399-407.
19. Felsenstein J. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. University of Washington, Seattle, WA.
20. Golino DA, Sim ST, Gill R, Rowhani A. 2002. California mealybugs can spread grapevine leafroll disease. California Agric. 56:196-201.
21. Hardy NB, Gullan PJ, Hodgson CJ. 2008. A subfamily-level classification of mealybugs (Hemiptera: Pseudococcidae) based on integrated molecular and morphological data. Syst. Entomol. 33:51-71.
22. Jaenike J. 2009. Coupled population dynamics of endosymbionts within and between hosts. Oikos 118:353-362.
23. Kantheti P, Jayarama KS, Chandra HS. 1996. Developmental analysis of a female-specific 16S rRNA gene from mycetome-associated endosymbionts of a mealybug, Planococcus lilacinus. Insect Biochem. Mol. Biol. 26:997-1009.
24. Kono M, Koga R, Shimada M, Fukatsu T. 2008. Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs. Appl. Environ. Microbiol. 74:4175-4184.
25. Lin Z, Rye HS. 2006. GroEL-mediated protein folding: making the impossible, possible. Crit. Rev. Biochem. Mol. Biol. 41:211-239.
26. Ling K-S, Zhu H-Y, Gonsalves D. 2004. Complete nucleotide sequence and genome organization of Grapevine leafroll-associated virus 3, type member of the genus Ampelovirus. J. Gen. Virol. 85:2099-2102.
27. Lund PA. 1995. The roles of molecular chaperones in vivo. Essays Biochem. 29:113-123.
28. McCutcheon JP, von Dohlen CD. 2011. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21:1366-1372.
29. Moran NA, Plague GR, Sandstrom JP, Wilcox JL. 2003. A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc. Natl. Acad. Sci. U. S. A. 100:14543-14548.
30. Morin S, Ghanim M, Sobol I, Czosnek H. 2000. The GroEL protein of the whitefly Bemisia tabaci interacts with the coat protein of transmissible and nontransmissible begomoviruses in the yeast two-hybrid system. Virology 276:404-416.
31. Morin S, et al. 1999. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of tomato yellow leaf curl virus. Virology 256:75-84.
32. Muller LL, Jacks TJ. 1975. Rapid chemical dehydration of samples for electron microscopic examinations. J. Histochem. Cytochem. 23:107-110.
33. Munson MA, Baumann P, Moran NA. 1992. Phylogenetic relationships of the endosymbionts of mealybugs (Homoptera: Pseudococcidae) based on 16S rDNA sequences. Mol. Phylogenet. Evol. 1:26-30.
34. Nicholas KB, Nicholas HB, Jr, Deerfield DWI. 1997. GeneDoc: analysis and visualization of genetic variation. Embnew. News 4:14.
35. O'Fallon B. 2008. Population structure, levels of selection, and the evolution of intracellular symbionts. Evolution 62:361-373.
36. Page RDM. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
37. Petersen CL, Charles JG. 1997. Transmission of grapevine leafrollassociated closteroviruses by Pseudococcus longispinus and P. calceolariae. Plant Pathol. 46:509-515.
38. Roland JC, Vian B. 1991. General preparation and staining of thin sections, p 1-66. In Hall JL, Hawes C (ed), Electron microscopy of plant cells. Academic Press, New York, NY.
39. Sforza R, Boudon-Padieu E, Greif C. 2003. New mealybug species vectoring Grapevine leafroll-associated viruses-1 and -3 (GLRaV-1 and -3). Eur. J. Plant Pathol. 109:975-981.
40. Stan G, Brooks BR, Lorimer GH, Thirumalai D. 2005. Identifying natural substrates for chaperonins using a sequence-based approach. Protein Sci. 14:193-201.
41. Thao ML, Gullan PJ, Baumann P. 2002. Secondary (gamma-Proteobacteria) endosymbionts infect the primary (beta-Proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts. Appl. Environ. Microbiol. 68:3190-3197.
42. 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.
43. Toh H, et al. 2006. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 16:149-156.
44. van den Heuvel J, et al. 1997. The N-terminal region of the luteovirus readthrough domain determines virus binding to Buchnera GroEL and is essential for virus persistence in the aphid. J. Virol. 71:7258-7265.
45. von Dohlen CD, Kohler S, Alsop ST, McManus WR. 2001. Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412:433-436.
46. Welburn SC, Maudlin I, Ellis DS. 1987. In vitro cultivation of Rickettsialike-organisms from Glossina spp. Ann. Trop. Med. Parasitol. 81:331-335.