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. 2001 Dec 22;268(1485):2565–2570. doi: 10.1098/rspb.2001.1839

Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila.

E A McGraw 1, D J Merritt 1, J N Droller 1, S L O'Neill 1
PMCID: PMC1088916  PMID: 11749711

Abstract

Estimates of Wolbachia density in the eggs, testes and whole flies of drosophilid hosts have been unable to predict the lack of cytoplasmic incompatibility (CI) expression in so-called mod(-) variants. Consequently, the working hypothesis has been that CI expression, although related to Wolbachia density, is also governed by unknown factors that are influenced by both host and bacterial genomes. Here, we compare the behaviour of the mod(-) over-replicating Wolbachia popcorn strain in its native Drosophila melanogaster host to the same strain transinfected into a novel host, namely Drosophila simulans. We report that (i) the popcorn strain is a close relative of other D. melanogaster infections, (ii) the mod(-) status of popcorn in D. melanogaster appears to result from its inability to colonize sperm bundles, (iii) popcorn is present in the bundles in D. simulans and induces strong CI expression, which demonstrates that the bacterial strain does not lack the genetic machinery for inducing CI and that there is host-species-specific control over Wolbachia tissue tropism, and (iv) infection of sperm bundles by the mod(-) D. simulans wCof strain indicates that there are several independent routes by which a strain can be a CI non-expressor.

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Selected References

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  1. Bourtzis K., Dobson S. L., Braig H. R., O'Neill S. L. Rescuing Wolbachia have been overlooked. Nature. 1998 Feb 26;391(6670):852–853. doi: 10.1038/36017. [DOI] [PubMed] [Google Scholar]
  2. Bourtzis K., Nirgianaki A., Markakis G., Savakis C. Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics. 1996 Nov;144(3):1063–1073. doi: 10.1093/genetics/144.3.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boyle L., O'Neill S. L., Robertson H. M., Karr T. L. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science. 1993 Jun 18;260(5115):1796–1799. doi: 10.1126/science.8511587. [DOI] [PubMed] [Google Scholar]
  4. Braig H. R., Zhou W., Dobson S. L., O'Neill S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 1998 May;180(9):2373–2378. doi: 10.1128/jb.180.9.2373-2378.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bressac C., Rousset F. The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol. 1993 May;61(3):226–230. doi: 10.1006/jipa.1993.1044. [DOI] [PubMed] [Google Scholar]
  6. Callaini G., Dallai R., Riparbelli M. G. Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J Cell Sci. 1997 Jan;110(Pt 2):271–280. doi: 10.1242/jcs.110.2.271. [DOI] [PubMed] [Google Scholar]
  7. Giordano R., O'Neill S. L., Robertson H. M. Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics. 1995 Aug;140(4):1307–1317. doi: 10.1093/genetics/140.4.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hoffmann A. A., Clancy D. J., Merton E. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics. 1994 Mar;136(3):993–999. doi: 10.1093/genetics/136.3.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hoffmann A. A., Clancy D., Duncan J. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity (Edinb) 1996 Jan;76(Pt 1):1–8. doi: 10.1038/hdy.1996.1. [DOI] [PubMed] [Google Scholar]
  10. Holden P. R., Jones P., Brookfield J. F. Evidence for a Wolbachia symbiont in Drosophila melanogaster. Genet Res. 1993 Aug;62(1):23–29. doi: 10.1017/s0016672300031529. [DOI] [PubMed] [Google Scholar]
  11. Jeyaprakash A., Hoy M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol. 2000 Aug;9(4):393–405. doi: 10.1046/j.1365-2583.2000.00203.x. [DOI] [PubMed] [Google Scholar]
  12. Min K. T., Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10792–10796. doi: 10.1073/pnas.94.20.10792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. O'Neill S. L., Giordano R., Colbert A. M., Karr T. L., Robertson H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2699–2702. doi: 10.1073/pnas.89.7.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Poinsot D., Bourtzis K., Markakis G., Savakis C., Merçot H. Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. Genetics. 1998 Sep;150(1):227–237. doi: 10.1093/genetics/150.1.227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sinkins S. P., Braig H. R., O'Neill S. L. Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc Biol Sci. 1995 Sep 22;261(1362):325–330. doi: 10.1098/rspb.1995.0154. [DOI] [PubMed] [Google Scholar]
  16. Turelli M., Hoffmann A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature. 1991 Oct 3;353(6343):440–442. doi: 10.1038/353440a0. [DOI] [PubMed] [Google Scholar]
  17. Tyagi S., Kramer F. R. Molecular beacons: probes that fluoresce upon hybridization. Nat Biotechnol. 1996 Mar;14(3):303–308. doi: 10.1038/nbt0396-303. [DOI] [PubMed] [Google Scholar]
  18. Zhou W., Rousset F., O'Neil S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci. 1998 Mar 22;265(1395):509–515. doi: 10.1098/rspb.1998.0324. [DOI] [PMC free article] [PubMed] [Google Scholar]

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