Skip to main content
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1996 Feb;62(2):332–339. doi: 10.1128/aem.62.2.332-339.1996

The endosymbiont (Buchnera sp.) of the aphid Diuraphis noxia contains plasmids consisting of trpEG and tandem repeats of trpEG pseudogenes.

C Y Lai 1, P Baumann 1, N Moran 1
PMCID: PMC167803  PMID: 8593038

Abstract

Most aphids are dependent for their survival on prokaryotic endosymbionts assigned to the genus Buchnera. Among the functions of Buchnera species is the synthesis of tryptophan, which is required by the aphid host. In Buchnera species from the aphid Diuraphis noxia, the genes for anthranilate synthase (trpEG) were found on a plasmid which consisted of seven tandem repeats of a 3.2-kb unit and one 2.6-kb unit which differed in containing a 0.6-kb deletion. One of the 3.2-kb units contained open reading frames corresponding to trpEG; the remaining units contained trpEG pseudogenes (psi). The nucleotide sequence upstream of trpE contained a region that has characteristics of an origin of replication (ori). Relative to trpB (a chromosomal gene), there were about two copies of the trpEG-containing plasmid. Comparisons of the nucleotide sequences of the 3.2-kb units containing trpEG and psi trpEG indicated that most changes occurred in a 700-nucleotide segment that included the region upstream of trpE and the portion of this gene coding for the N terminus. The consequence of these changes was the silencing of trpEG by inactivation of the putative promoter region and premature termination of the TrpE peptide. In contrast, the nucleotide sequence of the segment corresponding to ori was conserved in the units containing trpEG and psi trpEG. We offer a number of speculations on the evolutionary pressure in this lineage which resulted in the silencing of most of trpEG while still retaining the regions resembling ori.

Full Text

The Full Text of this article is available as a PDF (388.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson R. P., Roth J. R. Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol. 1977;31:473–505. doi: 10.1146/annurev.mi.31.100177.002353. [DOI] [PubMed] [Google Scholar]
  2. Baumann L., Baumann P. Growth Kinetics of the Endosymbiont Buchnera aphidicola in the Aphid Schizaphis graminum. Appl Environ Microbiol. 1994 Sep;60(9):3440–3443. doi: 10.1128/aem.60.9.3440-3443.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baumann P., Baumann L., Lai C. Y., Rouhbakhsh D., Moran N. A., Clark M. A. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu Rev Microbiol. 1995;49:55–94. doi: 10.1146/annurev.mi.49.100195.000415. [DOI] [PubMed] [Google Scholar]
  4. Baumann P., Lai C., Baumann L., Rouhbakhsh D., Moran N. A., Clark M. A. Mutualistic associations of aphids and prokaryotes: biology of the genus buchnera. Appl Environ Microbiol. 1995 Jan;61(1):1–7. doi: 10.1128/aem.61.1.1-7.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beverley S. M. Gene amplification in Leishmania. Annu Rev Microbiol. 1991;45:417–444. doi: 10.1146/annurev.mi.45.100191.002221. [DOI] [PubMed] [Google Scholar]
  6. Bracho A. M., Martínez-Torres D., Moya A., Latorre A. Discovery and molecular characterization of a plasmid localized in Buchnera sp. bacterial endosymbiont of the aphid Rhopalosiphum padi. J Mol Evol. 1995 Jul;41(1):67–73. doi: 10.1007/BF00174042. [DOI] [PubMed] [Google Scholar]
  7. Crawford I. P. Evolution of a biosynthetic pathway: the tryptophan paradigm. Annu Rev Microbiol. 1989;43:567–600. doi: 10.1146/annurev.mi.43.100189.003031. [DOI] [PubMed] [Google Scholar]
  8. Douglas A. E. Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc. 1989 Nov;64(4):409–434. doi: 10.1111/j.1469-185x.1989.tb00682.x. [DOI] [PubMed] [Google Scholar]
  9. Fisher D. B., Macnicol P. K. Amino Acid Composition Along the Transport Pathway during Grain Filling in Wheat. Plant Physiol. 1986 Dec;82(4):1019–1023. doi: 10.1104/pp.82.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harding N. E., Cleary J. M., Smith D. W., Michon J. J., Brusilow W. S., Zyskind J. W. Chromosomal replication origins (oriC) of Enterobacter aerogenes and Klebsiella pneumoniae are functional in Escherichia coli. J Bacteriol. 1982 Dec;152(3):983–993. doi: 10.1128/jb.152.3.983-993.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ishikawa H. Biochemical and molecular aspects of endosymbiosis in insects. Int Rev Cytol. 1989;116:1–45. doi: 10.1016/s0074-7696(08)60637-3. [DOI] [PubMed] [Google Scholar]
  12. Lai C. Y., Baumann L., Baumann P. Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3819–3823. doi: 10.1073/pnas.91.9.3819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lai C. Y., Baumann P. Genetic analysis of an aphid endosymbiont DNA fragment homologous to the rnpA-rpmH-dnaA-dnaN-gyrB region of eubacteria. Gene. 1992 Apr 15;113(2):175–181. doi: 10.1016/0378-1119(92)90393-4. [DOI] [PubMed] [Google Scholar]
  14. Lai C. Y., Baumann P., Moran N. A. Genetics of the tryptophan biosynthetic pathway of the prokaryotic endosymbiont (Buchnera) of the aphid Schlechtendalia chinensis. Insect Mol Biol. 1995 Feb;4(1):47–59. doi: 10.1111/j.1365-2583.1995.tb00007.x. [DOI] [PubMed] [Google Scholar]
  15. Løbner-Olesen A., Skarstad K., Hansen F. G., von Meyenburg K., Boye E. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell. 1989 Jun 2;57(5):881–889. doi: 10.1016/0092-8674(89)90802-7. [DOI] [PubMed] [Google Scholar]
  16. Manson M. D., Yanofsky C. Naturally occurring sites within the Shigella dysenteriae tryptophan operon severely limit tryptophan biosynthesis. J Bacteriol. 1976 May;126(2):668–678. doi: 10.1128/jb.126.2.668-678.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Miozzari G., Yanofsky C. Naturally occurring promoter down mutation: nucleotide sequence of the trp promoter/operator/leader region of Shigella dysenteriae 16. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5580–5584. doi: 10.1073/pnas.75.11.5580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moriya S., Fukuoka T., Ogasawara N., Yoshikawa H. Regulation of initiation of the chromosomal replication by DnaA-boxes in the origin region of the Bacillus subtilis chromosome. EMBO J. 1988 Sep;7(9):2911–2917. doi: 10.1002/j.1460-2075.1988.tb03149.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Munson M. A., Baumann P. Molecular cloning and nucleotide sequence of a putative trpDC(F)BA operon in Buchnera aphidicola (endosymbiont of the aphid Schizaphis graminum). J Bacteriol. 1993 Oct;175(20):6426–6432. doi: 10.1128/jb.175.20.6426-6432.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Puterka G. J., Black W. C., 4th, Steiner W. M., Burton R. L. Genetic variation and phylogenetic relationships among worldwide collections of the Russian wheat aphid, Diuraphis noxia (Mordvilko), inferred from allozyme and RAPD-PCR markers. Heredity (Edinb) 1993 Jun;70(Pt 6):604–618. doi: 10.1038/hdy.1993.87. [DOI] [PubMed] [Google Scholar]
  21. Skarstad K., Løbner-Olesen A., Atlung T., von Meyenburg K., Boye E. Initiation of DNA replication in Escherichia coli after overproduction of the DnaA protein. Mol Gen Genet. 1989 Jul;218(1):50–56. doi: 10.1007/BF00330564. [DOI] [PubMed] [Google Scholar]
  22. Wang R. F., Kushner S. R. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene. 1991 Apr;100:195–199. [PubMed] [Google Scholar]
  23. Yoshikawa H., Ogasawara N. Structure and function of DnaA and the DnaA-box in eubacteria: evolutionary relationships of bacterial replication origins. Mol Microbiol. 1991 Nov;5(11):2589–2597. doi: 10.1111/j.1365-2958.1991.tb01967.x. [DOI] [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES