Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Jan 3;92(1):305–309. doi: 10.1073/pnas.92.1.305

Virus-mediated or transgenic suppression of a G-protein alpha subunit and attenuation of fungal virulence.

G H Choi 1, B Chen 1, D L Nuss 1
PMCID: PMC42867  PMID: 7816838

Abstract

Strains of the chestnut blight fungus Cryphonectria parasitica harboring RNA viruses of the genus Hypovirus exhibit significantly reduced levels of virulence (called hypovirulence). The accumulation of a heterotrimeric GTP-binding protein (G protein) alpha subunit of the Gi class was found to be reduced in hypovirus-containing C. parasitica strains. Transgenic cosuppression, a phenomenon frequently observed in transgenic plants, reduced the accumulation of this alpha subunit in virus-free fungal strains. Significantly, the resulting transgenic fungal strains were also hypovirulent. These results indicate a crucial role for G-protein-linked signal transduction in fungal pathogenesis and suggest a molecular basis for virus-mediated attenuation of fungal virulence.

Full text

PDF
305

Images in this article

307Fig. 2
on p.307
307Fig. 3
on p.307
308Fig. 4
on p.308

Selected References

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

  1. Buss J. E., Mumby S. M., Casey P. J., Gilman A. G., Sefton B. M. Myristoylated alpha subunits of guanine nucleotide-binding regulatory proteins. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7493–7497. doi: 10.1073/pnas.84.21.7493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cameron F. H., Jennings P. A. Inhibition of gene expression by a short sense fragment. Nucleic Acids Res. 1991 Feb 11;19(3):469–475. doi: 10.1093/nar/19.3.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chen B., Choi G. H., Nuss D. L. Attenuation of fungal virulence by synthetic infectious hypovirus transcripts. Science. 1994 Jun 17;264(5166):1762–1764. doi: 10.1126/science.8209256. [DOI] [PubMed] [Google Scholar]
  4. Chen B., Choi G. H., Nuss D. L. Mitotic stability and nuclear inheritance of integrated viral cDNA in engineered hypovirulent strains of the chestnut blight fungus. EMBO J. 1993 Aug;12(8):2991–2998. doi: 10.1002/j.1460-2075.1993.tb05967.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Choi G. H., Larson T. G., Nuss D. L. Molecular analysis of the laccase gene from the chestnut blight fungus and selective suppression of its expression in an isogenic hypovirulent strain. Mol Plant Microbe Interact. 1992 Mar-Apr;5(2):119–128. doi: 10.1094/mpmi-5-119. [DOI] [PubMed] [Google Scholar]
  6. Choi G. H., Nuss D. L. A viral gene confers hypovirulence-associated traits to the chestnut blight fungus. EMBO J. 1992 Feb;11(2):473–477. doi: 10.1002/j.1460-2075.1992.tb05077.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Choi G. H., Nuss D. L. Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science. 1992 Aug 7;257(5071):800–803. doi: 10.1126/science.1496400. [DOI] [PubMed] [Google Scholar]
  8. Craven M. G., Pawlyk D. M., Choi G. H., Nuss D. L. Papain-like protease p29 as a symptom determinant encoded by a hypovirulence-associated virus of the chestnut blight fungus. J Virol. 1993 Nov;67(11):6513–6521. doi: 10.1128/jvi.67.11.6513-6521.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
  10. Hart C. M., Fischer B., Neuhaus J. M., Meins F., Jr Regulated inactivation of homologous gene expression in transgenic Nicotiana sylvestris plants containing a defense-related tobacco chitinase gene. Mol Gen Genet. 1992 Nov;235(2-3):179–188. doi: 10.1007/BF00279359. [DOI] [PubMed] [Google Scholar]
  11. Kaziro Y., Itoh H., Kozasa T., Nakafuku M., Satoh T. Structure and function of signal-transducing GTP-binding proteins. Annu Rev Biochem. 1991;60:349–400. doi: 10.1146/annurev.bi.60.070191.002025. [DOI] [PubMed] [Google Scholar]
  12. Larson T. G., Choi G. H., Nuss D. L. Regulatory pathways governing modulation of fungal gene expression by a virulence-attenuating mycovirus. EMBO J. 1992 Dec;11(12):4539–4548. doi: 10.1002/j.1460-2075.1992.tb05555.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Napoli C., Lemieux C., Jorgensen R. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. Plant Cell. 1990 Apr;2(4):279–289. doi: 10.1105/tpc.2.4.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Powell W. A., Jr, Van Alfen N. K. Two nonhomologus viruses of Cryphonectria (Endothia) parasitica reduce accumulation of specific virulence-associated polypeptides. J Bacteriol. 1987 Nov;169(11):5324–5326. doi: 10.1128/jb.169.11.5324-5326.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Powell W. A., Van Alfen N. K. Differential accumulation of poly(A)+ RNA between virulent and double-stranded RNA-induced hypovirulent strains of Cryphonectria (Endothia) parasitica. Mol Cell Biol. 1987 Oct;7(10):3688–3693. doi: 10.1128/mcb.7.10.3688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rigling D., Van Alfen N. K. Regulation of laccase biosynthesis in the plant-pathogenic fungus Cryphonectria parasitica by double-stranded RNA. J Bacteriol. 1991 Dec;173(24):8000–8003. doi: 10.1128/jb.173.24.8000-8003.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Romano N., Macino G. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol. 1992 Nov;6(22):3343–3353. doi: 10.1111/j.1365-2958.1992.tb02202.x. [DOI] [PubMed] [Google Scholar]
  18. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  19. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Simon M. I., Strathmann M. P., Gautam N. Diversity of G proteins in signal transduction. Science. 1991 May 10;252(5007):802–808. doi: 10.1126/science.1902986. [DOI] [PubMed] [Google Scholar]
  21. Smith C. J., Watson C. F., Bird C. R., Ray J., Schuch W., Grierson D. Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Mol Gen Genet. 1990 Dec;224(3):477–481. doi: 10.1007/BF00262443. [DOI] [PubMed] [Google Scholar]
  22. Strathmann M., Wilkie T. M., Simon M. I. Diversity of the G-protein family: sequences from five additional alpha subunits in the mouse. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7407–7409. doi: 10.1073/pnas.86.19.7407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Turner G. E., Borkovich K. A. Identification of a G protein alpha subunit from Neurospora crassa that is a member of the Gi family. J Biol Chem. 1993 Jul 15;268(20):14805–14811. [PubMed] [Google Scholar]
  24. Van Alfen N. K., Jaynes R. A., Anagnostakis S. L., Day P. R. Chestnut Blight: Biological Control by Transmissible Hypovirulence in Endothia parasitica. Science. 1975 Sep 12;189(4206):890–891. doi: 10.1126/science.189.4206.890. [DOI] [PubMed] [Google Scholar]
  25. Varley D. A., Podila G. K., Hiremath S. T. Cutinase in Cryphonectria parasitica, the chestnut blight fungus: suppression of cutinase gene expression in isogenic hypovirulent strains containing double-stranded RNAs. Mol Cell Biol. 1992 Oct;12(10):4539–4544. doi: 10.1128/mcb.12.10.4539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. West R. E., Jr, Moss J., Vaughan M., Liu T., Liu T. Y. Pertussis toxin-catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADP-ribose acceptor site. J Biol Chem. 1985 Nov 25;260(27):14428–14430. [PubMed] [Google Scholar]
  27. Zhang L., Villalon D., Sun Y., Kazmierczak P., van Alfen N. K. Virus-associated down-regulation of the gene encoding cryparin, an abundant cell-surface protein from the chestnut blight fungus, Cryphonectria parasitica. Gene. 1994 Feb 11;139(1):59–64. doi: 10.1016/0378-1119(94)90523-1. [DOI] [PubMed] [Google Scholar]
  28. de Carvalho F., Gheysen G., Kushnir S., Van Montagu M., Inzé D., Castresana C. Suppression of beta-1,3-glucanase transgene expression in homozygous plants. EMBO J. 1992 Jul;11(7):2595–2602. doi: 10.1002/j.1460-2075.1992.tb05324.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. van der Krol A. R., Mur L. A., Beld M., Mol J. N., Stuitje A. R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell. 1990 Apr;2(4):291–299. doi: 10.1105/tpc.2.4.291. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES