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. 1997 Nov;9(11):1973–1983. doi: 10.1105/tpc.9.11.1973

The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development.

W Choi 1, R A Dean 1
PMCID: PMC157051  PMID: 9401122

Abstract

Magnaporthe grisea, the causal agent of rice blast disease, differentiates a specialized infection structure called an appressorium that is crucial for host plant penetration. Previously, it was found that cAMP regulates appressorium formation. To further understand the cellular mechanisms involved in appressorium formation, we have cloned a gene (MAC1) encoding adenylate cyclase, a membrane-bound enzyme that catalyzes the production of cAMP from ATP, by using a polymerase chain reaction-based strategy. The entire gene was isolated and subcloned from a large insert bacterial artificial chromosome library. Sequence characterization showed that MAC1 has a high degree of identity with other adenylate cyclase genes from several filamentous fungi as well as yeasts. Gene deletion resulted in reduced vegetative growth, conidiation, and conidial germination. Transformants lacking MAC1 were unable to form appressoria on an inductive surface and were unable to penetrate susceptible rice leaves. mac1- transformants were also sterile and produced no perithecia. Appressorium formation was restored in the presence of exogenous cAMP derivatives. These results confirm that cell signaling involving cAMP plays a central role in the development and pathogenicity of M. grisea.

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Selected References

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  1. Beckerman J. L., Ebbole D. J. MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Mol Plant Microbe Interact. 1996 Aug;9(6):450–456. doi: 10.1094/mpmi-9-0450. [DOI] [PubMed] [Google Scholar]
  2. Colicelli J., Field J., Ballester R., Chester N., Young D., Wigler M. Mutational mapping of RAS-responsive domains of the Saccharomyces cerevisiae adenylyl cyclase. Mol Cell Biol. 1990 Jun;10(6):2539–2543. doi: 10.1128/mcb.10.6.2539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dean R. A. Signal pathways and appressorium morphogenesis. Annu Rev Phytopathol. 1997;35:211–234. doi: 10.1146/annurev.phyto.35.1.211. [DOI] [PubMed] [Google Scholar]
  4. Fedor-Chaiken M., Deschenes R. J., Broach J. R. SRV2, a gene required for RAS activation of adenylate cyclase in yeast. Cell. 1990 Apr 20;61(2):329–340. doi: 10.1016/0092-8674(90)90813-t. [DOI] [PubMed] [Google Scholar]
  5. Firtel R. A. Signal transduction pathways controlling multicellular development in Dictyostelium. Trends Genet. 1991 Nov-Dec;7(11-12):381–388. doi: 10.1016/0168-9525(91)90260-w. [DOI] [PubMed] [Google Scholar]
  6. Garnjobst L., Tatum E. L. New crisp genes and crisp-modifiers in neurospora crassa. Genetics. 1970 Oct;66(2):281–290. doi: 10.1093/genetics/66.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gold S., Duncan G., Barrett K., Kronstad J. cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev. 1994 Dec 1;8(23):2805–2816. doi: 10.1101/gad.8.23.2805. [DOI] [PubMed] [Google Scholar]
  8. Hamer J. E., Howard R. J., Chumley F. G., Valent B. A mechanism for surface attachment in spores of a plant pathogenic fungus. Science. 1988 Jan 15;239(4837):288–290. doi: 10.1126/science.239.4837.288. [DOI] [PubMed] [Google Scholar]
  9. Howard R. J., Ferrari M. A., Roach D. H., Money N. P. Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11281–11284. doi: 10.1073/pnas.88.24.11281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kataoka T., Broek D., Wigler M. DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase. Cell. 1985 Dec;43(2 Pt 1):493–505. doi: 10.1016/0092-8674(85)90179-5. [DOI] [PubMed] [Google Scholar]
  11. Kore-eda S., Murayama T., Uno I. Isolation and characterization of the adenylate cyclase structural gene of Neurospora crassa. Jpn J Genet. 1991 Jun;66(3):317–334. doi: 10.1266/jjg.66.317. [DOI] [PubMed] [Google Scholar]
  12. Kore-eda S., Murayama T., Uno I. Suppression of the cr-1 mutation in Neurospora crassa. Jpn J Genet. 1991 Feb;66(1):77–83. doi: 10.1266/jjg.66.77. [DOI] [PubMed] [Google Scholar]
  13. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. doi: 10.1126/science.3289117. [DOI] [PubMed] [Google Scholar]
  14. Lee Y. H., Dean R. A. cAMP Regulates Infection Structure Formation in the Plant Pathogenic Fungus Magnaporthe grisea. Plant Cell. 1993 Jun;5(6):693–700. doi: 10.1105/tpc.5.6.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Loubradou G., Bégueret J., Turcq B. An additional copy of the adenylate cyclase-encoding gene relieves developmental defects produced by a mutation in a vegetative incompatibility-controlling gene in Podospora anserina. Gene. 1996 Apr 17;170(1):119–123. doi: 10.1016/0378-1119(95)00847-0. [DOI] [PubMed] [Google Scholar]
  16. Matsumoto K., Uno I., Ishikawa T. Initiation of meiosis in yeast mutants defective in adenylate cyclase and cyclic AMP-dependent protein kinase. Cell. 1983 Feb;32(2):417–423. doi: 10.1016/0092-8674(83)90461-0. [DOI] [PubMed] [Google Scholar]
  17. Matsumoto K., Uno I., Oshima Y., Ishikawa T. Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2355–2359. doi: 10.1073/pnas.79.7.2355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mitchell T. K., Dean R. A. The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell. 1995 Nov;7(11):1869–1878. doi: 10.1105/tpc.7.11.1869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pastan I., Perlman R. Cyclic adenosine monophosphate in bacteria. Science. 1970 Jul 24;169(3943):339–344. doi: 10.1126/science.169.3943.339. [DOI] [PubMed] [Google Scholar]
  20. Punt P. J., Oliver R. P., Dingemanse M. A., Pouwels P. H., van den Hondel C. A. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene. 1987;56(1):117–124. doi: 10.1016/0378-1119(87)90164-8. [DOI] [PubMed] [Google Scholar]
  21. Rogers S., Wells R., Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986 Oct 17;234(4774):364–368. doi: 10.1126/science.2876518. [DOI] [PubMed] [Google Scholar]
  22. Sweigard J. A., Chumley F. G., Valent B. Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet. 1992 Mar;232(2):183–190. [PubMed] [Google Scholar]
  23. Terenzi H. F., Flawia M. M., Tellez-Inon M. T., Torres H. N. Control of Neurospora crassa morphology by cyclic adenosine 3', 5'-monophosphate and dibutyryl cyclic adenosine 3', 5'-monophosphate. J Bacteriol. 1976 Apr;126(1):91–99. doi: 10.1128/jb.126.1.91-99.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Uno I., Ishikawa T. Metabolism of adenosine 3',5'-cyclic monophosphate and induction of fruiting bodies in Coprinus macrorhizus. J Bacteriol. 1973 Mar;113(3):1249–1255. doi: 10.1128/jb.113.3.1249-1255.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wang J., Suzuki N., Nishida Y., Kataoka T. Analysis of the function of the 70-kilodalton cyclase-associated protein (CAP) by using mutants of yeast adenylyl cyclase defective in CAP binding. Mol Cell Biol. 1993 Jul;13(7):4087–4097. doi: 10.1128/mcb.13.7.4087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Woo S. S., Jiang J., Gill B. S., Paterson A. H., Wing R. A. Construction and characterization of a bacterial artificial chromosome library of Sorghum bicolor. Nucleic Acids Res. 1994 Nov 25;22(23):4922–4931. doi: 10.1093/nar/22.23.4922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yamawaki-Kataoka Y., Tamaoki T., Choe H. R., Tanaka H., Kataoka T. Adenylate cyclases in yeast: a comparison of the genes from Schizosaccharomyces pombe and Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5693–5697. doi: 10.1073/pnas.86.15.5693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yelton M. M., Hamer J. E., Timberlake W. E. Transformation of Aspergillus nidulans by using a trpC plasmid. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1470–1474. doi: 10.1073/pnas.81.5.1470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zhu H., Choi S., Johnston A. K., Wing R. A., Dean R. A. A large-insert (130 kbp) bacterial artificial chromosome library of the rice blast fungus Magnaporthe grisea: genome analysis, contig assembly, and gene cloning. Fungal Genet Biol. 1997 Jun;21(3):337–347. doi: 10.1006/fgbi.1997.0996. [DOI] [PubMed] [Google Scholar]

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