Traffic of chitin synthase 1 (CHS-1) to the spitzenkörper and developing septa in hyphae of neurospora crassa: Actin dependence and evidence of distinct microvesicle populations

Eukaryotic Cell

Volumn 10, Issue 5, 2011, Pages 683-695

  Sánchez León, Eddy ^a   Verdín, Jorge ^a   Freitag, Michael ^b   Roberson, Robert W ^c   Bartnicki Garcia, Salomon ^a   Riquelme, Meritxell ^a  

^a Center for Scientific Research and Higher Education of Ensenada (CICESE)   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CHITIN SYNTHASE; FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN;

ARTICLE; CYTOLOGY; CYTOPLASM VESICLE; ENZYMOLOGY; FLUORESCENCE MICROSCOPY; FUNGUS HYPHAE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROFILAMENT; NEUROSPORA CRASSA; PHYSIOLOGY;

ACTINS; CHITIN SYNTHASE; CYTOPLASMIC VESICLES; FUNGAL PROTEINS; GREEN FLUORESCENT PROTEINS; HYPHAE; MICROFILAMENTS; MICROSCOPY, FLUORESCENCE; NEUROSPORA CRASSA;

FUNGI; NEUROSPORA CRASSA;

EID: 79956025848     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00280-10     Document Type: Article

References (44)

1. Araujo-Bazán, L., M. A. Peñalva, and E. A. Espeso. 2008. Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol. Microbiol. 67:891-905.
2. Araujo-Palomares, C. L., E. Castro-Longoria, and M. Riquelme. 2007. Ontogeny of the spitzenkörper in germlings of Neurospora crassa. Fungal Genet. Biol. 44:492-503.
3. Bartnicki-Garcia, S. 1968. Cell wall chemistry, morphogenesis and taxonomy of fungi. Annu. Rev. Microbiol. 22:87-107.
4. Berepiki, A., A. Lichius, J.-Y. Shoji, J. Tilsner, and N. D. Read. 2010. F-actin dynamics in Neurospora crassa. Eukaryot. Cell 9:547-557.
5. Borgia, P. T., et al. 1996. The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet. Biol. 20:193-203.
6. Borkovich, K. A., et al. 2004. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 68:1-108.
7. Bulawa, C. E. 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47:505-534.
8. Bull, A. T. 1970. Chemical composition of wild-type and mutant Aspergillus nidulans cell walls. The nature of polysaccharide and melanin constituents. J. Gen. Microbiol. 63:75-94.
9. Choquer, M., M. Boccara, I. R. Gonçalves, M. Soulié, and A. Vidal-Cros. 2004. Survey of the Botrytis cinerea chitin synthase multigenic family through the analysis of six euascomycetes genomes. Eur. J. Biochem. 271:2153-2164.
10. Colot, H. V., et al. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U. S. A. 13:10352-10357.
11. Delgado-Alvarez, D. L., et al. 2010. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genet. Biol. 47:573-586.
12. Freitag, M., P. C. Hickey, N. B. Raju, E. U. Selker, and N. D. Read. 2004. GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 41:897-910.
13. Fukuda, K., et al. 2009. Class III chitin synthase ChsB of Aspergillus nidulans localizes at the sites of polarized cell wall synthesis and is required for conidial development. Eukaryot. Cell 8:945-956.
14. Galagan, J. E., et al. 2003. Genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868.
15. Glaser, L., and D. H. Brown. 1957. The synthesis of chitin in cell free extracts of Neurospora crassa. J. Biol. Chem. 228:729-742.
16. Helms, J. B., and J. E. Rothman. 1992. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360:352-354.
17. Hickey, P. C., S. M. Swift, M. G. Roca, and N. D. Read. 2005. Live-cell imaging of filamentous fungi using vital fluorescent dyes. Methods Microbiol. 34:63-87.
18. Kasuga, T., et al. 2005. Long-oligomer microarray profiling in Neurospora crassa reveals the transcriptional program underlying biochemical and physiological events of conidial germination. Nucleic Acids Res. 33:6469-6485.
19. Leal-Morales, C., C. E. Bracker, and S. Bartnicki-Garcia. 1988. Localization of chitin synthase in cell-free homogenates of Saccharomyces cerevisiae: chitosomes and plasma membrane. Proc. Natl. Acad. Sci. U. S. A. 85:8516-8520.
20. Leal-Morales, C. A., C. E. Bracker, and S. Bartnicki-Garcia. 1994. Subcellular localization, abundance and stability of chitin synthetases 1 and 2 from Saccharomyces cerevisiae. Microbiology 140:2207-2216.
21. Lopez-Franco, R., S. Bartnicki-Garcia, and C. E. Bracker. 1994. Pulsed growth of fungal hyphal tips. Proc. Natl. Acad. Sci. U. S. A. 91:12228-12232.
22. Mandel, M. A., J. N. Galgiani, S. Kroken, and M. J. Orbach. 2006. Coccidioides posadasii contains single chitin synthase genes corresponding to classes I to VII. Fungal Genet. Biol. 43:775-788.
23. Martinez, J. P., G. Gimenez, C. E. Bracker, and S. Bartnicki-Garcia. 1989. Sedimentation properties of chitosomal chitin synthetase from the wild-type strain and the 'slime' variant of Neurospora crassa. Biochim. Biophys. Acta 990:45-52. (Erratum, 1073:239, 1991.)
24. Martín-Udíroz, M., M. P. Madrid, and M. I. G. Roncero. 2004. Role of chitin synthase genes in Fusarium oxysporum. Microbiol. Mol. Biol. Rev. 150:3175-3187.
25. Mourino-Perez, R. R., R. W. Roberson, and S. Bartnicki-Garcia. 2006. Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa. Fungal Genet. Biol. 43:389-400.
26. Nickel, W. 2005. Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6:607-614.
27. Ninomiya, Y., K. Suzuki, C. Ishii, and H. Inoue. 2004. Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc. Natl. Acad. Sci. U. S. A. 101:12248-12253.
28. Pantazopoulou, A., and M. A. Penalva. 2009. Organization and dynamics of the Aspergillus nidulans golgi during apical extension and mitosis. Mol. Biol. Cell 20:4335-4347.
29. Read, N. D., and P. C. Hickey. 2001. The vesicle trafficking network and tip growth in fungal hyphae, p. 137-146. In A. Geitmann, M. Cresti, and I. B. Heath (ed.), Cell biology of plant and fungal tip growth. IOS Press, Amsterdam, Netherlands.
30. Riquelme, M., and S. Bartnicki-García. 2008. Advances in understanding hyphal morphogenesis: ontogeny, phylogeny and cellular localization of chitin synthases. Fungal Biol. Rev. 22:56-70.
31. Riquelme, M., et al. 2007. Spitzenkörper localization and intracellular trafficof green fluorescent protein-labeled CHS-3 and CHS-6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot. Cell 6:1853-1864.
32. Riquelme, M., C. G. Reynaga-Pena, G. Gierz, and S. Bartnicki-Garcia. 1998. What determines growth direction in fungal hyphae? Fungal Genet. Biol. 24:101-109.
33. Ruiz-Herrera, J., C. G. Leon, A. Carabez-Trejo, and E. Reyes-Salinas. 1996. Structure and chemical composition of the cell walls from the haploid yeast and mycelial forms of Ustilago maydis. Fungal Genet. Biol. 20:133-142.
34. Schmit, J. C., C. M. Edson, and S. Brody. 1975. Changes in glucosamine and galactosamine levels during conidial germination in Neurospora crassa. J. Bacteriol. 122:1062-1070.
35. Schoffelmeer, E. A. M., F. M. Klis, J. H. Sietsma, and B. J. C. Cornelissen. 1999. The cell wall of Fusarium oxysporum. Fungal Genet. Biol. 27:275-282.
36. Soulié, M. C., et al. 2006. Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell. Microbiol. 8:1310-1321.
37. Treitschke, S., G. Doehlemann, M. Schuster, and G. Steinberg. 2010. They myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell 22:2476-2494.
38. Upadhyay, S., and B. D. Shaw. 2008. The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol. Microbiol. 68:690-705.
39. Verdín, J., S. Bartnicki-Garcia, and M. Riquelme. 2009. Functional stratification of the Spitzenkörper of Neurospora crassa. Mol. Microbiol. 74:1044-1053.
40. Virag, A., and A. J. Griffiths. 2004. A mutation in the Neurospora crassa actin gene results in multiple defects in tip growth and branching. Fungal Genet. Biol. 41:213-225.
41. Vogel, H. J. 1956. A convenient growth medium for Neurospora (medium N). Microbiol. Gen. Bull. 13:42-43.
42. Werner, S., J. A. Sugui, G. Steinberg, and H. B. Deising. 2007. A chitin synthase with a myosin-like motor domain is essential for hyphal growth,appressorium differentiation, and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol. Plant Microbe Interact. 20:1555-1567.
43. Westergaard, M., and H. K. Mitchell. 1942. Neurospora V. A synthetic medium favoring sexual reproduction. Am. J. Bot. 14:573-577.
44. Yarden, O., and C. Yanofsky. 1991. Chitin synthase 1 plays a major role in cell wall biogenesis in Neurospora crassa. Genes Dev. 5:2420-2430.