WSC-1 and HAM-7 are MAK-1 MAP kinase pathway sensors required for cell wall integrity and hyphal fusion in Neurospora crassa

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Maddi, Abhiram ^a   Dettman, Anne ^b   Fu, Ci ^a   Seiler, Stephan ^b   Free, Stephen J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN HAM 7; PROTEIN MAK 1; PROTEIN SERINE THREONINE KINASE; PROTEIN WSC 1; UNCLASSIFIED DRUG;

ARTICLE; CELL WALL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FUNGAL GENE; FUNGAL LIFE CYCLE STAGE; FUNGAL STRAIN; FUNGUS HYPHAE; GENE DELETION; GENE IDENTIFICATION; GENE MUTATION; HAM 7 GENE; MORPHOLOGY; NEUROSPORA CRASSA; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; STRESS; WSC 1 GENE;

CELL WALL; DNA MUTATIONAL ANALYSIS; ENZYME ACTIVATION; FUNGAL PROTEINS; GENE DELETION; GENETIC COMPLEMENTATION TEST; HYPHAE; MAP KINASE SIGNALING SYSTEM; MEMBRANE FUSION; MUTANT PROTEINS; NEUROSPORA CRASSA; PHENOTYPE; PROTEIN KINASES; REPRODUCTION, ASEXUAL;

NEUROSPORA CRASSA;

EID: 84864555837     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042374     Document Type: Article

References (53)

1. Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B, Castro-Longoria E, et al. (2011) Architecture and development of the Neurospora crassa hypha - a model cell for polarized growth. Fungal Biol 115: 446-474.
2. Klis FM, Boorsma A, De Groot PW, (2006) Cell wall construction in Saccharomyces cerevisiae. Yeast 23: 185-202.
3. Chaffin WL, (2008) Candida albicans cell wall proteins. Microbiol Mol Biol Rev 72: 495-544.
4. Latge JP, (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66: 279-290.
5. Gastebois A, Clavaud C, Aimanianda V, Latge JP, (2009) Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol 4: 583-595.
6. Bowman SM, Free SJ, (2006) The structure and synthesis of the fungal cell wall. Bioessays 28: 799-808.
7. Seiler S, Plamann M, (2003) The genetic basis of cellular morphogenesis in the filamentous fungus Neurospora crassa. Mol Biol Cell 14: 4352-4364.
8. Bowman SM, Piwowar A, Al Dabbous M, Vierula J, Free SJ, (2006) Mutational analysis of the glycosylphosphatidylinositol (GPI) anchor pathway demonstrates that GPI-anchored proteins are required for cell wall biogenesis and normal hyphal growth in Neurospora crassa. Eukaryot Cell 5: 587-600.
9. Maddi A, Bowman SM, Free SJ, (2009) Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet Biol 46: 768-781.
10. Lesage G, Bussey H, (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 317-343.
11. Rispail N, Soanes DM, Ant C, Czajkowski R, Grunler A, et al. (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet Biol 46: 287-298.
12. Levin DE, (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189: 1145-1175.
13. Verna J, Lodder A, Lee K, Vagts A, Ballester R, (1997) A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94: 13804-13809.
14. Rodicio R, Heinisch JJ, (2010) Together we are strong-cell wall integrity sensors in yeasts. Yeast 27: 531-540.
15. Maerz S, Ziv C, Vogt N, Helmstaedt K, Cohen N, et al. (2008) The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179: 1313-1325.
16. Park G, Pan S, Borkovich KA, (2008) Mitogen-activated protein kinase cascade required for regulation of development and secondary metabolism in Neurospora crassa. Eukaryot Cell 7: 2113-2122.
17. Fleissner A, Simonin AR, Glass NL, (2008) Cell fusion in the filamentous fungus, Neurospora crassa. Methods Mol Biol 475: 21-38.
18. Read ND, Gorychev AB, Lichius A, (2012) The mechanistic basis of self-fusion between conidial anastomosis tubes during fungal colony initiation. Fungal Biol Rev 26: 1-11.
19. Fleissner A, Leeder AC, Roca MG, Read ND, Glass NL, (2009) Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci U S A 106: 19387-19392.
20. Pandey A, Roca MG, Read ND, Glass NL, (2004) Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot Cell 3: 348-358.
21. Goryachev AB Lichius A, Wright GD, Read ND, (2012) Excitable behavior can explain the "ping-pong" mode of communication between cells using the same chemoattractant. Bioessay 34: 259-266.
22. Fu C, Iyer P, Herkal A, Abdullah J, Stout A, et al. (2011) Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot Cell 10: 1100-1109.
23. De Groot PW, Hellingwerf KJ, Klis FM, (2003) Genome-wide identification of fungal GPI proteins. Yeast 20: 781-796.
24. Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F, (2004) A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J Mol Biol 337: 243-253.
25. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
26. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103: 10352-10357.
27. Dunlap JC, Borkovich KA, Henn MR, Turner GE, Sachs MS, et al. (2007) Enabling a community to dissect an organism: overview of the Neurospora functional genomics project. Adv Genet 57: 49-96.
28. McCluskey K, Wiest A, Plamann M, (2010) The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci 35: 119-126.
29. Davis RH, De Serres FJ, (1970) Genetic and microbiological research techniques for Neurospora crassa. Meth Enzymol 27: 79-143.
30. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, 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.
31. Maddi A, Free SJ, (2010) alpha-1,6-Mannosylation of N-linked oligosaccharide present on cell wall proteins is required for their incorporation into the cell wall in the filamentous fungus Neurospora crassa. Eukaryot Cell 9: 1766-1775.
32. Margolin BS, Freitag M, Selker EU, (1997) Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa. Fungal Genet Newsl 44: 34-36.
33. Selker EU, (1999) Gene silencing: repeats that count. Cell 97: 157-160.
34. Maerz S, Dettmann A, Ziv C, Liu Y, Valerius O, et al. (2009) Two NDR kinase-MOB complexes function as distinct modules during septum formation and tip extension in Neurospora crassa. Mol Microbiol 74: 707-723.
35. Maerz S, Dettmann A, Seiler S, (2012) Hydrophobic Motif Phosphorylation Coordinates Activity and Polar Localization of the Neurospora crassa Nuclear Dbf2-Related Kinase COT1. Mol Cell Biol 32: 2083-2098.
36. Richthammer C, Enseleit M, Sanchez-Leon E, Marz S, Heilig Y,et al. (2012) RHO1 and RHO2 share partially overlapping functions in the regulation of cell wall integrity and hyphal polarity in Neurospora crassa. Mol Microbiol in press.
37. Vogt N, Seiler S, (2008) The RHO1-specific GTPase-activating protein LRG1 regulates polar tip growth in parallel to Ndr kinase signaling in Neurospora. Mol Biol Cell 19: 4554-4569.
38. Aldabbous MS, Roca MG, Stout A, Huang IC, Read ND, et al. (2010) The ham-5, rcm-1 and rco-1 genes regulate hyphal fusion in Neurospora crassa. Microbiology 156: 2621-2629.
39. Xiang Q, Rasmussen C, Glass NL, (2002) The ham-2 locus, encoding a putative transmembrane protein, is required for hyphal fusion in Neurospora crassa. Genetics 160: 169-180.
40. Fleissner A, Sarkar S, Jacobson DJ, Roca MG, Read ND, et al. (2005) The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot Cell 4: 920-930.
41. Simonin AR, Rasmussen CG, Yang M, Glass NL, (2010) Genes encoding a striatin-like protein (ham-3) and a forkhead associated protein (ham-4) are required for hyphal fusion in Neurospora crassa. Fungal Genet Biol 47: 855-868.
42. Bowman SM, Piwowar A, Ciocca M, Free SJ, (2005) Mannosyltransferase is required for cell wall biosynthesis, morphology and control of asexual development in Neurospora crassa. Mycologia 97: 872-879.
43. Maerz S, Funakoshi Y, Negishi Y, Suzuki T, Seiler S, (2010) The Neurospora peptide:N-glycanase ortholog PNG1 is essential for cell polarity despite its lack of enzymatic activity. J Biol Chem 285: 2326-2332.
44. Philip B, Levin DE, (2001) Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol Cell Biol 21: 271-280.
45. Futagami T, Nakao S, Kido Y, Oka T, Kajiwara Y, et al. (2011) Putative stress sensors WscA and WscB are involved in hypo-osmotic and acidic pH stress tolerance in Aspergillus nidulans. Eukaryot Cell 10: 1504-1515.
46. Dichtl K, Helmschrott C, Dirr F, Wagener J, (2012) Deciphering cell wall integrity signalling in Aspergillus fumigatus: identification and functional characterization of cell wall stress sensors and relevant Rho GTPases. Mol Microbiol 83: 506-519.
47. Dupres V, Alsteens D, Wilk S, Hansen B, Heinisch JJ, et al. (2009) The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo. Nat Chem Biol 5: 857-862.
48. Khatun R, Lakin-Thomas P, (2010) Activation and localization of protein kinase C in Neurospora crassa. Fungal Genet Biol 48: 465-473.
49. Heinisch JJ, Dupres V, Wilk S, Jendretzki A, Dufrene YF, (2010) Single-molecule atomic force microscopy reveals clustering of the yeast plasma-membrane sensor Wsc1. PLoS One 5: e11104.
50. Kothe GO, Free SJ, (1998) The isolation and characterization of nrc-1 and nrc-2, two genes encoding protein kinases that control growth and development in Neurospora crassa. Genetics 149: 117-130.
51. Li D, Bobrowicz P, Wilkinson HH, Ebbole DJ, (2005) A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170: 1091-1104.
52. Leeder AC, Palma-Guerrero J, Glass NL, (2011) The social network: deciphering fungal language. Nat Rev Microbiol 9: 440-451.
53. Roca MG, Weichert M, Siegmund U, Tudzynski P, Fleissner A, (2012) Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol 116: 379-387.