The small GTPase BcCdc42 affects nuclear division, germination and virulence of the gray mold fungus Botrytis cinerea

Fungal Genetics and Biology

Volumn 48, Issue 11, 2011, Pages 1012-1019

  Kokkelink, Leonie ^a,d   Minz, Anna ^b   Al Masri, Muhamad ^c   Giesbert, Sabine ^a   Barakat, Radwan ^c   Sharon, Amir ^b   Tudzynski, Paul ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b TEL AVIV UNIVERSITY   (Israel)

^c HEBRON UNIVERSITY   (Palestine)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Cell cycle; G proteins; Host pathogen interaction; Pathogenic fungi

Indexed keywords

GUANOSINE TRIPHOSPHATASE;

ARTICLE; BOTRYTIS CINEREA; CELL DIFFERENTIATION; CONIDIUM; CONTROLLED STUDY; FUNGAL CELL; FUNGAL GENOME; FUNGAL SPORE GERMINATION; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE DELETION; GENE SEQUENCE; GROWTH RATE; HOST PATHOGEN INTERACTION; NONHUMAN; NUCLEAR DIVISION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; VEGETATIVE GROWTH; WILD TYPE;

BOTRYTIS; CDC42 GTP-BINDING PROTEIN; CELL NUCLEUS DIVISION; GENE DELETION; HYPHAE; PHASEOLUS; PLANT DISEASES; SPORES, FUNGAL; VIRULENCE;

BOTRYOTINIA FUCKELIANA; EUKARYOTA; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 80053278713     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.07.007     Document Type: Article

References (43)

1. Bourne H.R., Sanders D.A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature 1991, 349:117-127.
2. Boyce K.J., Hynes M.J., Andrianopoulos A. The CDC42 homolog of the dimorphic fungus Penicillium marneffei is required for correct cell polarization during growth but not development. J. Bacteriol. 2001, 183:3447-3457.
3. Boyce K.J., Hynes M.J., Andrianopoulos A. Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. J. Cell Sci. 2003, 116:1249-1260.
4. Boyce K.J., Hynes M.J., Andrianopoulos A. The Ras and Rho GTPases genetically interact to co-ordinately regulate polarity during development in Penicillium marneffei. Mol. Microbiol. 2005, 55:1487-1501.
5. Cenis J.L. Rapid extraction of fungal DNA for PCR amplification. Nucl. Acid Res. 1992, 20:2380.
6. Cerione R.A. Cdc42: new roads to travel. Trends Cell Biol. 2004, 14:127-132.
7. Chen C., Dickman M.B. CAMP blocks MAPK activation and sclerotial development via Rap-1 in a PKA- independent manner in Sclerotinia sclerotiorum. Mol. Microbiol. 2005, 55:299-311.
8. Chen C., Ha Y.S., Min J.Y., Memmott S.D., Dickman M.B. Cdc42 is required for proper growth and development in the fungal pathogen Colletotrichum trifolii. Eukaryot. Cell 2006, 5:155-166.
9. Diebold B.A., Fowler B., Lu J., Dinauer M.C., Bokoch G.M. Antagonistic cross-talk between Rac and Cdc42 GTPases regulates generation of reactive oxygen species. J. Biol. Chem. 2004, 279:28136-28281.
10. Döhlemann G., Berndt P., Hahn M. Different signalling pathways involving a Gα protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol. Microbiol. 2006, 59:821-835.
11. Etienne-Manneville S. Cdc42 - the centre of polarity. J. Cell Sci. 2004, 117:1291-1300.
12. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
13. Finkelshtein A., Shlezinger A., Bunis O., Sharon A. Botrytis cinerea BcNma is involved in apoptotic cell death but not in stress adaptation. Fungal Genet. Biol. 2011, 48:621-630.
14. Freitag M., Hickey P.C., Raju N.B., Sekler E.U., Read N.D. GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet. Biol. 2004, 41:897-910.
15. Harris S.D. Cdc42/Rho GTPases in fungi: variations on a common theme. Mol. Microbiol. 2011, 79:1123-1127.
16. Johnson D.I. Ddc42: an essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 1999, 63:54-105.
17. Kim J.M., Lu L., Shao R.Z., Chin J.L., Liu B. Isolation of mutations that bypass the requirement of the septation initiation network for septum formation and conidiation in Aspergillus nidulans. Genetics 2006, 173:685-696.
18. Kwon M.J., Arentshorst M., Roos E.D., van den Hondel C.A.M.J.J., Ram A.F.J. Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi. Mol. Microbiol. 2011, 79:1151-1167.
19. Lew D. The morphogenesis checkpoint: how yeast cells watch their figures. Curr. Opin. Cell Biol. 2003, 15:648-653.
20. Mahlert M., Leveleki L., Hlubek A., Sandrock B., Bölker M. Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol. Microbiol. 2006, 59:567-578.
21. Malonek S., Rojas M., Hedden P., Gaskin P., Tudzynski B. The NADPH cytochrome P450 reductase gene from Gibberella fujikuroi is essential for gibberellins biosynthesis. J. Biol. Chem. 2004, 279:25075-25084.
22. Nesher I., Barhoom S., Sharon A. Cell cycle and cell death are not necessary for appressorium formation and plant infection in the fungal plant pathogen Colletotrichum gloeosporioides. BMC Biol. 2008, 6:9.
23. Nesher I., Minz A., Kokkelink L., Tudzynski P., Sharon A. Regulation of pathogenic spore germination by CgRac1 in the fungal plant pathogen Colletotrichum gloeosporioides. Eukaryotic Cell 2011, 10:1127-1130.
24. Park H.-O., Bi E. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 2007, 71:48-96.
25. Pontecorvo G.V., Roper J.A., Hemmonns L.M., MacDonald K.D., Buften A.W. The genetics of Aspergillus nidulans. Adv. Genet. 1953, 141:141-238.
26. Quidde T., Büttner P., Tudzynski P. Evidence for three different specific saponin-detoxifying activities in Botrytis cinerea and cloning of a gene coding for a putative avenacinase. Eur. J. Plant. Pathol. 1999, 105:273-283.
27. Rolke Y., Tudzynski P. The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol. Microbiol. 2008, 68:405-423.
28. Rui O., Hahn M. The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol. Plant Pathol. 2007, 8:173-184.
29. Saunders D.G.O., Dagdas Y.F., Talbot N.J. Spatial uncoupling of mitosis and cytokinesis during appressorium-mediated plant infection by the rice blst fungus Magnaporthe oryzae. Plant cell 2010, 22:2417-2428.
30. Scheffer J., Chen C., Heidrich P., Dickman M.B., Tudzynski P. A CDC42 homologue in Claviceps purpurea is involved in vegetative differentiation and is essential for pathogenicity. Eukaryot. Cell 2005, 4:1228-1238.
31. Schulze Gronover C., Kasulke D., Tudzynski P., Tudzynski B. The role of G protein alpha subunits in the infection process of the gray mold fungus Botrytis cinerea. Mol. Plant-Microbe Interact. 2001, 14:1293-1302.
32. Schumacher J., Viaud M., Simon A., Tudzynski B. The Gα subunit BCG1, the phospholipase C BcPLC1) and the calcineurin phosphatase co-ordinately regulate gene expression in the grey mould fungus Botrytis cinerea. Mol. Microbiol. 2008, 67:1027-1050.
33. Schumacher J., Kokkelink L., Huesmann C., Jimenez-Teja D., Collado I.G., Barakat R., et al. The cAMP-dependent signaling pathway and its role in conidial germination, growth, and virulence of the gray mold Botrytis cinerea. Mol. Plant-Microbe Interact. 2008, 21:1443-1459.
34. Segmüller N., Ellendorf U., Tudzynski B., Tudzynski P. BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot. Cell 2007, 6:211-221.
35. Segmüller N., Kokkelink L., Giesbert S., Odinius D., van Kan J., Tudzynski P. NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol. Plant-Microbe Interact. 2008, 21:808-819.
36. Semighini C.P., Harris S.D. Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 2008, 179:1919-1932.
37. Shlezinger, N., Minz, A., Gur, Y., Hatam, I., Dagdas, Y.F., Talbot, N.J., Sharon, A., in press. Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PloS Pathogen.
38. Sudbery P.E. Regulation of polarised growth in fungi. Fungal Biol. Rev. 2008, 22:44-55.
39. van Kan J.A.L. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 2006, 11:247-253.
40. Virag A., Lee M.P., Si H., Harris S.D. Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Mol. Microbiol. 2007, 66:1579-1596.
41. Wennerberg K., Rossman K.L., Der C.J. The Ras superfamily at a glance. J. Cell Sci. 2005, 118:843-846.
42. Williamson B., Tudzynski B., Tudzynski P., van Kan J.A.L. Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol. 2007, 8:561-580.
43. Zheng W., Zhao Z., Chen J., Liu W., Ke H., Zhou J., Lu G., Darvill A.G., Albersheim P., Wu S., Wang Z. A Cdc42 ortholog is required for penetration and virulence of Magnaporthe grisea. Fungal Genet. Biol. 2009, 46:450-460.