Sclerotial development in Sclerotinia sclerotiorum: awakening molecular analysis of a "Dormant" structure

Fungal Biology Reviews

Volumn 22, Issue 1, 2008, Pages 6-16

  Erental, A ^a   Dickman, M B ^b   Yarden, O ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Aspergillus flavus; Botrytis cinerea; Claviceps purpurea; Coprinus cinereus; Fungal development; Physarum polycephalum; Rhizoctonia solani; Sclerotium rolfsii; Ser Thr phosphatase

Indexed keywords

ASCOMYCOTA; ASPERGILLUS FLAVUS; ATHELIA ROLFSII; BASIDIOMYCOTA; BOTRYOTINIA FUCKELIANA; CLAVICEPS PURPUREA; COPRINOPSIS CINEREA; COPRINUS; FUNGI; HYPHOMYCETES; PHYSARUM POLYCEPHALUM; SCLEROTINIA SCLEROTIORUM; SCLEROTIUM (ASCOMYCOTA); SCLEROTIUM (BASIDIOMYCOTA); THANATEPHORUS CUCUMERIS;

EID: 44449127116     PISSN: 17494613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbr.2007.10.001     Document Type: Review

References (81)

1. Abawi G.S., and Grogan R.G. Epidemiology of diseases caused by Sclerotinia species. Phytopathology 69 (1979) 899-904
2. Adams D.S., Noonan D., and Jeffery W.R. Stored messenger ribonucleoprotein particles in differentiated sclerotia of Physarum polycephalum. Differentiation 20 (1981) 177-187
3. Adams P.B., and Ayers W.A. Ecology of Sclerotinia species. Phytopathology 69 (1979) 896-899
4. Ahn J.-H., McAvoy T., Rakhilin S.V., Nishi A., Greengard P., and Nairn A.C. Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56δ subunit. Proceedings of the National Academy of Sciences of the United States of America 104 (2007) 2979-2984
5. Boland G.J., and Hall R. Index of plant hosts of Sclerotinia sclerotiorum. Canadian Journal of Plant Pathology 16 (1994) 93-108
6. Bolton M.V., Bart P.H., Thomma J., and Nelson B.D. Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Molecular Plant Pathology 7 (2006) 1-16
7. Borkovich K.A., Alex L.A., Yarden O., Freitag M., Turner G.E., Read N.D., Seiler S., Bell-Pedersen D., Paietta J., Plesofsky N., Plamann M., Goodrich-Tanrikulu M., Schulte U., Mannhaupt G., Nargang F.E., Radford A., Selitrennikoff C., Galagan J.E., Dunlap J.C., Loros J.J., Catcheside D., Inoue H., Aramayo R., Polymenis M., Selker E.U., Sachs M.S., Marzluf G.A., Paulsen I., Davis R., Ebbole D.J., Zelter A., Kalkman E., O'Rourke R., Bowring F., Yeadon J., Ishii C., Suzuki K., Sakai W., and Pratt R. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiology and Molecular Biology Reviews 68 (2004) 1-108
8. Caddick M.X., Brownlee A.G., and Arst Jr. H.N. Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Molecular and General Genetics 203 (1986) 346-353
9. Calvo A.M., Bok J., Brooks W., Keller N.P., Hinze L.L., and Gardner H.W. veA is required for toxin and sclerotial production in Aspergillus parasiticus sporogenic effect of polyunsaturated fatty acids on development of Aspergillus spp. Applied and Environmental Microbiology 70 (2004) 4733-4739
10. Chen C.B., and Dickman M.B. cAMP blocks MAPK activation and sclerotial development via Rap-1 in a PKA-independent manner in Sclerotinia sclerotiorum. Molecular Microbiology 55 (2005) 299-311
11. Chen C.B., Harel A., Gorovoits R., Yarden O., and Dickman M.B. MAPK regulation of sclerotial development in Sclerotinia sclerotiorum is linked with pH and cAMP sensing. Molecular Plant-Microbe Interactions 17 (2004) 404-413
12. Chet I., and Henis Y. Effect of catechol and disodium EDTA on melanin content of hyphal and sclerotial walls of Sclerotium rolfsii Sacc. and the role of melanin in the susceptibility of these walls to (1 + 3) glucanase and chitinase. Soil Biology and Biochemistry 1 (1969) 131-138
13. Chet I., and Henis Y. Sclerotial morphogenesis in fungi. Annual Review of Phytopathology 13 (1975) 169-192
14. Chet I., Henis I., and Mitchell R. The morphogenetic effect of sulphur-containing amino acids, glutathione and iodoacetic acid on Sclerotium rolfsii Sacc. Journal of General Microbiology 45 (1966) 541-546
15. Dickman M.B., and Yarden O. Ser/Thr kinases and phosphatases in filamentous fungi. Fungal Genetics and Biology 26 (1999) 99-117
16. Doehlemann G., Berndt P., and Hahn M. Different signalling pathways involving a G alpha protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Molecular Microbiology 59 (2006) 821-835
17. Duran R.M., Cary J.W., and Calvo A.M. Production of cyclopiazonic acid, aflatrem, and aflatoxin by Aspergillus flavus is regulated by veA, a gene necessary for sclerotial formation. Applied Genetics Molecular Biotechnology 74 (2006) 1158-1168
18. Eliahu N., Igbaria A., Rose M.S., Horwitz B.A., and Lev S. Melanin biosynthesis in the maize pathogen Cochliobolus heterostrophus depends on two MAP kinases, Chk1 and Mps1, and the transcription factor Cmr1. Eukaryotic Cell 6 (2007) 421-429
19. Erental A., Harel A., and Yarden O. Type 2A phosphoprotein phosphatase is required for asexual development and pathogenesis of Sclerotinia sclerotiorum. Molecular Plant-Microbe Interactions 20 (2007) 944-954
20. Fang G.C., Hanau R.M., and Vaillancourt L. The SOD2 gene, encoding a manganese-type superoxide dismutase, is up-regulated during conidiogenesis in the plant pathogenic fungus Colletotrichum graminicola. Fungal Genetics and Biology 36 (2002) 155-165
21. Galagan J.E., Calvo S.E., Borkovich K.A., Selker E.U., Read N.D., Jaffe D., FitzHugh W., Ma L.J., Smirnov S., Purcell S., Rehman B., Elkins T., Engels R., Wang S., Nielsen C.B., Butler J., Endrizzi M., Qui D., Ianakiev P., Bell-Pedersen D., Nelson M.A., Werner-Washburne M., Selitrennikoff C.P., Kinsey J.A., Braun E.L., Zelter A., Schulte U., Kothe G.O., Jedd G., Mewes W., Staben C., Marcotte E., Greenberg D., Roy A., Foley K., Naylor J., Stange-Thomann N., Barrett R., Gnerre S., Kamal M., Kamvysselis M., Mauceli E., Bielke C., Rudd S., Frishman D., Krystofova S., Rasmussen C., Metzenberg R.L., Perkins D.D., Kroken S., Cogoni C., Macino G., Catcheside D., Li W., Pratt R.J., Osmani S.A., DeSouza C.P., Glass L., Orbach M.J., Berglund J.A., Voelker R., Yarden O., Plamann M., Seiler S., Dunlap J., Radford A., Aramayo R., Natvig D.O., Alex L.A., Mannhaupt G., Ebbole D.J., Freitag M., Paulsen I., Sachs M.S., Lander E.S., Nusbaum C., and Birren B. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422 (2003) 859-868
22. Georgiou C.D., Patsoukis N., Papapostolou I., and Zervoudakis G. Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integrative and Comparative Biology 46 (2006) 691-712
23. Georgiou C.D., Tairis N., and Sotiropoulou A. Hydroxyl radical scavengers inhibit sclerotial differentiation and growth in Sclerotinia sclerotiorum and Rhizoctonia solani. Mycological Research 104 (2000) 1191-1196
24. Glass N.L., Rasmussen C., Roca M.G., and Read N.D. Hyphal homing, fusion and mycelial interconnectedness. Trends in Microbiology 12 (2004) 135-141
25. Godoy G., Steadman J.R., Dickman M.B., and Dam R. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiological and Molecular Plant Pathology 37 (1990) 179-191
26. Goujon M. Physiological mechanisms in the formation of sclerotia in Corticium rolfsii (Sacc.) Curzi. Physiologie Vegetale 8 (1970) 349-360
27. Hadar Y., Henis Y., and Chet I. The potential for the formation of sclerotia in submerged mycelium of Sclerotinia rolfsii. Journal of General Microbiology 122 (1981) 137-141
28. Hadar Y., Pines M., Chet I., and Henis Y. The regulation of sclerotium initiation in sclerotium rolfsii by glucose and cyclic-AMP. Canadian Journal of Microbiology 29 (1983) 21-26
29. Halaouli S., Asther M., Sigoillot J.C., Hamdi M., and Lomascolo A. Fungal tyrosinases: new prospects in molecular characteristics, bioengineering and biotechnological applications. Journal of Applied Microbiology 100 (2006) 219-232
30. Hansberg W., and Aguirre J. Hyperoxidant states cause microbial cell-differentiation by cell isolation from dioxygen. Journal of Theoretical Biology 142 (1990) 201-221
31. Harel A., Bercovich S., and Yarden O. Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Molecular Plant-Microbe Interactions 19 (2006) 682-693
32. Harel A., Gorovits R., and Yarden O. Changes in protein kinase A activity accompany sclerotial development in Sclerotinia sclerotiorum. Phytopathology 95 (2005) 397-404
33. Hashiba T., and Ishikawa T. Effect of adenosine 3′,5′-cyclic monophosphate on induction of sclerotia in Rhizoctonia solani. Phytopathology 68 (1978) 1723-1727
34. Henis Y., Okon Y., and Chet I. The relationship between early hyphal branching and sclerotial formation in Sclerotium rolfsii. Journal of General Microbiology 79 (1973) 147-150
35. Henson J.M., Butler M.J., and Day A.W. The dark side of the mycelium: melanins of phytopathogenic fungi. Annual Review of Phytopathology 37 (1999) 447-471
36. Hou Z., Xue C., Peng Y., Katan T., Kistler H.C., and Xu J.R. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Molecular Plant-Microbe Interactions 15 (2002) 1119-1127
37. Jurick W.M., Dickman M.B., and Rollins J.A. Characterization and functional analysis of a cAMP-dependent protein kinase A catalytic sub unit gene (pka1) in Sclerotinia sclerotiorum. Physiological and Molecular Plant Pathology 64 (2004) 155-163
38. Jurick W.M., and Rollins J.A. Deletion of the adenylate cyclase (sac1) gene affects multiple developmental pathways and pathogenicity in Sclerotinia sclerotiorum. Fungal Genetics and Biology 44 (2007) 521-530
39. Kafadar K.A., and Cyert M.S. Integration of stress responses: modulation of calcineurin signaling in Saccharomyces cerevisiae by protein kinase A. Eukaryotic Cell 3 (2004) 1147-1153
40. Kim D.S., Park S.H., Kwon S.B., Youn S.W., Park E.S., and Park K.C. Heat treatment decreases melanin synthesis via protein phosphatase 2A inactivation. Cellular Signalling 17 (2005) 1023-1031
41. Kohn L.M., Carbone I., and Anderson J.B. Mycelial interactions in Sclerotinia-Sclerotiorum. Experimental Mycology 14 (1990) 255-267
42. Kojima K., Kikuchi T., Takano Y., Oshiro E., and Okuno T. The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. Molecular Plant-Microbe Interactions 15 (2002) 1268-1276
43. Kritzman G., Chet I., and Henis Y. Metabolism of L-threonine and its relationship to sclerotium formation in Sclerotium rolfsii. Journal of General Microbiology 95 (1976) 78-86
44. Kronstad J., de Maria A., Funnell D., Laidlaw R.D., Lee N., de Sa M.M., and Ramesh M. Signalling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathway. Archives of Microbiology 170 (1998) 395-404
45. Lara-Ortiz T., Riveros-Rosas H., and Aguirre J. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Molecular Microbiology 50 (2003) 1241-1255
46. Lee N., D'Souza C.A., and Kronstad J.W. Of smuts, blasts, mildews, and blights: cAMP signaling in phytopathogenic fungi. Annual Review of Phytopathology 41 (2003) 399-427
47. Lengeler K.B., Davidson R.C., D'Souza C., Harashima T., Shen W.C., Wang P., Pan X., Waugh M., and Heitman J. Signal transduction cascades regulating fungal development and virulence. Microbiology and Molecular Biology Reviews 64 (2000) 746-785
48. Léveillé J.M. Mémoire sur le genre sclerotium. Annales des Sciences Naturelles. Botanique 20 (1843) 218-248
49. Liu Y., and Bell-Pedersen D. Circadian rhythms in Neurospora crassa and other filamentous fungi. Eukaryotic Cell 5 (2006) 1184-1193
50. Marukawa S., Funakawa S., and Satomura Y. Role of sclerin on morphogenesis in Sclerotinia sclerotiorum de Bary (including S. libertiana Fuckel). Agricultural and Biological Chemistry 39 (1975) 645-650
51. Mehrabi R., Van der Lee T., Waalwijk C., and Gert H.J. MgSlt2, a cellular integrity MAP kinase gene of the fungal wheat pathogen Mycosphaerella graminicola, is dispensable for penetration but essential for invasive growth. Molecular Plant-Microbe Interactions 19 (2006) 389-398
52. Mitsushita J., Lambeth J.D., and Kamata T. The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Research 64 (2004) 3580-3585
53. Munir E., Yoon J.J., Tokimatsu T., Hattori T., and Shimada M. A physiological role for oxalic acid biosynthesis in the wood-rotting basidiomycete Fomitopsis palustris. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 11126-11130
54. Ng T.B. Peptides and proteins from fungi. Peptides 25 (2004) 1055-1073
55. Okon Y., Chet I., and Henis Y. Lactose-induced synchronous sclerotium formation in Sclerotium rolfsii and its inhibition by ethanol. Journal of General Microbiology 71 (1972) 465-470
56. Ortega-Perez I., Cano E., Were F., Villar M., Vazquez J., and Redondo J.M. c-Jun N-terminal kinase (JNK) positively regulates NFATc2 transactivation through phosphorylation within the N-terminal regulatory domain. Journal of Biological Chemistry 280 (2005) 20867-20878
57. Panaccione D.G. Origins and significance of ergot alkaloid diversity in fungi. FEMS Microbiology Letters 251 (2005) 9-17
58. Punja Z.K. The biology, ecology and control of Sclerotium rolfsii. Annual Review of Phytopathology 23 (1985) 97-127
59. Purdy L.H. Sclerotinia sclerotiorum: history, diseases and symptomatology, host range, geographic distribution and impact. Phytopathology 69 (1979) 875-880
60. Rodriguez M.A., Cabrera G., and Godeas A. Cyclosporine A from a nonpathogenic Fusarium oxysporum suppressing Sclerotinia sclerotiorum. Journal of Applied Microbiology 100 (2006) 575-586
61. Rollins J.A. The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulance. Molecular Plant-Microbe Interactions 16 (2003) 785-795
62. Rollins J.A., and Dickman M.B. Increase in endogenous and exogenous cyclic AMP levels inhibits development in Sclerotinia sclerotiorum. Applied and Environmental Microbiology 64 (1998) 2539-2544
63. Rollins J.A., and Dickman M.B. pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Applied and Environmental Microbiology 67 (2001) 75-81
64. Rosenberg G.B., and Pall M.L. Properties of two cyclic-nucleotide deficient mutants of Neurospora crassa. Journal of Bacteriology 137 (1979) 1140-1144
65. Rudolph E.D. The effect of some physiological and environmental factors in sclerotia aspergilli. American Journal of Botany 49 (1962) 71-78
66. Rui O., and 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. Molecular Plant Pathology 8 (2007) 173-184
67. Russo G.M., Dahlberg K.R., and Van Etten J.L. Identification of a development-specific protein in sclerotia of Sclerotinia sclerotiorum. Experimental Mycology 6 (1982) 259-262
68. Stathopoulos-Gerontides A., Guo J.J., and Cyert M.S. Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes and Development 13 (1999) 798-803
69. Steadman J.R. Control of plant disease caused by Sclerotinia species. Phytopathology 69 (1979) 904-907
70. Stork P.J., and Schmitt J.M. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends in Cell Biology 12 (2002) 258-266
71. Townsend B.B. Nutritional factors influencing the production of sclerotia by certain fungi. Annals of Botany 21 (1957) 153-166
72. Townsend B.B., and Willetts H.J. The development of sclerotia of certain fungi. Annals of Botany 21 (1954) 153-166
73. Tu J.C. An integrated control of white mold (Sclerotinia sclerotiorum) of beans, with emphasis on recent advances in biological control. Botany Bulletin of the Academia Sinica 38 (1997) 73-76
74. Tudzynski P., and Scheffer J. Claviceps purpurea: Molecular aspects of a unique pathogenic lifestyle. Molecular Plant Pathology 5 (2004) 377-388
75. Wang H.X., and Ng T.B. Isolation of pleuturegin, a novel ribosome-inactivating protein from fresh sclerotia of the edible mushroom Pleurotus tuber-regium. Biochemical and Biophysical Research Communications 288 (2001) 718-721
76. Weld R.J., Eady C.C., and Ridgway H.J. Agrobacterium-mediated transformation of Sclerotinia sclerotiorum. Journal of Microbiological Methods 65 (2006) 202-207
77. Willetts H.J., and Bullock S. Developmental biology of sclerotia. Mycological Research 96 (1992) 801-816
78. Wong A.L., and Willetts H.J. Polyacrylamide-gel electrophoresis of enzymes during morphogenesis of sclerotia of Sclerotinia-sclerotiorum. Journal of General Microbiology 81 (1974) 101-109
79. Yager L.N. Early developmental events during asexual and sexual sporulation in Aspergillus nidulans. Biotechnology 23 (1992) 19-41
80. Yatzkan E., and Yarden O. The B regulatory subunit of protein phosphatase 2A is involved in different developmental stages in Neurospora crassa. Molecular Microbiology 31 (1999) 197-210
81. Yu J.H., and Keller N. Regulation of secondary metabolism in filamentous fungi. Annual Review of Phytopathology 43 (2005) 437-458