Factors governing the regulation of Sclerotinia sclerotiorum cutinase a and polygalacturonase 1 during different stages of infection

Canadian Journal of Microbiology

Volumn 58, Issue 5, 2012, Pages 605-616

  Bashi, Zafer Dallal ^a,b   Roger Rimmer, S ^a   Khachatourians, George G ^b   Hegedus, Dwayne D ^a,b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Calcium signalling; cAMP; Cutinase; Polygalacturonase; Sclerotinia sclerotiorum; Virulence

Indexed keywords

CUTINASE; CYCLIC AMP; GALACTURONIC ACID; GLUCOSE; HYDROLASE; POLYGALACTURONASE;

CALCIUM; CUTICLE; ENZYME ACTIVITY; FUNGUS; GENE EXPRESSION; HYDROLYSIS; INOCULATION; LESION; STARVATION; VIRULENCE; WAX;

ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; IN VITRO STUDY; INOCULATION; MYCELIUM; MYCOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT LEAF; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCLEROTINIA SCLEROTIORUM; STARVATION; VIRULENCE;

AMINO ACID SEQUENCE; ASCOMYCOTA; CALCIUM SIGNALING; CARBOXYLIC ESTER HYDROLASES; CYCLIC AMP; FUNGAL PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; HEXURONIC ACIDS; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT LEAVES; POLYGALACTURONASE;

SCLEROTINIA SCLEROTIORUM;

EID: 84860465556     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/W2012-031     Document Type: Article

References (55)

1. Abawi, G.S., and Grogan, R.G. 1979. Epidemiology of diseases caused by Sclerotionia species. Phytopathology, 69(8): 899-904. doi:10.1094/Phyto-69-899.
2. Baker, E.A. 1982. Chemistry and morphology of plant epicuticular waxes. In The plant cuticle. Edited by D.F. Cutler, K.L. Alvin, and C.E. Price. Academic Press, London, UK. pp. 139-165.
3. Baker, C.J., and Bateman, D.F. 1978. Cutin degradation by plant pathogenic fungi. Phytopathology, 68(11): 1577-1584. doi:10.1094/Phyto-68-1577.
4. Berridge, M.J. 1997. Elementary and global aspects of calcium signaling. J. Physiol. 499(2): 291-306.
5. Boland, G.J., and Hall, R. 1994. Index of plant hosts of Sclerotinia sclerotiorum. Can. J. Plant Pathol. 16(2): 93-108. doi:10.1080/07060669409500766.
6. Bolton, M.D., Thomma, B., and Nelson, B.D. 2006. Sclerotinia sclerotiorum (Lib.) de Bary; biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 7(1): 1-16. doi:10.1111/j.1364-3703.2005.00316.x.
7. Carpita, N.C., and Gibeaut, D.M. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3 (1): 1-30. doi:10.1111/j.1365-313X.1993.tb00007.x.
8. Chaky, J., Anderson, K., Moss, M., and Vaillancourt, L. 2001. Surface hydrophobicity and surface rigidity induce spore germination in Colletotrichum graminicola. Phytopathology, 91(6): 558-564. doi:10.1094/PHYTO.2001.91.6.558.
9. Chen, C., and Dickman, M.B. 2005. cAMP blocks MAPK activation and sclerotial development via Rap-1 in a PKA-independent manner in Sclerotinia sclerotiorum. Mol. Microbiol. 55(1): 299-311. doi:10.1111/j.1365-2958.2004.04390.x.
10. Chen, C., Harel, A., Gorovoits, R., Yarden, O., and Dickman, M.B. 2004. MAPK regulation of sclerotial development in Sclerotinia sclerotiorum is linked with pH and cAMP sensing. Mol. Plant-Microbe Interact. 17(4): 404-413. doi:10.1094/MPMI.2004.17.4.404.
11. Coleman, M., Henricot, B., Arnau, J., and Oliver, R.P. 1997. Starvation-induced genes of the tomato pathogen Cladosporium fulvum are also induced during growth in planta. Mol. Plant-Microbe Interact. 10(9): 1106-1109. doi:10.1094/MPMI.1997.10.9.1106.
12. Collmer, A., and Keen, N.T. 1986. The role of pectic enzymes in plant pathogenesis. Annu. Rev. Phytopathol. 24(1): 383-409. doi:10.1146/annurev.py.24.090186.002123.
13. Comménil, P., Belingheri, L., and Dehorter, B. 1998. Antilipase antibodies prevent infection of tomato leaves by Botrytis cinerea. Physiol. Mol. Plant Pathol. 52(1): 1-14. doi:10.1006/pmpp.1997.0130.
14. Cotton, P., Rascle, C., and Fevre, M. 2002. Characterization of PG2, an early endoPG produced by Sclerotinia sclerotiorum, expressed in yeast. FEMS Microbiol. Lett. 213(2): 239-244. doi:10.1111/j.1574-6968.2002.tb11312.x.
15. Cotton, P., Kasza, Z., Bruel, C., Rascle, C., and Fèvre, M. 2003. Ambient pH controls the expression of endopolygalacturonase genes in the necrotrophic fungus Sclerotinia sclerotiorum. FEMS Microbiol. Lett. 227(2): 163-169. doi:10.1016/S0378-1097(03)00582-2.
16. Dallal Bashi, Z., Hegedus, D.D., Buchwaldt, L., Rimmer, R., and Borhan, M.H. 2010. Expression and regulation of Sclerotinia sclerotiorum necrosis and ethylene-inducing peptides (NEPs). Mol. Plant Pathol. 11(1): 43-53. doi:10.1111/j.1364-3703.2009.00571.x.
17. Darvill, A.G., McNeil, M., and Albersheim, P. 1978. Structure of plant cell walls. A new pectic polysaccharide. Plant Physiol. 62(3): 418-422. doi:10.1104/pp.62.3.418.
18. Dickman, M., Podila, G., and Kolattukudy, P. 1989. Insertion of cutinase gene into a wound pathogen enables it to infect intact host. Nature, 342(6248): 446-448. doi:10.1038/342446a0.
19. Doehlemann, G., Berndt, P., and Hahn, M. 2006. Different signalling pathways involving a Ga protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol. Microbiol. 59(3): 821-835. doi:10.1111/j.1365-2958.2005.04991.x.
20. D'Souza, C.A., and Heitman, J. 2001. Conserved cAMP signalling cascades regulate fungal development and virulence. FEMS Microbiol. Rev. 25(3): 349-364. doi:10.1111/j.1574-6976.2001.tb00582.x.
21. Fox, D.S., and Heitman, J. 2002. Good fungi gone bad: the corruption of calcineurin. Bioessays, 24(10): 894-903. doi:10.1002/bies.10157.
22. Fraissinet-Tachet, L., and Fevre, M. 1996. Regulation by galacturonic acid of pectinolytic enzyme production by Sclerotinia sclerotiorum. Curr. Microbiol. 33(1): 49-53. doi:10.1007/s002849900073.
23. Fraissinet-Tachet, L., Reymond-Cotton, P., and Fèvre, M. 1995. Characterization of a multigene family encoding an endopolygalacturonase in Sclerotinia sclerotiorum. Curr. Genet. 29(1): 96-99. doi:10.1007/BF00313199.
24. Godoy, G., Steadman, J., Dickman, M., and Dam, R. 1990. Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol. Mol. Plant Pathol. 37(3): 179-191. doi:10.1016/0885-5765(90)90010-U.
25. Harel, A., Bercovich, S., and Yarden, O. 2006. Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid independent manner. Mol. Plant-Microbe Interact. 19(6): 682-693. doi:10.1094/MPMI-19-0682.
26. Jarvis, M. 1984. Structure and properties of pectin gels in plant cell walls. Plant Cell Environ. 7: 153-164.
27. Jetter, R., Schaffer, S., and Riederer, M. 2000. Leaf cuticular waxes are arranged in chemically and mechanically distinct layers: evidence from Prunus laurocerasus L. Plant Cell Environ. 23(6): 619-628. doi:10.1046/j.1365-3040.2000.00581.x.
28. Joubert, D.A., Kars, I., Wagemakers, L., Bergmann, C., Kemp, G., Vivier, M.A., and van Kan, J.A.L. 2007. A polygalacturonaseinhibiting protein from grapevine reduces the symptoms of the endopolygalacturonse BcPg2 from Botrytis cinerea in Nicotiana benthamiana leaves without any evidence for in vitro interaction. Mol. Plant-Microbe Interact. 20(4): 392-402. doi:10.1094/MPMI-20-4-0392.
29. Jurick, W.M., II, and Rollins, J.A. 2007. Deletion of the adenylate cyclase (sac1) gene affects multiple developmental pathways and pathogenicity in Sclerotinia sclerotiorum. Fungal Genet. Biol. 44(6): 521-530. doi:10.1016/j.fgb.2006.11.005.
30. Kasza, Z., Vagvölgyi, C., Fèvre, M., and Cotton, P. 2004. Molecular characterization and in planta detection of Sclerotinia sclerotiorum endopolygalacturonase genes. Curr. Microbiol. 48(3): 208-213. doi:10.1007/s00284-003-4166-6.
31. 2+-calmodulin signaling by hard-surface contact primes Colletotrichum gloeosporioides conidia to germinate and form appressoria. J. Bacteriol. 180(19): 5144-5150.
32. Kim, Y.T., Prusky, D., and Rollins, J. 2007. An activating mutation of the Sclerotinia sclerotiorum pac1 gene increases oxalic acid production at low pH but decreases virulence. Mol. Plant Pathol. 8(5): 611-622. doi:10.1111/j.1364-3703.2007.00423.x.
33. Lau, J., McNeil, M., Darvill, A., and Albersheim, P. 1985. Structure of the backbone of rhamnogalacturonan I, a pectic polysaccharide in the primary walls of plants. Carbohydr. Res. 137: 111-125. doi:10.1016/0008-6215(85)85153-3.
34. Li, D., Sirakova, T., Rogers, L., Ettinger, W.F., and Kolattukudy, P.E. 2002. Regulation of constitutively expressed and induced cutinase genes by different zinc finger transcription factors in Fusarium solani f. sp. pisi (Nectria haematococca). J. Biol. Chem. 277(10): 7905-7912. doi:10.1074/jbc.M108799200.
35. Li, R., Rimmer, R., Buchwaldt, L., Sharpe, A., Seguin-Swartz, G., and Hegedus, D. 2004. Interaction of Sclerotinia sclerotiorum with Brassica napus: cloning and characterization of endo-and exopolygalacturonases expressed during saprophytic and parasitic modes. Fungal Genet. Biol. 41(8): 754-765. doi:10.1016/j.fgb.2004.03.002.
36. Mogami, H., Lloyd Mills, C., and Gallacher, D. 1997. Phospholipase C inhibitor, U73122, releases intracellular Ca2+, potentiates Ins (1,4,5)P3-mediated Ca2+ release and directly activates ion channels in mouse pancreatic acinar cells. Biochem. J. 324(2): 645-651.
37. Morid, B., Zare, R., Rezaee, S., Zamani-Zadeh, H., and Hajmansour, S. 2009. The relationship between cutinases and the pathogenicity/virulence of Fusarium solani in potato tubers. Phytopathol. Mediterr. 48: 403-410.
38. Pascholati, S., Yoshioka, H., Kunoh, H., and Nicholson, R. 1992. Preparation of the infection court by Erysiphe graminis f. sp. hordei: cutinase is a component of the conidial exudates. Physiol. Mol. Plant Pathol. 41(1): 53-59. doi:10.1016/0885-5765(92)90048-Z.
39. Pascholati, S., Deising, L., Leiti, B., Anderson, D., and Nicholson, R. 1993. Cutinase and non specific esterase activities in the conidial mucilage of Colletotrichum graminicola. Physiol. Mol. Plant Pathol. 42(1): 37-51. doi:10.1006/pmpp.1993.1004.
40. Purdy, S.J., and Truter, E.V. 1963. Constitution of the surface lipid from the leaves of Brassica oleracea (var. capitata (Winnigstadt)). I. Isolation and quantitative fractionation. Proc. R. Soc. Biol. Sci. Ser. B, 158: 536-543. doi:10.1098/rspb.1963.0062.
41. Reis, H., Pfiffi, S., and Hahn, M. 2005. Molecular and functional characterization of a secreted lipase from Botrytis cinerea. Mol. Plant Pathol. 6(3): 257-267. doi:10.1111/j.1364-3703.2005.00280.x.
42. Reymond-Cotton, P., Fraissinet-Tachet, L., and Fèvre, M. 1996. Expression of the Sclerotinia sclerotiorum polygalacturonase pg1 gene: possible involvement of CREA in glucose catabolite repression. Curr. Genet. 30(3): 240-245. doi:10.1007/s002940050127.
43. Riou, C., Freyssinet, G., and Fevre, M. 1992. Purification and characterization of extracellular pectinolytic enzymes produced by Sclerotinia sclerotiorum. Appl. Environ. Microbiol. 58(2): 578-583.
44. Rollins, J.A. 2003. The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol. Plant-Microbe Interact. 16(9): 785-795. doi:10.1094/MPMI.2003.16.9.785.
45. Rollins, J.A., and Dickman, M. 1998. Increase in endogenous and exogenous cyclic AMP levels inhibits sclerotial development in Sclerotinia sclerotiorum. Appl. Environ. Microbiol. 64(7): 2539-2544.
46. Schumacher, J., Viaud, M., Simon, A., and Tudzynski, B. 2008. The Ga subunit BCG1, the phospholipase C (BcPLC1) and the calcineurin phosphatase co-ordinately regulate gene expression in the grey mould fungus Botrytis cinerea. Mol. Microbiol. 67(5): 1027-1050. doi:10.1111/j.1365-2958.2008.06105.x.
47. Sella, L., Tomassini, A., D'Ovidio, R., and Favaron, F. 2005. Expression of two Sclerotinia sclerotiorum endo-PG genes correlates with endo-polygalacturonase activity during Glycine max colonization. J. Plant Pathol. 87: 199-205.
48. Skamnioti, P., and Gurr, S. 2007. Magnaporthe grisea cutinase 2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell, 19(8): 2674-2689. doi:10.1105/tpc.107.051219.
49. Tariq, V., and Jeffries, P. 1987. Cytochemical localization of lipolytic enzyme activity during penetration of host tissues by Sclerotinia sclerotiorum. Physiol. Mol. Plant Pathol. 30(1): 77-91. doi:10.1016/0885-5765(87)90084-1.
50. ten Have, A., Mulder, W., Visser, J., and van Kan, J.A.L. 1998. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol. Plant-Microbe Interact. 11(10): 1009-1016. doi:10.1094/MPMI.1998.11.10.1009.
51. Van den Ackerveken, G.F.J.M., Dunn, R.M., Cozijnsen, A.J., Vossen, J.P.M.J., Van den Broek, H.W.J., and De Wit, P.J.G.M. 1994. Nitrogen limitation induces expression of the avirulence gene avr9 in the tomato pathogen Cladosporium fulvum. Mol. Gen. Genet. 243(3): 277-285. doi:10.1007/BF00301063.
52. van der Vlugt-Bergmans, C.J.B., Wagemakers, C.A.M., and van Kan, J.A.L. 1997. Cloning and expression of the cutinase A gene of Botrytis cinerea. Mol. Plant-Microbe Interact. 10(1): 21-29.
53. van Kan, J.A.L., van't Klooster, J.W., Wagemakers, C.A.M., Dees, D. C.T., and van der Vlugt-Bergmans, C.J.B. 1997. Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol. Plant-Microbe Interact. 10(1): 30-38. doi:10.1094/MPMI.1997.10.1.30.
54. Viaud, M., Brunet-Simon, A., Brygoo, Y., Pradier, J., and Levis, C. 2003. Cyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporin A inhibition and cDNA array approaches in the phytopathogenic fungus Botrytis cinerea. Mol. Microbiol. 50(5): 1451-1465. doi:10.1046/j.1365-2958.2003.03798.x.
55. Wubben, J.P., ten Have, A., van Kan, J.A.L., and Visser, J. 2000. Regulation of endopolygalacturonase gene expression in Botrytis cinerea by galacturonic acid, ambient pH and carbon catabolite repression. Curr. Genet. 37(2): 152-157. doi:10.1007/s002940050022.