Penicillium digitatum suppresses production of hydrogen peroxide in host tissue during infection of citrus fruit

Phytopathology

Volumn 97, Issue 11, 2007, Pages 1491-1500

  Macarisin, D ^a   Cohen, L ^b   Eick, A ^b   Rafael, G ^b   Belausov, E ^b   Wisniewski, M ^a   Droby, S ^b  

^a APPALACHIAN FRUIT RESEARCH STATION   (United States)

^b VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CITRUS; PENICILLIUM DIGITATUM; PENICILLIUM EXPANSUM;

EID: 36048935285     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-97-11-1491     Document Type: Article

References (59)

1. Afek, U., Orenstein, J., Carmeli, S., Rodov, V., and Bar Joseph, M. 1999. Umbelliferone, a phytoalexin associated with resistance of immature Marsh grapefruit to Penicillium digitatum. Phytochemistry 50:1129-1132.
2. Allan, A., and Fluhr, R. 1997. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559-1572.
3. Ballester, A., Lafuente, M., and González-Candelas, L. 2006. Spatial study of antioxidant enzymes, peroxidase and phenylalanine ammonialyase in the citrus fruit-Penicillium digitatum interaction. Postharvest Bio. Tech. 39:115-124.
4. Bateman, D., and Beer, S. 1965. Simultaneous production and synergistic action of oxalic acid and polygalacturonase during pathogenesis by Sclerotiorum rolfsii. Phytopathology 55:204-211.
5. Beno-Moualem, D., and Prusky, D. 2000. Early events during quiescent infection development by Colletotrichum gloeosporioides in unripe avocado fruits. Phytopathology 90:553-559.
6. Bindschedler, L., Dewdney, J., Blee, K., Stone, J., Asai, T., Plotnikov, J., Denoux, C., Hayes, T., Gerrish, C., Davies, D., Ausubel, F., and Bolwell, G. 2006. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47:851-863.
7. Borden, S., and Higgins, V. 2002. Hydrogen peroxide plays a critical role in the defense response of tomato to Cladosporium fulvum. Physiol. Mol. Plant Pathol. 61:227-236.
8. Brisson, L. F., Tenhaken, R., and Lamb, C. 1994. Function of oxidative crosslinking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703-1712.
9. Bussink, H., Oliver, R. 2001. Identification of two highly divergent catalase genes in the fungal tomato pathogen, Cladosporium fulvum. Eur. J. Biochem. 268:15-24.
10. Castoria, R., Caputo, L., De Curtis, F., and De Cicco, V. 2003. Resistance of postharvest biocontrol yeasts to oxidative stress: A possible new mechanism of action. Phytopathology 93:564-572.
11. Cessna, S., Sears, V., Dickman, M., and Low, P. 2000. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12:2191-2199.
12. Chaga, G. S., Medin, A. S., Chaga, S. G., and Porath, J. O. 1992. Isolation and characterization of catalase from Penicillium chrysogenum. J. Chromatogr. 604:177-183.
13. Chien, P., Sheu, F., and Lin, H. 2007. Coating citrus (Murcott tangor) fruit with low molecular weight chitosan increases postharvest quality and shelf life. Food Chem. 100:1160-1164.
14. Davies, D., Bindschedler, L., Strickland, T., and Bolwell, G. 2006. Production of reactive oxygen species in Arabidopsis thaliana cell suspension cultures in response to an elicitor from Fusarium oxysporum: Implications for basal resistance. J. Exp. Bot. 57:1817-1827.
15. De Gara, L., De Pinto, C., Tommasi, F. 2003. The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol. Biochem. 41:863-870.
16. Droby, S., Cohen, L., Daus, A., Weiss, B., Horev, B., Chalutz, E., Katz, H., Keren-Tzur, M., and Shachnai, A. 1998. Commercial testing of aspire: A yeast preparation for the biological control of postharvest decay of citrus. Biol. Control 12:97-101.
17. Droby, S., Lischinski, S., Cohen, L., Weiss, B., Daus, A., Chand-Goyal, T., Eckert, J., and Manulis, S. 1999. Characterization of an epiphytic yeast population of grapefruit capable of suppression of green mold decay caused by Penicillium digitatum. Biol. Control 16:27-34.
18. Duccio, R., Caccioni, L., Guizzardi, M., Biondi, D., Renda, A., and Ruberto, G. 1998. Relationship between volatile components of citrus fruit essential oils and antimicrobial action on Penicillium digitatum and Penicillium italicum. Int. J. Food Microbiol. 43:73-79.
19. Dutton, M., and Evans, C. 1996. Oxalate production by fungi: Its role in pathogenicity and ecology in the soil environment. Can. J. Microbiol. 42:881-895.
20. El-Ghaouth, A., Smilanick, J., and Wilson, C. 2000. Enhancement of the performance of Candida saitoana by the addition of glycolchitosan for the control of postharvest decay of apple and citrus fruit. Postharvest Biol. Technol. 19:103-110.
21. Fajardo, J., McCollum, T., McDonald, R., and Mayer, R. 1998. Differential induction of proteins in orange flavedo by biologically based elicitors and challenged by Penicillium digitatum Sacc.1. Biol. Control 13:143-151.
22. Garre, V., Tenberge, B., and Eising, R. 1998. Secretion of a fungal extracellular catalase by Claviceps purpurea during infection of rye: Putative role in pathogenicity and suppression of host defense. Phytopathology 88:744-753.
23. Godoy, G., Steadman, R., Dickman, B., 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. 37:179-191.
24. Grant, J., and Loake, G. 2000. Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol. 124:21-30.
25. Hadas, Y., Goldberg, I., Pines, O., and Prusky, D. 2007. Involvement of gluconic acid and glucose oxidase in the pathogenicity of Penicillium expansum in apples. Phytopathology 97:384-390.
26. Hasdai, M., Elmaci, C., Goldschmidt, E., Droby, S., and Porat, R. 2004. Isolation of a thioredoxin h cDNA from grapefruit peel tissue that is induced upon infection by Penicillium digitatum and elicitation of pathogen resistance. Physiol. Mol. Plant Pathol. 65:277-283.
27. Hückelhoven, R., Dechert, C., and Kogel, K. 2001. Non-host resistance of barley is associated with a hydrogen peroxide burst at sites of attempted penetration by wheat powdery mildew fungus. Mol. Plant Pathol. 2:199-205.
28. Ismail, M. A., and Brown, G. E. 1979. Postharvest wound healing in citrus fruit: Induction of PAL in injured Valencia orange flavedo. J. Am. Soc. Hort. 104:126-129.
29. Lamb, C., and Dixon, R. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
30. Leangon, S., Maddox, I., and Brooks, J. 2000. A proposed biochemical mechanism for citric acid accumulation by Aspergillus niger Yang No. 2 growing in solid state fermentation. World J. Microbiol. Biotech. 16:271-275.
31. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
32. 2 accumulation in compatible and incompatible wheat-powdery mildew interactions. Plant Pathol. 54:308-316.
33. Lisker, N., Cohen, L., Chalutz, E., and Fuchs, Y. 1983. Fungal infections suppress ethylene induced phenylalanine ammonia-lyase activity in grapefruits. Physiol. Plant Pathol. 22:331-338.
34. Low, S., and Merida, R. 1996. The oxidative burst in plant defense: Function and signal transduction. Physiol. Plantarum 96:533-542.
35. Lu, H., and Higgins, J. 1999. The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum. Physiol. Mol. Plant Pathol. 54:131-143.
36. Marcos, J, Gonzalez-Candelas, L., and Zacarias, L. 2005. Involvement of ethylene biosynthesis and perception in the susceptibility of citrus fruits to Penicillium digitatum infection and accumulation of defense-related mRNAs. J. Exp. Bot. 56:2183-2193.
37. 2 plays different roles in determining penetration in three diverse plant-fungal interactions. Plant J. 29:257-268.
38. Noyes, R. D., and Hancock, J. G. 1981. Role of oxalic acid in the Sclerotinia wilt of sunflower. Physiol. Plant Pathol. 18:123-132.
39. Olson, P., and Varner, J. 1993. Hydrogen peroxide and lignification. Plant J. 4:887-892.
40. Ortuño, A., Báidez, A., Gómez, P., Arcas, M., Porras, I., García-Lidón, A., and Del Río, J. 2006. Citrus paradisi and Citrus sinensis flavonoids: Their influence in the defense mechanism against Penicillium digitatum. Food Chem. 98:351-358.
41. Porat, R., Vinokur, V., Weiss, B., Cohen, L., Daus, A., Goldschmidt, E., and Droby, S. 2003. Induction of resistance to Penicillium digitatum in grapefruit by β-aminobutyric acid. Eur. J. Plant Pathol. 109:901-907.
42. Prusky, D., McEvoy, J., Saftner, R., Conway, S., Jones, R. 2004. The relationship between host acidification and virulence of Penicillium spp. on apple and citrus fruit. Phytopathology 94:44-51.
43. Prusky, D., and Yakoby, N. 2003. Pathogenic fungi: Leading or led by ambient pH? Mol. Plant Pathol. 4:509-516.
44. Scora, M., and Scora, R. 1998. Effect of volatiles on mycelium growth of Penicillium digitatum, P. italicum, and P. ulaiense. J. Basic Microbiol. 38:405-413.
45. Snowdon, A. 1990. Chapter 2. Citrus fruits. Page 59 in: A Color Atlas of Post-Harvest Diseases and Disorders of Fruits and Vegetables. Vol. 1. CRC Press, Boca Raton, FL.
46. Stange, R., Midland, S., Sims, J., and McCollum, T. 2002. Differential effects of citrus peel extracts on growth of Penicillium digitatum, P. italicum, and P. expansum. Physiol. Mol. Plant Pathol. 61:303-311.
47. Stevens, C., Khan, V., Lu, J., Wilson, C., Pusey, P., Igwegbe, E., Kabwe, K., Mafolo, Y., Liu, J., Chalutz, E., and Droby, S. 1997. Integration of ultraviolet (UV-C) light with yeast treatment for control of postharvest storage rots of fruits and vegetables. Biol. Control 10:98-103.
48. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-1194.
49. Tomankova, K., Luhova, L., Petrivalsky, M., Pec, P., and Lebeda, A. 2006. Biochemical aspects of reactive oxygen species formation in the interaction between Lycopersicon spp. and Oidium neolycopersici. Physiol. Mol. Plant Pathol. 68:22-32.
50. Torres, R., Valentines, M., Usall, J., Vinas, I., and Larrigaudiere, C. 2003. Possible involvement of hydrogen peroxide in the development of resistance mechanisms in 'Golden Delicious' apple fruit. Postharvest Biol. Technol. 27:235-242.
51. Unger, Ch., Kleta, S., Jandl, G., and Tiedemann, A. 2005. Suppression of the defense-related oxidative burst in bean leaf tissue and bean suspension cells by the necrotrophic pathogen Botrytis cinerea. J. Phytopathol. 153:15-26.
52. 2 accumulation in mesophyll cells leads to induction of glutathione during the hypersensitive response in the barley-powdery mildew interaction. Plant Physiol. 123:1289-1300.
53. Venditti, T., Molinu, M., Dore, A., Agabbio, M., and D'Hallewin, G. 2005. Sodium carbonate treatment induces scoparone accumulation, structural changes, and alkalinization in the albedo of wounded citrus fruits. J. Agric. Food Chem. 53:3510-3518.
54. Wilson, T., DeLisle, G., and Collins, D. 1995. Effect of inhA and katG on isoniazid resistance and virulence of Mycobacterium bovis. Mol. Microbiol. 15:1009-1015.
55. Wojtaszek, P. 1997. Oxidative burst: An early plant response to pathogen infection. Biochem. J. 322:681-692.
56. Wysong, D. R., Christin, L., Sugar, A. M., Robbins, P. W., and Diamond, R. D. 1998. Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect. Immune. 66:1953-1961.
57. Xu, X. Q., and Pan, S. Q. 2000. An Agrobacterium catalase is a virulence factor involved in tumorigenesis. Mol. Microbiol. 35:407-414.
58. Zhang, Z., Henderson, C., and Gurr, S. 2004. Blumeria graminis secretes an extracellular catalase during infection of barley: Potential role in suppression of host defense. Mol. Plant Pathol. 5:537-547.
59. Zhou, T., and Boland, J. 1999. Mycelial growth and production of oxalic acid by virulent and hypovirulent isolates of Sclerotinia sclerotiorum. Can. J. Plant Pathol. 21:93-99.