Nitrogen fertilization of the host plant influences production and pathogenicity of Botrytis cinerea secondary inoculum

Phytopathology

Volumn 103, Issue 3, 2013, Pages 261-267

  Abro, Manzoor Ali ^a   Lecompte, François ^b   Bryone, Florian ^a   Nicot, Philippe C ^a  

^a INRA   (France)

^b Domaine Saint Paul   (France)

Author keywords

Gray mold; Solanum lycopersicum

Indexed keywords

FERTILIZER; NITRATE; NITROGEN;

ARTICLE; BIOMASS; BOTRYTIS; FUNGUS SPORE; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT STEM; TOMATO;

BIOMASS; BOTRYTIS; FERTILIZERS; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; NITRATES; NITROGEN; PLANT DISEASES; PLANT LEAVES; PLANT STEMS; SPORES, FUNGAL;

EID: 84874381944     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO-08-12-0189-R     Document Type: Article

References (60)

1. Amselem, J., Cuomo, C. A., van Kan, J. A. L., Viaud, M., Benito, E. P., Couloux, A., Coutinho, P. M., de Vries, R. P., Dyer, P. S., Fillinger, S., Fournier, E., Gout, L., Hahn, M., Kohn, L., Lapalu, N., Plummer, K. M., Pradier, J.-M., Eveline, Q., Sharon, A., Simon, A., ten Have, A., Tudzynski, B., Tudzynski, P., Wincker, P., Andrew, M., Veronique, A., Beever, R. E., Beffa, R., Benoit, I., Bouzid, O., Brault, B., Chen, Z., Choquer, M., Jerome, C., Cotton, P., Danchin, E. G., Da Silva, C., Angelique, G., Giraud, C., Giraud, T., Gonzalez, C., Grossetete, S., Ulrish, G., Henrissat, B., Howlett, B. J., Kodira, C., Kretschmer, M., Lappartient, A., Leroch, M., Levis, C., Mauceli, E., Cecile, N., Oeser, B., Pearson, M., Poulain, J., Poussereau, N., Quesneville, H., Rascle, C., Schumacher, J., Beatrice, S., Sexton, A., Silva, E., Sirven, C., Soanes, D. M., Talbot, N. J., Templeton, M., Yandava, C., Yarden, O., Zeng, Q., Rollins, J. A., Lebrun, M.-H., and Dickman, M. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLOS Genet. 7(8):e1002230. Online publication. doi:10.1371/ journal.pgen.1002230
2. Arora, D. K., Filonow, A. B., and Lockwood, J. L. 1985. Decreased aggressiveness of Bipolaris-sorokiniana conidia in response to nutrient stress. Physiol. Plant Pathol. 26:135-142.
3. Bainbridge, A. 1974. Effect of nitrogen nutrition of the host on barley powdery mildew. Plant Pathol. 23:160-161.
4. Bena-Molaei, P., Talaei-Hassanloui, R., and Askary, H. 2011. Effect of culture substrates on virulence of Beauveria bassiana (Ascomycota: Cordycipitaceae) conidia against the brown tail moth, Euproctis chrysorrhoea (Lepidoptera: Lymantriidae). Biocontrol Sci. Technol. 21:619-624.
5. Burdge, G. C., Hanson, M. A., Slater-Jefferies, J. L., and Lillycrop, K. A. 2007. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br. J. Nutr. 97:1036-1046.
6. Cliquet, S., and Jackson, M. A. 2005. Impact of carbon and nitrogen nutrition on the quality, yield and composition of blastospores of the bioinsecticidal fungus Paecilomyees fumosoroseus. J. Ind. Microbiol. Biotechnol. 32:204-210.
7. Dallemole-Giaretta, R., de Freitas, L. G., Caixeta, L. d. B., Xavier, D. M., Ferraz, S., and Silva Fabry, C. d. F. 2011. Production of chlamydospores of Pochonia chlamydosporia in different substrates. Cien. Agrotecnol. 35:314-321.
8. Decognet, V., Bardin, M., Trottin-Caudal, Y., and Nicot, P. C. 2009. Rapid change in the genetic diversity of Botrytis cinerea populations after the introduction of strains in a tomato glasshouse. Phytopathology 99:185-193.
9. De la Torre, M., and Cárdenas-Cota, H. 1996. Production of Paecilomyces Fumosoroseus conidia in submerged culture. Biocontrol 41:443-453.
10. De Vallavieille-Pope, C., Giosue, S., Munk, L., Newton, A. C., Niks, R. E., Ostergard, H., Pons-Kuhnemann, J., Rossi, V., and Sache, I. 2000. Assessment of epidemiological parameters and their use in epidemiological and forecasting models of cereal airborne diseases. Agronomie 20:715-727.
11. Dietrich, R., Ploss, K., and Heil, M. 2004. Constitutive and induced resistance to pathogens in Arabidopsis thaliana depends on nitrogen supply. Plant. Cell Environ. 27:896-906.
12. Divon, H. H., and Fluhr, R. 2007. Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol. Lett. 266:65-74.
13. Elad, Y., Williamson, B., Tudzynski, P., and Delen, N. 2004. Botrytis spp. and diseases they cause in agricultural systems - an introduction. Pages 1-24 in: Botrytis: Biology, Pathology and Control. Y. Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
14. Feil, R. 2006. Environmental and nutritional effects on the epigenetic regulation of genes. Mutat. Res./Fundam. Mol. Mech. Mutag. 600:46-57.
15. Gao, L. 2011. Optimize culture conditions for biomass and sporulation of the nematophagous fungus Pochonia chlamydosporia, isolate HSY-12-14 by "two-step" cultivation. Afr. J. Microbiol. Res. 5:4731-4738.
16. Gao, L., and Liu, X. 2010. Effects of carbon concentrations and carbon to nitrogen ratios on sporulation of two biological control fungi as determined by different culture methods. Mycopathologia 169:475-481.
17. Gao, L., Sun, M. H., Liu, X. Z., and Che, Y. S. 2007. Effects of carbon concentration and carbon to nitrogen ratio on the growth and sporulation of several biocontrol fungi. Mycol. Res. 111:87-92.
18. Gomez, L., Bancel, D., Rubio, E., and Vercambre, G. 2007. The microplate reader: an efficient tool for the separate enzymatic analysis of sugars in plant tissues - validation of a micro-method. J. Sci. Food Agric. 87:1893-1905.
19. Hallsworth, J. E., and Magan, N. 1994. Effect of carbohydrate type and concentration on polyhydroxy alcohol and trehalose content of conidia of 3 entomopathogenic fungi. Microbiology 140:2705-2713.
20. Hallsworth, J. E., and Magan, N. 1995. Manipulation of intercellular glycerol and erythritol enhances germination of conidia at lower water availability. Microbiology 141:1109-1115.
21. Hoffland, E., Jeger, M. J., and van Beusichem, M. L. 2000. Effect of nitrogen supply rate on disease resistance in tomato depends on the pathogen. Plant Soil 218:239-247.
22. Hoffland, E., van Beusichem, M. L., and Jeger, M. J. 1999. Nitrogen availability and susceptibility of tomato leaves to Botrytis cinerea. Plant Soil 210:263-272.
23. Huber, D. M. 1980. The role of mineral nutrition in defense. Pages 381-406 in: Plant Disease. An Advanced Treatise. Vol. V. How Plants Defend Themselves. J. G. Horsfall and E. B. Cowling, eds. Academic Press, New York.
24. Ibrahim, L., Butt, T. M., and Jenkinson, P. 2002. Effect of artificial culture media on germination, growth, virulence and surface properties of the entomopathogenic hyphomycete Metarhizium anisopliae. Mycol. Res. 106:705-715.
25. Jensen, B., and Munk, L. 1997. Nitrogen-induced changes in colony density and spore production of Erysiphe graminis f. sp. hordei on seedlings of six spring barley cultivars. Plant Pathol. 46:191-202.
26. Kassa, A., Brownbridge, M., Parker, B. L., Skinner, M., Gouli, V., Gouli, S., Guo, M., Lee, F., and Hata, T. 2008. Whey for mass production of Beauveria bassiana and Metarhizium anisopliae. Mycol. Res. 112:583-591.
27. Köhl, J., Molhoek, W. L., van der Plas, C. H., and Fokkema, N. J. 1995. Suppression of sporulation of Botrytis spp. as a valid biocontrol strategy. Eur. J. Plant Pathol. 101:251-259.
28. Krauss, S., Schnitzler, W. H., Grassmann, J., and Woitke, M. 2005. The Influence of different electrical conductivity values in a simplified recirculation soilless system on inner and outer fruit quality characteristics of tomato. J. Agric. Food. Chem. 54:441-448.
29. Lane, B. S., Trinci, A. P. J., and Gillespie, A. T. 1991. Endogenous reserves and survival of blastospores of Beauveria-bassiana harvested from carbon-limited and nitrogen-limited batch cultures. Mycol. Res. 95:821-828.
30. Le Bot, J., Jeannequin, B., and Fabre, R. 2001. Impacts of N-deprivation on the yield and nitrogen budget of rockwool grown tomatoes. Agronomie 21:341-350.
31. Lecompte, F., Abro, M. A., and Nicot, P. C. 2010. Contrasted responses of Botrytis cinerea isolates developing on tomato plants grown under different nitrogen nutrition regimes. Plant Pathol. 59:891-899.
32. Maas, J. L., and Powelson, R. L. 1972. Growth and sporulation of Botrytis convoluta with various carbon and nitrogen sources. Mycologia 64:897-903.
33. Meredith, D. S. 1973. Significance of spore release and dispersal mechanisms in plant disease epidemiology. Annu. Rev. Phytopathol. 11:313-342.
34. Mustafa, U., and Kaur, G. 2009. Effects of carbon and nitrogen sources and ratio on the germination, growth and sporulation characteristics of Metarhizium anisopliae and Beauveria bassiana isolates. Afr. J. Agric. Res. 4:922-930.
35. Nicot, P. C., Mermier, M., Vaissiere, B. E., and Lagier, J. 1996. Differential spore production by Botrytis cinerea on agar medium and plant tissue under near-ultraviolet light-absorbing polyethylene film. Plant Dis. 80:555-558.
36. Oneill, T. M., Shtienberg, D., and Elad, Y. 1997. Effect of some host and microclimate factors on infection of tomato stems by Botrytis cinerea. Plant Dis. 81:36-40.
37. Panepinto, J. C., Oliver, B. G., Amlung, T. W., Askew, D. S., and Rhodes, J. C. 2002. Expression of the Aspergillus fumigatus rhe b homologue, rhbA, is induced by nitrogen starvation. Fungal Genet. Biol. 36:207-214.
38. Phillips, D. J., Margosan, D. A., and Mackey, B. E. 1987. Size, nuclear number, and aggressiveness of Botrytis cinerea spore produced on media of varied glucose concentrations. Phytopathology 77:1606-1608.
39. Rangel, D. E. 2008. Stress induced cross-protection against environmental challenges on prokaryotic and eukaryotic microbes. World J. Microbiol. Biotechnol. 27:1281-1296.
40. Rangel, D. E., Alston, D. G., and Roberts, D. W. 2008. Effects of physical and nutritional stress conditions during mycelial growth on conidial germination speed, adhesion to host cuticle, and virulence of Metarhizium anisopliae, an entomopathogenic fungus. Mycol. Res. 112:1355-1361.
41. Rangel, D. E., Anderson, A. J., and Roberts, D. W. 2008. Evaluating physical and nutritional stress during mycelial growth as inducers of tolerance to heat and UV-B radiation in Metarhizium anisopliae conidia. Mycol. Res. 112:1362-1372.
42. Robert, C., Bancal, M. O., and Lannou, C. 2004. Wheat leaf rust uredospore production on adult plants: Influence of leaf nitrogen content and Septoria tritici blotch. Phytopathology 94:712-721.
43. Schisler, D. A., Jackson, M. A., and Bothast, R. J. 1991. Influence of nutrition during conidiation of Colletotrichum truncatum on conidial germination and efficacy in inciting disease in Sesbania exaltata. Phytopathology 81:458-461.
44. Shah, F. A., Wang, C. S., and Butt, T. M. 2005. Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol. Lett. 251:259-266.
45. Shtienberg, D., Elad, Y., Niv, A., Nitzani, Y., and Kirshner, B. 1998. Significance of leaf infection by Botrytis cinerea in stem rotting of tomatoes grown in non-heated greenhouses. Eur. J. Plant Pathol. 104:753-763.
46. Skromne, I., Sanchez, O., and Aguirre, J. 1995. Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. Microbiology 141:21-28.
47. Snoeijers, S. S., Perez-Garcia, A., Joosten, M., and De Wit, P. 2000. The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur. J. Plant Pathol. 106:493-506.
48. Solomon, P. S., Nielsen, P. S., Clark, A. J., and Oliver, R. P. 2000. Methionine synthase, a gene required for methionine synthesis, is expressed in planta by Cladosporium fulvum. Mol. Plant Pathol. 1:315-323.
49. Solomon, P. S., Tan, K. C., and Oliver, R. P. 2003. The nutrient supply of pathogenic fungi; a fertile field for study. Mol. Plant Pathol. 4:203-210.
50. Steyaert, J. M., Weld, R. J., and Stewart, A. 2010. Isolate-specific conidiation in Trichoderma in response to different nitrogen sources. Fungal Biol. 114:179-188.
51. Stout, M. J., Brovont, R. A., and Duffey, S. S. 1998. Effect of nitrogen availability on expression of constitutive and inducible chemical defenses in tomato, Lycopersicon esculentum. J. Chem. Ecol. 24:945-963.
52. Verhoeff, K. 1968. Studies on Botrytis cinerea in tomatoes. Effect of soil nitrogen level and of methods of deleafing upon the occurrence of B. cinerea under commercial conditions. Eur. J. Plant Pathol. 74:184-192.
53. Williamson, B., Tudzynski, B., Tudzynski, P., and van Kan, J. 2007. Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol. 8:561-580.
54. Winder, R. S. 1999. The influence of substrate and temperature on the sporulation of Fusarium avenaceum and its virulence on marsh reed grass. Mycol. Res. 103:1145-1151.
55. Yermiyahu, U., Shamai, I., Peleg, R., Dudai, N., and Shtienberg, D. 2006. Reduction of Botrytis cinerea sporulation in sweet basil by altering the concentrations of nitrogen and calcium in the irrigation solution. Plant Pathol. 55:544-552.
56. Ypsilos, I. K., and Magan, N. 2005. Characterization of optimum cultural environmental conditions for the production of high numbers of Metarhizium anisopliae blastospores with enhanced ecological fitness. Biocontrol. Sci. Technol. 15:683-699.
57. Zar, J. H. 1984. Biostatistical Analysis. Prentice Hall, Englewood Cliffs, NJ.
58. Zarzycka, H. 1995. Effect of culturing Phytophthora infestans on various substrates on expression of its virulence and aggressiveness to potato. Phytopathol. Pol. 9(XXI):81-88.
59. Zeisel, S. H. 2009. Epigenetic mechanisms for nutrition determinants of later health outcomes. Am. J. Clin. Nutr. 89:S1488-S1493.
60. Zhao, S., and Shamoun, S. F. 2006. The effects of culture media, solid substrates, and relative humidity on growth, sporulation and conidial discharge of Valdensinia heterodoxa. Mycol. Res. 110:1340-1346.