Expression of an oxalate decarboxylase impairs the necrotic effect induced by Nep1-like protein (NLP) of Moniliophthora perniciosa in transgenic tobacco

Molecular Plant-Microbe Interactions

Volumn 24, Issue 7, 2011, Pages 839-848

  Da Silva, Leonardo F ^a   Dias, Cristiano V ^a   Cidade, Luciana C ^a   Mendes, Juliano S ^a   Pirovani, Carlos P ^a   Alvim, Fátima C ^a   Pereira, Gonçalo A G ^b   Aragão, Francisco J L ^c   Cascardo, Júlio C M ^a   Costa, Marcio G C ^a  

^a DEPARTAMENTO DE CIÊNCIAS BIOLÓGICAS   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLYASE; FORMIC ACID; FORMIC ACID DERIVATIVE; OXALATE DECARBOXYLASE; OXALIC ACID; REACTIVE OXYGEN METABOLITE;

AGARICALES; ARTICLE; BIOSYNTHESIS; CELL DEATH; ENZYMOLOGY; FLAMMULINA; GENETICS; METABOLISM; MICROBIOLOGY; NECROSIS; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOBACCO; TRANSGENIC PLANT;

AGARICALES; CARBOXY-LYASES; CELL DEATH; FLAMMULINA; FORMIC ACIDS; NECROSIS; OXALIC ACID; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TOBACCO;

BASIDIOMYCOTA; FLAMMULINA VELUTIPES; FUNGI; MONILIOPHTHORA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; THEOBROMA CACAO;

EID: 79959339943     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-12-10-0286     Document Type: Article

References (55)

1. Aguilar, C., Urzúa, U., Koenig, C., and Vicuña, R. 1999. Oxalate oxidase from Ceriporiopsis subvermispora: Biochemical and cytochemical studies. Arch. Biochem. Biophys. 366:275-282. (Pubitemid 29394220)
2. Alvim, F. C., Carolino, S. M. B., Cascardo, J. C. M., Nunes, C. C., Martinez, C. A., Otoni, W. C., and Fontes, E. P. B. 2001. Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol. 126:1042-1054. (Pubitemid 32656792)
3. Amsellem, Z., Cohen, B. A., and Gressel, J. 2002. Engineering hypovirulence in a mycoherbicidal fungus for efficient weed control. Nat. Biotechnol. 20:1035-1039.
4. Bae, H., Moon, S. K., Richard, C. S., Bae, H.-J., and Bailey, B. 2006. Necrosis and ethylene inducing peptide from Fusarium oxysporum induces a complex cascade of transcripts associated with signal transduction and cell death in Arabidopsis. Plant Physiol. 141:1056-1067. (Pubitemid 44061611)
5. Bailey, B. A. 1995. Purification of a protein from culture filtrate of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology 85:1250-1255. (Pubitemid 3002252)
6. Bashi, Z. D., Hegedus, D. D., Buchwaldt, L., Rimmer, S. R., and Borhan, M. H. 2010. Expression and regulation of Sclerotinia sclerotiorum necrosis and ethylene-inducing peptides (NEPs). Mol. Plant Pathol. 11:43-53.
7. Bateman, D. F., and Beer, S. V. 1965. Simultaneous production and synergistic action of oxalic acid and polygalacturonase during pathogenesis by Sclerotiorum rolfsii. Phytopathology 55:204-211.
8. Berna, A., and Bernier, F. 1997. Regulated expression of a wheat germin gene in tobacco: Oxalate oxidase activity and apoplastic localization of the heterologous protein. Plant Mol. Biol. 33:417-429. (Pubitemid 27115274)
9. Ceita, G. O., Macêdo, J. N. A., Santos, T. B., Alemanno, L., Gesteira, A. S., Micheli, F., Mariano, A. C., Gramacho, K. P., Silva, D. C., Meinhardt, L. W., Mazzafera, P., Pereira, G. A. G., and Cascardo, J. C. M. 2007. Involvement of calcium oxalate degradation during programmed cell death in Theobroma cacao tissues triggered by the hemibiotrophic fungus Moniliophthora perniciosa. Plant Sci. 173:106-117. (Pubitemid 46992841)
10. Cessna, S. G., Sears, V. E., Dickman, M. B., and Low, P. S. 2000. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12:2191-2200.
11. Choquer, M., Fournier, E., Kunz, C., Levis, C., Pradier, J.-M., Simon, A., and Viaud, M. 2007. Botrytis cinerea virulence factors: New insights into a necrotrophic and polyphageous pathogen. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 277:1-10. (Pubitemid 350045656)
12. Cunha, W. G., Tinoco, M. L. P., Pancoti, H. L., Ribeiro, R. E., and Aragão, F. J. L. 2010. High resistance to Sclerotinia sclerotiorum in transgenic soybean plants transformed to express an oxalate decarboxylase gene. Plant Pathol. 59:654-660.
13. Davidson, R. M., Reeves, P. A., Manosalva, P. M., and Leach, J. E. 2009. Germins: A diverse protein family important for crop improvement. Plant Sci. 177:499-510.
14. Dias, B. B. A., Cunha, W. G., Morais, L. S., Vianna, G. R., Rech, E. L., Capdeville, G. de, and Aragão, F. J. L. 2006. Expression of an oxalate decarboxylase gene from Flammulina sp. in transgenic lettuce (Lactuca sativa) plants and resistance to Sclerotinia sclerotiorum. Plant Pathol. 55:187-193.
15. Donaldson, P. A., Anderson, T., Lane, B. G., Davidson, A. L., and Simmonds, D. H. 2001. Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiol. Mol. Plant Pathol. 59:297-307. (Pubitemid 34190693)
16. Dong, X., Ji, R., Guo, X., Foster, S. J., Chen, H., Dong, C., Liu, Y., Hu, Q., and Liu, S. 2008. Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Planta 228:331-340.
17. Doyle, J. J., and Doyle, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19:11-15.
18. Dunwell, J. M., Gibbings, J. G., Mahmood, T., and Naqvi, S. M. S. 2008. Germin and germin-like proteins: Evolution, structure, and function. Crit. Rev. Plant Sci. 27:342-375.
19. Escutia, M. R., Bowater, L., Edwards, A., Bottrill, A. R., Burrell, M. R., Polanco, R., Vicuña, R., and Bornemann, S. 2005. Cloning and sequencing of two Ceriporiopsis subvermispora bicupin oxalate oxidase allelic isoforms: Implications for the reaction specificity of oxalate oxidases and decarboxylases. Appl. Environ. Microbiol. 71:3608-3616. (Pubitemid 40980527)
20. Fellbrich, G., Romanski, A., Varet, A., Blume, B., Brunner, F., Enelhardt, S., Felix, G., Kemmerling, B., Krzymowska, M., and Nurnberger, T. 2002. NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J. 32:375-390. (Pubitemid 35307270)
21. Garcia, O., Macedo, J. A., Tiburcio, R., Zaparoli, G., Rincones, J., Bittencourt, L. M., Ceita, G. O., Micheli, F., Gesteira, A., Mariano, A. C., Schiavinato, M. A., Medrano, F. J., Meinhardt, L. W., Pereira, G. A. G., and Cascardo, J. C. M. 2007. Characterization of necrosis and ethylene-inducing proteins (NEP) in the basidiomycete Moniliophthora perniciosa, the causal agent of witches' broom in Theobroma cacao. Mycol. Res. 111:443-455. (Pubitemid 46819000)
22. Gijzen, M., and Nürnberger, T. 2006. Nep1-like proteins from plant pathogens: Recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67:1800-1807. (Pubitemid 44262364)
23. Godoy, G., Steadman, J. R., Dickman, M. 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. Griffith, G. W., Nicholson, J., Nenninger, A., Birch, R. N., and Hedger, J. N. 2003. Witches' brooms and frosty pods: Two major pathogens of cacao. N. Z. J. Bot. 41:423-435. (Pubitemid 38062117)
25. Guimaraes, R. L., and Stotz, H. U. 2004. Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol. 136:3703-3711.
26. Guo, X., and Stotz, H. U. 2007. Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol. Plant-Microbe Interact. 20:1384-1395. (Pubitemid 47612501)
27. Guo, X., and Stotz, H. U. 2010. ABA signaling inhibits oxalate-induced production of reactive oxygen species and protects against Sclerotinia sclerotiorum in Arabidopsis thaliana. Eur. J. Plant Pathol. 128:7-19.
28. 2-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol. 133:170-181. (Pubitemid 37144091)
29. Jabs, T. 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57:231-245. (Pubitemid 29056201)
30. Jennings, J. C., Apel-Birkhold, P. C., Mock, N. M., Baker, C. J., Anderson, J. D., and Bailey, B. A. 2001. Induction of defense responses in tobacco by the protein Nep1 from Fusarium oxysporum. Plant Sci. 161:891-899. (Pubitemid 32995294)
31. Jones, J. D. G., Dunsmuir, P., and Bedbrook, J. 1985. High level expression of introduced chimaeric genes in regenerated transformed plants. EMBO (Eur. Mol. Biol. Organ.) J. 4:2411-2418.
32. Keates, S. E., Tarlyn, N. M., Loewus, F. A., and Franceschi, V. R. 2000. L-ascorbic acid and L-galactose are sources for oxalic acid and calcium oxalate in Pistia stratiotes. Phytochemistry 53:433-440. (Pubitemid 30141034)
33. Keates, S. E., Kostman, T. A., Anderson, J. D., and Bailey, B. A. 2003. Altered gene expression in three plant species in response to treatment with Nep1, a fungal protein that causes necrosis. Plant Physiol. 132:1610-1622. (Pubitemid 36872908)
34. Kesarwani, M., Azam, M., Natarajan, K., Mehta, A., and Datta, A. 2000. Oxalate decarboxylase from Collybia velutipes: Molecular cloning and its overexpression to confer resistance to fungal infection in transgenic tobacco and tomato. J. Biol. Chem. 275:7230-7238. (Pubitemid 30146274)
35. Kim, K. S., Min, J. Y., and Dickman, M. B. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant-Microbe Interact. 21:605-612. (Pubitemid 351679739)
36. Liang, H., Maynard, C. A., Allen, R. D., and Powell, W. A. 2001. Increased Septoria musiva resistance in transgenic hybrid poplar leaves expressing wheat oxalate oxidase gene. Plant Mol. Biol. 45:619-629. (Pubitemid 33635752)
37. Livingstone, D. M., Hampton, J. L., Phipps, P. M., and Grabau, E. A. 2005. Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiol. 137:1354-1362. (Pubitemid 43119334)
38. Mattinen, L., Tshuikina, M., Mae, A., and Pirhonen, M. 2004. Identification and characterization of Nip, necrosis-inducing virulence protein of Erwinia carotovora subsp. carotovora. Mol. Plant-Microbe Interact. 17:1366-1375. (Pubitemid 39527330)
39. Mondego, J. M. C., Carazzolle, M. F., Costa, G. G. L., Formighieri, E. F., Parizzi, L. P., Rincones, J., Cotomacci, C., Carraro, D. M., Cunha, A. F., Carrer, H., Vidal, R. O., Estrela, R. C., Garcia, O., Thomazella, D. P. T., Oliveira, B. V. de, Pires, A. B. L., Rio, M. C. S., Araújo, M. R. R., Moraes, M. H. de, Castro, L. A. B., Gramacho, K. P., Gonçalves, M. S., Neto, J. P. M., Neto, A. G., Barbosa, L. V., Guiltinan, M. J., Bailey, B. A., Meinhardt, L. W., Cascardo, J. C. M., and Pereira, G. A. G. 2008. A genome survey of Moniliophthora perniciosa gives new insights into witches' broom disease of cacao. BMC Genomics 9:548.
40. Murashige, T., and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15:473-497.
41. Nitsch, J. P. 1969. Experimental androgenesis in Nicotiana. Phytomorphology 19:389-404.
42. Oliver, R. P., and Ipcho, S. V. S. 2004. Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol. Plant Pathol. 4:347-352. (Pubitemid 38940770)
43. Pemberton, C. L., and Salmond, G. P. C. 2004. The Nep1-like proteins-a growing family of microbial elicitors of plant necrosis. Mol. Plant Pathol. 5:353-359. (Pubitemid 38940771)
44. Purdy, L. H., and Schmidt, R. A. 1996. Status of cacao witches' broom: Biology, epidemiology, and management. Annu. Rev. Phytopathol. 34:573-594.
45. Qutob, D., Kemmerling, B., Brunner, F., Kufner, I., Engelhardt, S., Gust, A. A., Luberacki, B., Seitz, U. H., Stahl, D., Rauhut, T., Glawischnig, E., Schween, G., Lacombe, B., Watanabe, N., Lam, E., Schlichting, R., Scheel, D., Nau, K., Dodt, G., Hubert, D., Gijzen, M., and Numberger, T. 2006. Phytotoxicity and innate immune responses induced by Nep1 like proteins. Plant Cell 18:3721-3744. (Pubitemid 46464923)
46. Rio, M. C. S., Oliveira, B. V., Thomazella, D. P., Fracassi da Silva, J. A., and Pereira, G. A. G. 2008. Production of calcium oxalate crystals by the basidiomycete Moniliophthora perniciosa, the causal agent of the witches' broom disease of cacao. Curr. Microbiol. 56:363-370.
47. Schouten, A., Van Baarlen, P., and Van Kan, J. 2008. Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytol. 177:493-505. (Pubitemid 350295782)
48. Shetty, N. P., Jorgensen, H. J. L., Jensen, J. D., Collinge, D. B., and Shetty, H. S. 2008. Roles of reactive oxygen species in interactions between plants and pathogens. Eur. J. Plant Pathol. 121:267-280. (Pubitemid 351724234)
49. Staats, M., Van Baarlen, P., Schouten, A., and Van Kan, J. 2007. Functional analysis of NLP genes from Botrytis elliptica. Mol. Plant Pathol. 8:209-214.
50. Svedruzic, D., Jonsson, S., Toyota, C. G., Reinhardt, L. A., Ricagno, S., Lindqvist, Y., and Richards, N. G. J. 2005. The enzymes of oxalate metabolism: Unexpected structures and mechanisms. Arch. Biochem. Biophys. 433:176-192. (Pubitemid 39586592)
51. Thompson, C., Dunwell, J. M., Johnstone, C. E., Lay, V., Ray, J., Schmitt, M., Watson, H., and Nisbet, G. 1995. Degradation of oxalic acid by transgenic oilseed rape plants expressing oxalate oxidase. Euphytica 85:169-172.
52. Van Breusegem, F., and Dat, J. F. 2006. Reactive oxygen species in plant cell death. Plant Physiol. 141:384-390. (Pubitemid 43974532)
53. Van Kan, J. 2006. Licensed to kill: The lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11:247-253.
54. Veit, S., Worle, J. M., Nurnberger, T., Koch, W., and Seitz, H. U. 2001. A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defence responses in carrot, Arabidopsis, and tobacco. Plant Physiol. 127:832-841. (Pubitemid 33112145)
55. Walz, A., Zingen-Sell, I., Theisen, S., and Kortekamp, A. 2008. Reactive oxygen intermediates and oxalic acid in the pathogenesis of the necrotrophic fungus Sclerotinia sclerotiorum. Eur. J. Plant Pathol. 120:317-330. (Pubitemid 351322395)