Hostname: page-component-76fb5796d-9pm4c Total loading time: 0 Render date: 2024-04-26T12:00:36.925Z Has data issue: false hasContentIssue false
  • English
  • Français

Induction of ethylene biosynthesis and necrosis in weed leaves by a Fusarium oxysporum protein

Published online by Cambridge University Press:  20 January 2017

James C. Jennings ,
Patricia C. Apel-Birkhold ,
Bryan A. Bailey  and
James D. Anderson
James C. Jennings
Affiliation:
Weed Science Laboratory, USDA/ARS, Beltsville Agricultural Research Center, Beltsville, MD 20705
Patricia C. Apel-Birkhold
Affiliation:
Biocontrol of Plant Diseases Laboratory, USDA/ARS, Beltsville Agricultural Research Center Beltsville, MD 20705
Bryan A. Bailey
Affiliation:
Biocontrol of Plant Diseases Laboratory, USDA/ARS, Beltsville Agricultural Research Center Beltsville, MD 20705
Get access Rights & Permissions [Opens in a new window]

Abstract

A small assortment of microbial proteins have the ability to activate defense responses and induce necrosis in plant cells through cell signaling pathways. These proteins are of interest because of their potential use as bioherbicides and inducers of plant resistance in agriculture. A 24-kDa protein (Nep1) was purified from culture filtrates of Fusarium oxysporum, and the effects of this protein on weed leaves were investigated. This protein induced necrosis in detached leaves of Papaver somniferum, Lycopersicon esculentum, Malva neglecta, and Acroptilon repens when taken up through the petiole. The pattern and level of necrosis were dependent on the plant species. Treatment with Nep1 induced the production of ethylene in isolated leaves of various species, and the level of ethylene response was shown to be correlated to the concentration of the protein. Pretreating leaves of P. somniferum, L. esculentum, M. neglecta, and Cardaria draba with 100 µl L−1 ethylene enhanced the protein induction of ethylene biosynthesis in those leaves. Application of Nep1 (200 nM) as a spray to intact plants of Abutilon theophrasti, P. somniferum, Centaurea solstitialis, Centaurea maculosa, and Sonchus oleraceus resulted in extensive necrosis of leaves within 48 h. The results of this research are supplemental to our understanding of the role of specific polypeptides in plant/microbe interactions and demonstrates for the first time that a fungal protein can cause extensive necrosis when applied to weed species as a foliar spray.

Keywords

Fusarium oxysporum Schlechtend:Fr. f. sp. erythroxyliMalva neglecta Wallr., MALNE, common mallowCardaria draba L., CADDR, hoary cressPapaver somniferum L., PAPSO, opium poppyAcroptilon repens L. CENRE, Russian knapweedCentaurea maculosa Lam., CENMA, spotted knapweedSonchus oleraceus L. SONOL, annual sowthistleAbutilon theophrasti Medicus, ABUTH, velvetleafCentaurea solstitialis L. CENSO, yellow starthistleLycopersicon esculentum L. ‘Bonnie Best,’ tomatoBioherbicideelicitorethyleneSilwet L-77hairy vetch
Type
Research Article
Information
Weed Science , Volume 48 , Issue 1 , February 2000 , pp. 7 - 14
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abeles, F. B., Morgan, P. W., and Saltveit, M. E. Jr. 1992. Ethylene in Plant Biology, 2nd ed. San Diego: Academic Press, pp. 83–119.Google Scholar
Anderson, J. D., Bailey, B. A., Taylor, R., Sharon, A., Avni, A., Mattoo, A. K., and Fuchs, Y. 1993. Fungal xylanase elicits ethylene biosynthesis and other defense responses in tobacco. Pages 197–204 In Pech, J. C. et al., eds. Cellular and Molecular Aspects of the Plant Hormone Ethylene. Dordrecht: Kluwer Academic Publishers.CrossRefGoogle Scholar
Anderson, J. D., Cardinale, F. C., Jennings, J. C., Norman, H. A., Avni, A., Hanania, U., and Bailey, B. A. 1997. Involvement of ethylene in protein elicitor-induced plant responses. Pages 267–274 In Kanellis, A. K. et al., eds. Biology and Biotechnology of the Plant Hormone Ethylene. Dordrecht: Kluwer Academic Publishers.Google Scholar
Avni, A., Bailey, B. A., Mattoo, A. K., and Anderson, J. D. 1994. Induction of ethylene biosynthesis in Nicotiana tabacum by a Trichoderma viride xylanase is correlated to the accumulation of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase transcripts. Plant Physiol. 106:1049–1055.CrossRefGoogle Scholar
Bailey, B. A. 1995. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca . Phytopathology 85:1250–1255.CrossRefGoogle Scholar
Bailey, B. A., Avni, A., and Anderson, J. D. 1995. The influence of ethylene and tissue age on the sensitivity of Xanthi tobacco leaves to a Trichoderma viride xylanase. Plant Cell Physiol. 36:1669–1676.Google Scholar
Bailey, B. A., Hebbar, K. P., Strem, M., Darlington, L. C., and Lumsden, R. D. 1997a. An alginate prill formulation of Fusarium oxysporum Schlechtend:Fr. f.sp. erythroxyli for biocontrol of Erythroxylum coca var. coca . Biocontrol Sci. Technol. 7:423–435.Google Scholar
Bailey, B. A., Jennings, J. C., and Anderson, J. D. 1997b. Sensitivity of Erythroxylum coca var. coca to ethylene and fungal proteins. Weed Sci. 45:716–721.Google Scholar
Bailey, B. A., Jennings, J. C., and Anderson, J. D. 1997c. The 24 kDa protein from Fusarium oxysporum f.sp. erythroxyli: occurrence in related fungi and the effect of growth medium on its production. Can. J. Microbiol. 43:45–55.CrossRefGoogle ScholarPubMed
Bailey, B. A., Korcak, R. F., and Anderson, J. D. 1993. Sensitivity to an ethylene biosynthesis-inducing endoxylanase in Nicotiana tabacum L. cv. Xanthi is controlled by a single dominant gene. Plant Physiol. 101:1081–1088.Google Scholar
Bauer, D. W., Wei, Z.-M., Beer, S. V., and Collmer, A. 1995. Erwinia chrysanthemi HarpinEch: an elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol. Plant-Microbe Interact. 8:484–491.Google Scholar
Bauer, D. W., Zumoff, C. H., Theisen, T. M., Bogdanove, A. J., and Beer, S. V. 1997. Optimized production of Erwinia amylovora harpin and its use to control plant disease and enhance plant growth. Phytopathology 87:S7.Google Scholar
Boller, T. 1991. Ethylene in pathogenesis and disease resistance. Pages 293–314 In Mattoo, A. K. and Suttle, J. C., eds. The Plant Hormone Ethylene. Boca Raton, FL: CRC Press.Google Scholar
Bonnet, P., Bourdon, E., Ponchet, M., Blein, J.-P., and Ricci, P. 1996. Acquired resistance triggered by elicitins in tobacco and other plants. Eur. J. Plant Pathol. 102:181–192.Google Scholar
Boyette, C. D., Abbas, H. K., and Connick, W. J. Jr. 1993. Evaluation of Fusarium oxysporum as a potential bioherbicide for sicklepod (Cassia obtusifolia), coffee senna (C. occidentalis), and hemp sesbania (Sesbania exaltata) . Weed Sci. 41:678–681.Google Scholar
Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.Google Scholar
De Wit, P.J.G.M. and Spikman, G. 1982. Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiol. Plant Pathol. 21:1–11.Google Scholar
Dong, H., Bauer, D. W., Delaney, T. P., and Beer, S. V. 1997. Effect of harpin on Arabidopsis thaliana . Phytopathology 87:S24 (publication no. P-1997-0171-AMA).Google Scholar
Felix, G., Grosskopf, D. G., Regenass, M., Basse, C. W., and Boller, T. 1991. Elicitor-induced ethylene biosynthesis in tomato cells: characterization and use as a bioassay for elicitor action. Plant Physiol. 97:19–25.Google Scholar
Fravel, D. R., Stosz, S. K., and Larkin, R. P. 1996. Effect of temperature, soil type, and matric potential on proliferation and survival of Fusarium oxysporum f.sp. erythroxyli from Erythroxylum coca . Phytopathology 86:236–240.Google Scholar
Fuchs, Y., Saxena, A., Gamble, H. R., and Anderson, J. D. 1989. Ethylene biosynthesis-inducing protein from Celluylsin is an endoxylanase. Plant Physiol. 89:138–143.CrossRefGoogle ScholarPubMed
Hammond-Kosack, K. E., Silverman, P., Raskin, I., and Jones, J.D.G. 1996. Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology and the synthesis of ethylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance gene. Plant Physiol. 110:1381–1394.Google Scholar
Hanania, U. and Avni, A. 1997. High-affinity binding site for ethylene-inducing xylanase elicitor on Nicotiana tabacum membranes. Plant J. 12:113–120.Google Scholar
Hebbar, K. P., Lewis, J. A., Poch, S. M., and Lumsden, R. D. 1996. Agricultural by-products as substrates for growth, conidiation and chlamydospore formation by a potential mycoherbicide, Fusarium oxysporum strain EN4. Biocontrol Sci. Technol. 6:263–275.Google Scholar
Kooman-Gersmann, M., Honée, G., Bonnema, G., and De Wit, P.J.G. M. 1996. A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants. Plant Cell 8:929–938.Google Scholar
Kremer, R. J. and Schulte, L. K. 1989. Influence of chemical treatment and Fusarium oxysporum on velvetleaf (Abutilon theophrasti) . Weed Technol. 3:369–374.Google Scholar
Madhosingh, G. 1995a. Rapid tomato seedling assay for virulent isolates of Fusarium oxysporum f.sp. radicis-lycopersici (FORL), the tomato crown and root rot pathogen. J. Phytopathol. 143:435–437.Google Scholar
Madhosingh, G. 1995b. Relative wilt-inducing capacity of the culture filtrates of isolates of Fusarium oxysporum f.sp. radicis-lycopersici, the tomato crown and root rot pathogen. J. Phytopathol. 143:193–198.Google Scholar
May, M. J., Hammond-Kosack, K. E., and Jones, J.D.G. 1996. Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum . Plant Physiol. 110:1367–1379.Google Scholar
Pandey, A. K., Farkya, S., and Rajak, R. C., 1992. A preliminary evaluation of Fusarium spp. for biological control of Parthenium . J. Indian Bot. Soc. 71:103–105.Google Scholar
Qui, D., Wei, Z.-M., Bauer, D. W., and Beer, S. V. 1997. Treatment of tomato seed with harpin enhances germination and growth and induces resistance to Ralstonia solanacearum . Phytopathology 87:S80 (publication no. P-1997-0572-AMA).Google Scholar
Ricci, P., Panabieres, F., Bonnet, P., Maia, N., Ponchet, M., Devergne, J.-C., Marais, A., Cardin, L., Milat, M. L., and Blein, J. P. 1993. Proteinaceous elicitors of plant defense responses. Pages 121–135 In Fritig, B. and Legrand, M., eds. Mechanisms of Plant Defense Responses. Dordrecht: Kluwer Academic Publishers.Google Scholar
Schägger, H. and von Jagow, G. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368–379.Google Scholar
Sutherland, M. L. and Pegg, G. F. 1995. Purification of a toxin from Fusarium oxysporum f.sp. lycopersici race 1. Physiol. Mol. Plant Pathol. 46:243–254.Google Scholar
Theisen, T. M., Bauer, D. W., and Beer, S. V. 1997. Harpin from Erwinia amylovora induces plant resistance without causing macroscopic necrosis. Phytopathology 87:S96 (publication no. P-1997-0685-AMA).Google Scholar
Wei, Z.-M., Laby, R. J., Zumoff, C. H., Bauer, D. W., He, S. Y., Collmer, A., and Beer, S. V. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora . Science 257:85–88.Google Scholar
Wray, W., Boulikas, T., Wray, V. P., and Hancock, R. 1981. Silver staining of proteins in polyacrylamide gels. Anal. Biochem. 118:197–203.Google Scholar
Yu, L. M. 1995. Elicitins from Phytophthora and basic resistance in tobacco. Proc. Natl. Acad. Sci. USA 92:4088–4094.Google Scholar