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Chemotaxis Disruption in Pratylenchus Scribneri by Tall Fescue Root Extracts and Alkaloids

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Abstract

Tall fescue (Festuca arundinacea) forms a symbiotic relationship with the clavicipitalean fungal endophyte Neotyphodium coenophialum. Endophyte-infected grass is tolerant to nematode, but the factors responsible are unknown. One objective of this work was to determine if root extracts of tall fescue effected chemoreceptor activity of Pratylenchus scribneri by using an in vitro chemoreception bioassay. Another objective was to determine if specific ergot alkaloids (ergovaline, ergotamine, a-ergocryptine, ergonovine), and loline alkaloids, all produced by the fungal endophyte, altered chemotaxis with this bioassay. Methanolic extract from roots altered chemotaxis activities in this nematode but only from roots of plants cultured 45 ≥ d, which repelled nematodes. Extracts prepared from noninfected grasses were attractants. This assay indicated that the alkaloids were either repellents or attractants. N-formylloline was an attractant at concentrations of 20 μg/ml and lower, while at higher concentrations it was a repellent. Ergovaline, the major ergot alkaloid produced by the endophyte, was repellent at both high and low concentrations and caused complete death of the nematodes.

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References

  • AGEE, C. S., and HILL, N. S. 1994. Ergovaline variability in Acremonium-infected tall fescue due to environment and plant genotype. Crop. Sci. 34: 221–226.

    Article  Google Scholar 

  • BACETTY, A. A. 2008. Nematoxicity of Neotyphodium-infected tall fescue alkaloids and other secondary metabolites on the plant-parasitic nematode Pratylenchus scribneri. PhD dissertation. University of Georgia, Athens.

  • BACETTY, A. A., SNOOK, M. E., GLENN, A. E., BACON, C. W., NAGABHYRU, P. N., and SCHARDL, C. L. 2007. Nematotoxic effects of endophyte-infected tall fescue toxins and extracts in an in vitro bioassay using the nematode Pratylenchus scribneri, pp. 357–361, in A. J. Popay and E. R. Thom (eds.). Proc. 6th International Symposium on Fungal Endophytes of Grasses, Christchurch, NZ. New Zealand Grassland Association, Dunedin, New Zealand.

  • BACON, C. W., PORTER, J. K., ROBBINS, J. D., and LUTTRELL, E. S. 1977. Epichloe typhina from toxic tall fescue grasses. Appl. Environ.Microbiol. 34: 576–581.

    PubMed  CAS  Google Scholar 

  • BERNARD, E. C., GWINN, K. D., PLESS, C. D., and WILLIVER, C. D. 1997. Soil Invertebrate species diversity and abundance in endophyte-infected tall fescue pastures, pp. 125–135, in C. W. Bacon and N. S. Hill (eds.). Neotyphodium/Grass Interactions. Plenum, New York.

    Google Scholar 

  • BUSH, L. P., FANNIN, F. F., SIEGEL, M. R., DAHLMAN, D. L., and BURTON, H. L. 1993. Chemistry, occurrence and biological effects of saturated pyrrolizidine alkaloids associated with endophyte—grass interaction. Agri. Ecosys. Environ. 44: 81–102.

    Article  CAS  Google Scholar 

  • CROSS, D. L., REDMOND, L. M., and STRICKLAND, J. R. 1995. Equine fescue toxicosis: Signs and solutions. J. Anim. Sci. 73: 899–908.

    PubMed  CAS  Google Scholar 

  • DENTON, C. S., BRADGETT, R. D., COOK, R., and HOBBS, P. J. 1999. Low amounts of root herbivory positively influence the rhizosphere microbial community in a perpetrate grassland soil. Soil Biol. Biochem. 31: 155–165.

    Article  CAS  Google Scholar 

  • DYER, D. C. 1993. Evidence that ergovaline acts on serotonin receptors. Life Sci. 53: 223–228.

    Article  Google Scholar 

  • GARCIA, L. R., MEHTA, P., and STERNBERG, P. W. 2001. Regulation of distinct muscle behaviors controls the C. elegans male’s copulatory spicules during mating. Cell 107: 777–788.

    Article  PubMed  CAS  Google Scholar 

  • GLENN, A. E., BACON, C. W., PRICE, R., and HANLIN, R. T. 1996. Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88: 369–383.

    Article  CAS  Google Scholar 

  • GWINN, K. D., BERNARD, E. C., and PLESS, C. D. 1992. Pathogen and pest resistance in endophyte-infected tall fescue, pp. 139–145, in P. M. Gresshoff (ed.). Plant Biotechnology and Development. CRC, Boca Raton.

    Google Scholar 

  • HALLAM, S., SINGER, E., WARING, D., and YIN, Y. S. 2000. The C. elegans neuroD homolog cnd-1 functions in multiple aspects of motor neuron fate specification. Development 127: 4239–4252.

    PubMed  CAS  Google Scholar 

  • HIATT, E. E., and HILL, N. S. 1997. Neotyphodium coenophialum mycelial protein and herbage mass effects on ergot alkaloid concentration in tall fescue. J. Chem. Ecol. 23: 2721–2736.

    Article  CAS  Google Scholar 

  • HINTON, D. M., and BACON, C. W. 1985. The distribution and ultrastructure of the endophyte of toxic tall fescue. Can. J. Bot. 63: 36–42.

    Google Scholar 

  • KIMMONS, C. A., GWINN, K. D., and BERNARD, E. C. 1990. Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis. 74: 757–761.

    Article  Google Scholar 

  • LARSON, B. T., SAMFORD, M. D., CAMDEN, J. M., PIPER, E. L., KERLEY, M. S., PATERSON, J. A., and TURNER, J. T. 1995. Ergovaline binding and activation of D2 dopamine receptors in GH4ZR7 cells. J. Anim. Sci. 73: 1396–1400.

    PubMed  CAS  Google Scholar 

  • LARSON, B. T., HARMON, E. L., PIPER, E. L., GRIFFIS, L. M., and BUSH, L. P. 1999. Alkaloid binding and activation of D2 dopamine receptors in cell culture. J. Anim. Sci. 77942: 947.

    Google Scholar 

  • LEUCHTMANN, A., SCHMIDT, D., and BUSH, L. P. 2000. Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophyes. J. Chem. Ecol. 26: 1025–1036.

    Article  CAS  Google Scholar 

  • LOER, C. M., and KENYON, C. 1993. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. Neuroscience 13: 5407–5417.

    PubMed  CAS  Google Scholar 

  • LYONS, P. C., PLATTNER, R. D., and BACON, C. W. 1986. Occurrence of peptide and clavine ergot alkaloids in tall fescue. Science 232: 487–489.

    Article  PubMed  CAS  Google Scholar 

  • MATTOCKS, A. R. 1986. Chemistry and Toxicology of Pyrrolizidine Alkaloids. Academic, New York.

    Google Scholar 

  • MCGLOHON, N. E., SASER, J. N., and SHERWOOD, R. T. 1961. Investigations of plant-parasitic nematodes associated with forage crops in North Carolina. N. C. Agric. Exper. Stat. Tech. Bull. 148: 1–39.

    Google Scholar 

  • MEYER, S. L. F., HUETTEL, R. N., and SAYRE, R. M. 1990. Isolation of fungi from Heterodera glycines and in vitro bioassays for their antagonism to eggs. J. Nematology 22: 532–537.

    CAS  Google Scholar 

  • PERRY, R. N. 1996. Chemoreception in plant parasitic nematodes. Annu. Rev. Phytopathol. 34: 181–191.

    Article  PubMed  CAS  Google Scholar 

  • ROBERTS, C. A., MAREK, S. M., NIBLACK, T. L., and KARR, A. L. 1992. Parasitic Meloidogyne and mutualistic Acremonium increase chitinase in tall fescue. J. Chem. Ecol. 18: 1107–1116.

    Article  CAS  Google Scholar 

  • SALMINEN, S. O., and PARWINDER, S. G. 2002. Does decreased mowing frequency enhance alkaloid production in endophytic tall fescue and perennial ryegrass? J. Chem. Ecol. 28: 939–950.

    Article  PubMed  CAS  Google Scholar 

  • SALMINEN, S. O., PARWINDER, S. G., and QUIGLEY, M. F. 2003. Does mowing height influence alkaloid production in endophytic tall fescue and perennial ryegrass? J. Chem. Ecol. 29: 1319–1328.

    Article  PubMed  CAS  Google Scholar 

  • SCHAFER, W. R., and KENYON, C. 1995. A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375: 73–78.

    Article  PubMed  CAS  Google Scholar 

  • SHARP, M. J., and AKINSON, H. J. 1980. Improved visualization of dopaminergic-neurons in nematodes using the glycoxilic-acid fluorescence method. Zoology 190: 273–284.

    Google Scholar 

  • STEWART, G. R., PERRY, R. N., and WRIGHT, D. J. 2001. Occurrence of dopamine in Pangrellus redivivus and Meloidogyne incognita. Nematology 3: 843–858.

    Article  CAS  Google Scholar 

  • WEINSHENKER, D. Z., GARRIGA, G., and THOMAS, J. H. 1995. Genetic and pharmalogical analysis of neurotransmitters controlling egg laying in C. elegans. Neuroscience 15: 6975–6985.

    PubMed  CAS  Google Scholar 

  • WEST, C. P., IZEKOR, E., OOSTERHUIS, D. M., and ROBBINS, R. T. 1988. The effects of Acremonium coenophialum on growth and nematode infestation of tall fescue. Plant Soil 112: 3–6.

    Article  Google Scholar 

  • WUYTS, N., SWENNEN, R., and WAELE, D. D. 2006. Effects of plant phenylpropanoid pathy products and selected terpenoids and alkaloids on the behavior of the plant parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne. Nematology 8: 89–101.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank D. M. Hinton, USDA, ARS, for technical advice; C. Schardl, Univ. Kentucky, USDA-ARS Specific Cooperative Agreement Grant 200506271031 Department of Plant Pathology, University of Kentucky for his assistance and donation of loline; Dr. Susan Meyer for assistance concerning the sterile nematode culture and care used in this work; and H.R. Harrison, Jr. for supplying an authentic sample of 3,5-dicaffeoylquinic acid. We also acknowledge the assistance of Trevor Mitchell, USDA, ARS, with chemical analyses and Donald Woods, Crop and Soil Sciences Department, University of Georgia for assistance with the tall fescue cultivar Jesup.

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Authors and Affiliations

  1. Toxicology & Mycotoxin Research Unit, USDA, ARS Russell Research Center, Athens, GA, 30604, USA

    Ada A. Bacetty, Maurice E. Snook, Anthony E. Glenn & Charles W. Bacon

  2. Department of Plant Pathology, University of Georgia, Athens, GA, 30602, USA

    Ada A. Bacetty & James P. Noe

  3. Department of Plant Pathology, University of Kentucky, Lexington, USA

    Padmaja Nagabhyru

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  1. Ada A. Bacetty
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  2. Maurice E. Snook
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  3. Anthony E. Glenn
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  5. Padmaja Nagabhyru
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  6. Charles W. Bacon
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Correspondence to Charles W. Bacon.

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Bacetty, A.A., Snook, M.E., Glenn, A.E. et al. Chemotaxis Disruption in Pratylenchus Scribneri by Tall Fescue Root Extracts and Alkaloids. J Chem Ecol 35, 844–850 (2009). https://doi.org/10.1007/s10886-009-9657-x

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  • DOI: https://doi.org/10.1007/s10886-009-9657-x

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