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Changes in FaRP-like peptide levels during development of eggs from the plant-parasitic cyst nematode, Heterodera glycines

Published online by Cambridge University Press:  12 April 2024

E.P. Masler*
Affiliation:
Nematology Laboratory, Agricultural Research Service, United States Department of Agriculture, Beltsville, MD 20705, USA.
*
* Fax: 301 504 5589, E-mail: maslere@ba.ars.usda.gov Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture.

Abstract

The plant-parasitic cyst nematode Heterodera glycines requires a host plant to complete its life cycle, which involves hatching of infective juveniles that parasitize through root entry. A laboratory population of H. glycines grown on soybean, Glycine max, undergoes a sharp increase in maturity between 5 and 6 weeks in culture, as measured by the proportion of eggs containing well developed pre-hatch juveniles (late development eggs) versus eggs without visible juveniles (early development eggs). The median percent of eggs classified as late development, representing all samples taken from 4 to 7 weeks in culture, was 61%. For all samples taken up to 5 weeks, 80% scored below the median. In samples taken after 5 weeks, 15% scored below the median. This shift in population maturity was accompanied by a significant increase (P < 0.01) in the number of hatched juveniles present in each sample. There was also a significant increase (P < 0.02) in amount of FaRP-like peptide detected by specific ELISA. Total FaRP levels increased from 0.18 ± 0.07 fMol FLRFamide equivalents per ng protein in early development eggs to 0.40 ± 0.17 in late development eggs. The level remained high in hatched juveniles. HPLC/ELISA detected as many as nine potential FaRPs in H. glycines, two of which were specifically increased (P < 0.005) in hatched juveniles. The association of FaRPs with maturing eggs and the possible involvement of these neuropeptides with juvenile hatching and motility are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

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References

Brownlee, D.J.A. & Fairweather, I. (1999) Exploring the neurotransmitter labyrinth in nematodes. Trends in Neurosciences 22, 1624.CrossRefGoogle ScholarPubMed
Davis, E.E. & Stretton, A.O.W. (1996) The motornervous system of Ascaris: electrophysiology and anatomy of the neurones and their control by neuromodulators. Parasitology 113, S97S117.CrossRefGoogle ScholarPubMed
Davis, R.E. & Stretton, A.O.W. (2001) Structure-activity relationships of 18 endogenous neuropeptides on the motonervous system of the nematode Ascaris suum . Peptides 22, 723.CrossRefGoogle Scholar
Day, T.A. & Maule, A.G. (1999) Parasitic peptides. The structure and function of neuropeptides in parasitic worms. Peptides 20, 9991019.CrossRefGoogle ScholarPubMed
Edison, A.S., Messinger, L.A. & Stretton, A.O.W. (1997) Afp-1: a gene encoding multiple transcripts of a new class of FMRFamide-like neuropeptides in the nematode Ascaris suum . Peptides 18, 929935.CrossRefGoogle ScholarPubMed
Geary, T.G., Price, D.A., Bowman, J.W., Winterrowd, C.A., MacKenzie, C.D., Garrison, R.D., Williams, J.F. & Friedman, A.R. (1992) Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus . Peptides 13, 209214.CrossRefGoogle ScholarPubMed
Geary, T.G., Marks, N.J., Maule, A.G., Bowman, J.W., Alexander-Bowman, S.J., Larsen, M.L., Kubiak, T.M., Davis, J.P. & Thompson, D.P. (1999) Pharmacology of FMRFamide-related peptides (FaRPs) in helminths. Annals of the New York Academy of Sciences 897, 212227.CrossRefGoogle ScholarPubMed
Jacob, T.C. & Kaplan, J.M. (2003) The EGL-21 carboxypeptidase E facilitates acetylcholine release at Caenorhabditis elegans neuromuscular junctions. Journal of Neuroscience 23, 21222130.CrossRefGoogle ScholarPubMed
Keating, C., Thorndyke, M.C., Holden-Dye, L., Williams, R.G. & Walker, R.J. (1995) The isolation of a FMRFamide-like peptide from the nematode Haemonchus contortus . Parasitology 111, 515521.CrossRefGoogle ScholarPubMed
Keller, R. (1992) Crustacean neuropeptides: structures, functions and comparative aspects. Experientia 48, 439448.CrossRefGoogle ScholarPubMed
Kim, K. & Li, C. (2004) Expression and regulation of am FMRFamide-related neuropeptide gene family in Caenorhabditis elegans . Journal of Comparative Neurology 475, 540550.CrossRefGoogle Scholar
Kimber, M.J., Fleming, C.C., Bjourson, A.J., Halton, D.W. & Maule, A.G. (2001) FMRFamide-related peptides in potato cyst nematodes. Molecular and Biochemical Parasitology 116, 199208.CrossRefGoogle ScholarPubMed
Kimber, M.J., Fleming, C.C., Prior, A., Jones, J.T., Halton, D.W. & Maule, A.G. (2002) Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. International Journal for Parasitology 32, 10951105.CrossRefGoogle ScholarPubMed
Kingan, T.G., Zitnan, D., Jaffe, H. & Beckage, N.E. (1997) Identification of neuropeptides in the midgut of parasitized insects: FLRFamides as candidate paracrines. Molecular and Cellular Endocrinology 133, 1932.CrossRefGoogle ScholarPubMed
Klowden, M.J. (2003) Contributions of insect research toward our understanding of neurosecretion. Archives of Insect Biochemistry and Physiology 53, 101114.CrossRefGoogle ScholarPubMed
Marder, E.R., Calabrese, R.L., Nusbaum, M.P. & Trimmer, B. (1987) Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous systems of the rock crab, Cancer borealis, and the spiny lobster, Palinurus interruptus . Journal of Comparative Neurology 259, 150163.CrossRefGoogle Scholar
Marks, N.J., Maule, A.G., Halton, D.W., Li, C., Geary, T.G., Thompson, D.P. & Shaw, C. (1998) KSAYFMRFamide (PF3/AF8) is present in the free-living nematode Caenorhabditis elegans . Biochemical and Biophysical Research Communications 248, 422424.CrossRefGoogle ScholarPubMed
Marks, N.J., Sangster, N.C., Maule, A.G., Halton, D.W., Thompson, D.P., Geary, T.G. & Shaw, C. (1999) Structural characterization of KHEYLRFamide (AF2) and KSAYMRFamide (PF3/AF8) from Haemonchus contortus . Molecular and Biochemical Parasitology 100, 185194.CrossRefGoogle ScholarPubMed
Marks, N.J., Shaw, C., Halton, D.W., Thompson, D.P., Geary, T.G., Li, C. & Maule, A.G. (2001) Isolation and preliminary biological assessment of AADGAPLIRFamide and SVPGVLRFamide from Caenorhabditis elegans . Biochemical and Biophysical Research Communications 286, 11701176.CrossRefGoogle ScholarPubMed
Masler, E.P. (1999) Detection and partial characterization of egg proteins from Heterodera glycines . Journal of Nematology 31, 305311.Google ScholarPubMed
Masler, E.P., Kelly, T.J. & Menn, J.J. (1993) Insect neuropeptides: discovery and application in insect management. Archives of Insect Biochemistry and Physiology 22, 87111.CrossRefGoogle ScholarPubMed
Masler, E.P., Kovaleva, E.S. & Sardanelli, S.S. (1999) FMRFamide-like immunoactivity in Heterodera glycines (Nemata: Tylenchida). Journal of Nematology 31, 224231.Google ScholarPubMed
Merte, J. & Nichols, R. (2002) Drosophila melanogaster FMRFamide-containing peptides: redundant or diverse functions? Peptides 23, 209220.CrossRefGoogle ScholarPubMed
Muneoka, Y. & Kobayashi, M. (1992) Comparative aspects of structure and action of molluscan neuropeptides. Experientia 48, 448456.CrossRefGoogle ScholarPubMed
Nassel, D.R. (2002) Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progress in Neurobiology 68, 184.CrossRefGoogle ScholarPubMed
Nelson, L.S., Kim, K., Memmott, J.E. & Li, C. (1998) FMRFamide-like gene family in the nematode, Caenorhabditis elegans . Molecular Brain Research 58, 103111.CrossRefGoogle ScholarPubMed
Rex, E., Harmych, S., Puckett, T. & Komuniecki, R. (2004) Regulation of carbohydrate metabolism in Ascaris suum body wall muscle: a role for the FMRFamide AF2, not serotonin. Molecular and Biochemical Parasitology 13, 311313.CrossRefGoogle Scholar
Rogers, C., Reale, V., Kim, K., Chatwin, H., Li, C., Evans, P. & de Bono, M. (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nature Neuroscience 6, 11781185.CrossRefGoogle ScholarPubMed
Sardanelli, S. & Kenworthy, W.J. (1997) Soil moisture control and direct seeding for bioassay of Heterodera glycines on soybean. Journal of Nematology (Supplement) 29, 625634.Google ScholarPubMed
Taussig, R. & Scheller, R.H. (1986) The Aplysia FMRFamide gene encodes sequences related to mammalian brain peptides. DNA 5, 453461.CrossRefGoogle ScholarPubMed
Thompson, D.P., Davis, J.P., Larsen, M.J., Coscarelli, E.M., Zinser, E.W., Bowman, J.W., Alexander-Bowman, S.J., Marks, N.J. & Geary, T.G. (2003) Effects of KNEFIRFamide on cyclic adenosine monophosphate levels in Ascaris suum somatic muscle. International Journal for Parasitology 33, 199208.CrossRefGoogle ScholarPubMed
Thompson, J.M. & Tylka, G.L. (1997) Differences in hatching of Heterodera glycines egg-mass and encysted eggs in vitro . Journal of Nematology 29, 315321.Google ScholarPubMed