Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-28T04:24:50.590Z Has data issue: false hasContentIssue false
  • English
  • Français

FMRFamide-like peptides in root knot nematodes and their potential role in nematode physiology†

Published online by Cambridge University Press:  21 October 2009

M.J.G. Johnston ,
P. McVeigh ,
S. McMaster ,
C.C. Fleming  and
A.G. Maule
M.J.G. Johnston*
Affiliation:
Parasitology, School of Biological Sciences, Medical Biology Centre, Queen's University Belfast, 97 Lisburn Road, BelfastBT9 7BL, Northern Ireland Applied Plant Science, Newforge Lane, Agri-Food and Biosciences Institute, BelfastBT9 5PX, Northern Ireland
P. McVeigh
Affiliation:
Parasitology, School of Biological Sciences, Medical Biology Centre, Queen's University Belfast, 97 Lisburn Road, BelfastBT9 7BL, Northern Ireland
S. McMaster
Affiliation:
Parasitology, School of Biological Sciences, Medical Biology Centre, Queen's University Belfast, 97 Lisburn Road, BelfastBT9 7BL, Northern Ireland Applied Plant Science, Newforge Lane, Agri-Food and Biosciences Institute, BelfastBT9 5PX, Northern Ireland
C.C. Fleming
Affiliation:
Applied Plant Science, Newforge Lane, Agri-Food and Biosciences Institute, BelfastBT9 5PX, Northern Ireland
A.G. Maule
Affiliation:
Parasitology, School of Biological Sciences, Medical Biology Centre, Queen's University Belfast, 97 Lisburn Road, BelfastBT9 7BL, Northern Ireland
*
*E-mail: michael.johnston@qub.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

FMRFamide-like peptides (FLPs) are a diverse group of neuropeptides that are expressed abundantly in nematodes. They exert potent physiological effects on locomotory, feeding and reproductive musculature and also act as neuromodulators. However, little is known about the specific expression patterns and functions of individual peptides. The current study employed rapid amplification of cDNA ends-polymerase chain reaction (RACE-PCR) to characterize flp genes from infective juveniles of the root knot nematodes, Meloidogyne incognita and Meloidogyne minor. The peptides identified from these transcripts are sequelogs of FLPs from the free-living nematode, Caenorhabditis elegans; the genes have therefore been designated as Mi-flp-1, Mi-flp-7, Mi-flp-12, Mm-flp-12 and Mi-flp-14. Mi-flp-1 encodes five FLPs with the common C-terminal moiety, NFLRFamide. Mi-flp-7 encodes two copies of APLDRSALVRFamide and APLDRAAMVRFamide and one copy of APFDRSSMVRFamide. Mi-flp-12 and Mm-flp-12 encode the novel peptide KNNKFEFIRFamide (a longer version of RNKFEFIRFamide found in C. elegans). Mi-flp-14 encodes a single copy of KHEYLRFamide (commonly known as AF2 and regarded as the most abundant nematode FLP), and a single copy of the novel peptide KHEFVRFamide. These FLPs share a high degree of conservation between Meloidogyne species and nematodes from other clades, including those of humans and animals, perhaps suggesting a common neurophysiological role which may be exploited by novel drugs. FLP immunoreactivity was observed for the first time in Meloidogyne, in the circumpharyngeal nerve ring, pharyngeal nerves and ventral nerve cord. Additionally, in situ hybridization revealed Mi-flp-12 expression in an RIR-like neuron and Mi-flp-14 expression in SMB-like neurons‡, respectively. These localizations imply physiological roles for FLP-12 and FLP-14 peptides, including locomotion and sensory perception.

Type
Research Papers
Information
Journal of Helminthology , Volume 84 , Issue 3 , September 2010 , pp. 253 - 265
Copyright
Copyright © Cambridge University Press 2010

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.)

Footnotes

†

Nucleotide sequence data reported in this paper are available in the GenBank™, EMBL and DDBJ databases under the accession numbers AY729023, AY856132, AY804187, AY907829 and DQ228710.

References

Abad, P., Gouzy, J., Aury, J.M., Castagnone-Sereno, P., Danchin, E.G., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V.C., Caillaud, M.C., Countinho, P.M., Dasilva, C., De Luca, F., Deau, F., Esquibet, M., Flutre, T., Goldstone, J.V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T.R., Markov, G.V., McVeigh, P., Pesole, G., Poulain, J., Robinson-Rechavi, M., Sallet, E., Segurens, B., Steinbach, D., Tytgat, T., Ugarte, E., van Ghelder, C., Veronico, P., Baum, T.J., Blaxter, M., Bleve-Zacheo, T., Davis, E.L., Ewbank, J.J., Favery, B., Grenier, E., Henrissat, B., Jones, J.T., Laudet, V., Maule, A.G., Quenseville, H., Rosso, M.N., Schiex, T., Smant, G., Weissenbach, J. & Wincker, P. (2008) Genome sequence of the metazoan plant parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909–915.CrossRefGoogle ScholarPubMed
Atkinson, H.J., Isaac, R.E., Harris, P.D. & Sharpe, C.M. (1988) FMRFamide-like immunoreactivity within the nervous system of the nematodes Panagrellus redivivus, Caenorhabditis elegans and Heterodera glycines. Journal of Zoology 216, 663–671.CrossRefGoogle Scholar
Bowman, J.W., Winterrowd, C.A., Freidman, A.R., Thompson, D.P., Klein, R.D., Davis, J.P., Maule, A.G., Blair, K.L. & Geary, T.G. (1995) Nitric oxide mediates the inhibitory effects of SDPNFLRFamide, a nematode FMRFamide related neuropeptide, in Ascaris suum. Journal of Neurophysiology 74, 1880–1888.CrossRefGoogle ScholarPubMed
Brownlee, D.J., Holden-Dye, L., Fairweather, I. & Walker, R.J. (1995a) The action of serotonin and the nematode neuropeptide KSAYMRFamide on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitology 111, 379–384.CrossRefGoogle ScholarPubMed
Brownlee, D.J.A., Holden-Dye, L., Walker, R.J. & Fairweather, I. (1995b) The pharynx of the nematode Ascaris suum: structure and function. Acta Biologica Hungarica 46, 195–204.Google ScholarPubMed
Brownlee, D., Holden-Dye, L. & Walker, R. (2000) The range and biological activity of FMRFamide-related peptides and classical neurotransmitters in nematodes. Advances in Parasitology 45, 109–180.CrossRefGoogle ScholarPubMed
Calvert, G.M., Talaska, G., Mueller, C.A., Ammenhauser, M.M., Au, W.W., Fajen, J.M., Fleming, L.E., Briggle, T. & Ward, E. (1998) Genotoxicity in workers exposed to methyl bromide. Mutant Research Genetics and Toxicological Effects 417, 115–128.Google ScholarPubMed
Chitwood, D.J. (2002) Phytochemical based strategies for nematode control. Annual Review of Phytopathology 40, 221–249.CrossRefGoogle ScholarPubMed
Chitwood, D.J. (2003) Research on plant parasitic nematode biology conducted by the United States Department of Agriculture–Agricultural Research Service. Pest Management Science 59, 748–753.CrossRefGoogle ScholarPubMed
Coons, A.H., Leduc, E.H. & Connolly, J. (1955) Studies on antibody production. A method for the histochemical demonstration of specific antibody and its application to a study of hyper immune rabbit. Journal of Experimental Medicine 102, 49–60.CrossRefGoogle Scholar
Cowden, C. & Stretton, A.O.W. (1993) AF2, an Ascaris neuropeptide: isolation, sequence and bioactivity. Peptides 14, 423–430.CrossRefGoogle ScholarPubMed
Cowden, C., Sithigorngul, P., Brackley, P., Guastella, J. & Stretton, A.O.W. (1993) Localisation and differential expression of FMRFamide-like immunoreactivity in the nematode Ascaris suum. Journal of Comparative Neurology 333, 455–468.CrossRefGoogle ScholarPubMed
Davis, R.E. (1998) Neurophysiology of glutamatergic signalling and anthelmintic action in Ascaris suum: pharmacological evidence for a kainite receptor. Parasitology 116, 471–486.CrossRefGoogle Scholar
Davis, R.E. & Stretton, A.O.W. (2001) Structure activity relationships of 18 endogenous neuropeptides on the motornervous system of the nematode, Ascaris suum. Peptides 22, 7–23.CrossRefGoogle Scholar
De Boer, J.M., Yan, Y., Smant, G., Davis, E.L. & Baum, T.J. (1998) In situ hybridization to messenger RNA in Heterodera glycines. Journal of Nematology 30, 309–312.Google ScholarPubMed
Fellowes, R.A., Maule, A.G., Marks, N.J., Geary, T.G., Thompson, D.P., Shaw, C. & Halton, D.W. (1998) Modulation of the motility of the vagina vera of Ascaris suum in vitro by FMRFamide–related peptides. Parasitology 116, 277–287.CrossRefGoogle Scholar
Franks, C.J., Holden-Dye, L., Williams, R.G., Pang, F.Y. & Walker, R.J. (1994) A nematode FMRFamide like peptide, SDPNFLRFamide, relaxes the dorsal muscle strip preparation of Ascaris suum. Parasitology 108, 229–236.CrossRefGoogle ScholarPubMed
Giannakou, I.O., Sidiropoulos, A. & Prophetou-Athanasiadou, D. (2002) Chemical alternatives to methyl bromide for the control of root knot nematodes in greenhouses. Pest Management Science 58, 290–296.CrossRefGoogle ScholarPubMed
Jackson, R.J. & Goldman, L. (1986) Aldicarb poisoning. Journal of the American Medical Association 256, 3218.CrossRefGoogle Scholar
Jacob, T.C. & Kaplan, J. (2003) The EGL-21 carboxypeptidase E facilitates acetylcholine release at Caenorhabditis elegans neuromuscular junctions. Journal of Neuroscience 23, 2122–2130.CrossRefGoogle ScholarPubMed
Johnson, A.W., Burtton, G.W., Sumner, D.R. & Handoo, Z. (1997) Coastal bermudagrass rotation and fallow for management of nematodes and soil borne fungi on vegetable crops. Journal of Nematology 29, 710–716.Google Scholar
Johnson, C.D. & Stretton, A.O.W. (1985) Localisation of choline acetyltransferase within identified motorneurones of the nematode, Ascaris. Journal of Neuroscience 5, 1984–1992.CrossRefGoogle Scholar
Karssen, G., Bolk, R.J., Van Aelst, A.C., van den Beld, I., Kox, L.F.F., Korthals, G., Molendjik, L., Zijlstra, C., Van Hoof, R. & Cook, R. (2004) Description of Meloidogyne minor, a root knot nematode associated with yellow patch disease in golf courses. Nematology 6, 59–72.CrossRefGoogle Scholar
Keating, C.D., Holden-Dye, L., Thorndyke, M.C., Williams, R.G., Mallett, A. & Walker, R.J. (1995) The FMRFamide-like neuropeptide AF2 is present in the parasitic nematode Haemonchus contortus. Parasitology 111, 515–521.CrossRefGoogle ScholarPubMed
Kim, K. & Li, C. (2004) Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Journal of Comparative Neurology 475, 540–550.CrossRefGoogle ScholarPubMed
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, 199–208.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, 1095–1105.CrossRefGoogle ScholarPubMed
Kimber, M.J., McKinney, S., McMaster, S., Day, T.A., Fleming, C.C. & Maule, A.G. (2007) Flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB Journal 21, 1233–1243.CrossRefGoogle Scholar
Kubiak, T.M., Larsen, M.J., Davis, J.P., Zantello, M.R. & Bowman, J.W. (2003) AF2 interaction with Ascaris suum body wall muscle membranes involves G-protein activation. Biochemical and Biophysical Research Communications 301, 456–459.CrossRefGoogle ScholarPubMed
Landau, M. & Tucker, J.W. Jr (1984) Acute toxicity of EDB and aldicarb to young of two esuarine fish species. Bulletin for Environmental Contamination and Toxicology 33, 127–132.CrossRefGoogle ScholarPubMed
Li, C. & Kim, K. (2008) Neuropeptides. Wormbook 25, 1–36.CrossRefGoogle Scholar
Li, C., Nelson, L.S., Kim, K., Nathoo, A. & Hart, A.C. (1999) Neuropeptide gene families in the nematode Caenorhabditis elegans. Annals of the New York Academy of Sciences 897, 239–252.CrossRefGoogle ScholarPubMed
Liu, T., Kim, K., Li, C. & Barr, M.M. (2007) FMRFamide-like neuropeptides and mechanosensory touch receptor neurons regulate male sexual turning behaviour in Caenorhabditis elegans. Journal of Neuroscience 27, 7174–7182.CrossRefGoogle ScholarPubMed
Marks, N.J., Shaw, C., Maule, A.G., Davis, J.P., Halton, D.W., Verhaert, P., Geary, T.G. & Thompson, D.P. (1995) Isolation of AF2 (KHEYLRFamide) from Caenorhabditis elegans: evidence for the presence of more than one FMRFamide-related peptide encoding gene. Biochemical and Biophysical Research Communications 217, 845–851.CrossRefGoogle ScholarPubMed
Marks, N.J., Sangster, N.C., Maule, A.G., Halton, D.W., Thompson, D.P., Geary, T.G. & Shaw, C. (1999) Structural characterisation and pharmacology of KHEYLRFamide (AF2) and KSAYMRFamide (PF3/AF8) from Haemonchus contortus. Molecular and Biochemical Parasitology 100, 185–194.CrossRefGoogle ScholarPubMed
Masler, E.P., Kovaleva, E.S. & Sardanelli, S. (1999) FMRFamide like immunoreactivity in Heterodera glycines (Nematoda: Tylenchida). Journal of Nematology 31, 224–231.Google Scholar
Maule, A.G., Shaw, C., Bowman, J.W., Halton, D.W., Thompson, D.P., Geary, T.G. & Thim, L. (1994) The FMRFamide-like neuropeptide AF2 (Ascaris suum) is present in the free living nematode, Panagrellus redivivus (Nematoda, Rhabditida). Parasitology 109, 351–356.CrossRefGoogle ScholarPubMed
Maule, A.G., Geary, T.G., Bowman, J.W., Shaw, C., Halton, D.W. & Thompson, D.P. (1996) The pharmacology of nematode FMRFamide related peptides. Parasitology Today 12, 351–357.CrossRefGoogle ScholarPubMed
McIntire, S.L., Jorgensen, E., Kaplan, J. & Horvitz, H.R. (1993) The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337–341.CrossRefGoogle ScholarPubMed
McVeigh, P., Leech, S., Mair, G.R., Marks, N.J., Geary, T.G. & Maule, A.G. (2005) Analysis of FMRFamide-like peptide (FLP) diversity in phylum Nematoda. International Journal for Parasitology 35, 1043–1060.CrossRefGoogle ScholarPubMed
McVeigh, P., Geary, T.G., Marks, N.J. & Maule, A.G. (2006) The FLP side of nematodes. Trends in Parasitology 22, 385–396.CrossRefGoogle ScholarPubMed
Moffett, C.L., Beckett, A.M., Mousley, A., Geary, T.G., Marks, N.J., Halton, D.W., Thompson, D.P. & Maule, A.G. (2003) The ovijector of Ascaris suum: multiple response types revealed by Caenorhabditis elegans FMRFamide related peptides. International Journal for Parasitology 33, 859–876.CrossRefGoogle ScholarPubMed
Mousley, A., Maule, A.G., Halton, D.W. & Marks, N.J. (2005a) Interphyla studies on neuropeptides: the potential for broad spectrum anthelmintic and/or endectocide discovery. Parasitology 131 (Suppl. 1), S143–S167.CrossRefGoogle ScholarPubMed
Mousley, A., Moffett, C.L., Duve, H., Thorpe, A., Halton, D.W., Geary, T.G., Thompson, D.P., Maule, A.G. & Marks, N.J. (2005b) Expression and bioactivity of allatostatin like neuropeptides in helminths. International Journal for Parasitology 35, 1557–1567.CrossRefGoogle ScholarPubMed
Nelson, L.S., Rosoff, M.L. & Li, C. (1998) Disruption of a neuropeptide gene, flp-1, causes multiple behavioural defects in Caenorhabditis elegans. Science 281, 1686–1689.CrossRefGoogle ScholarPubMed
Nico, A.I., Jimenez-Diaz, R.M. & Castillo, P. (2003) Solarization of soil in piles for the control of Meloidogyne incognita in olive nurseries in southern Spain. Plant Pathology 52, 770–778.CrossRefGoogle Scholar
Pang, F.Y., Mason, J., Holden-Dye, L., Franks, C.J., Williams, R.G. & Walker, R.J. (1995) The effects of the nematode peptide, KHEYLRFamide (AF2), on the somatic musculature of the parasitic nematode Ascaris suum. Parasitology 110, 353–362.CrossRefGoogle ScholarPubMed
Piedra Buena, A., Garcia Alvarez, A., Diez Rojo, M.A., Ros, C., Fernandez, P., Lacasa, A. & Bello, A. (2007) Use of pepper crop residues for the control of root knot nematodes. Bioresource Technology 98, 2846–2851.CrossRefGoogle ScholarPubMed
Reinitz, C.A., Herfel, H.G., Messinger, L.A. & Stretton, A.O. (2000) Changes in locomotory behaviour and cAMP produced in Ascaris suum by neuropeptides from Ascaris suum or Caenorhabditis elegans. Molecular and Biochemical Parasitology 111, 185–197.CrossRefGoogle ScholarPubMed
Ringstad, N. & Horvitz, H.R. (2008) FMRFamide neuropeptides and acetylcholine synergistically inhibit egg laying by C. elegans. Nature Neuroscience 11, 1168–1176.CrossRefGoogle ScholarPubMed
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, 1178–1185.CrossRefGoogle ScholarPubMed
Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. & Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences USA 95, 9750–9754.CrossRefGoogle ScholarPubMed
Sanchez Moreno, S., Alonso-Prados, E., Alonso-Prados, J.L. & Garcia-Baudin, J.M. (2009) Multivariate analysis of toxicological and environmental properties of soil nematodes. Pest Management Science 65, 82–92.CrossRefGoogle Scholar
Terefe, M., Terefa, T. & Sakhuja, P.K. (2009) Effect of a formulation of Bacillus firmus on root knot nematode Meloidogyne incognita infestation and the growth of tomato plants in the greenhouse and nursery. Journal of Invertebrate Pathology 100, 94–99.CrossRefGoogle ScholarPubMed
Trailovic, S.M., Clark, C.L., Roberston, A.P. & Martin, R.J. (2005) Brief application of AF2 produces long lasting potentiation of nAChR responses in Ascaris suum. Molecular and Biochemical Parasitology 139, 51–64.CrossRefGoogle ScholarPubMed
Trudgill, D.L. & Blok, V.C. (2001) Apomictic, polyphagous root knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annual Review of Phytopathology 39, 53–77.CrossRefGoogle ScholarPubMed
UNEP (United Nations Environmental Programme), (1992) Synthesis report of the methyl bromide interim scientific assessment and methyl bromide interim technology and economic assessment. Montreal Protocol Assessment Supplement 33. Nairobi, Kenya, UNEP.Google Scholar
Walker, R.J., Franks, C.J., Pemberton, D., Rogers, C. & Holden-Dye, L. (2000) Physiological and pharmacological studies on nematodes. Acta Biologica Hungarica 51, 379–394.CrossRefGoogle ScholarPubMed
Warbrick, E.V., Rees, H.H. & Howells, R.E. (1992) Immunocytochemical localisation of an FMRFamide-like peptide in the filarial nematodes Dirofilaria immitis and Brugia pahangi. Parasitology Research 78, 252–256.CrossRefGoogle ScholarPubMed
Watson, R.T., Albritton, D.L., Anderson, S.O. & Lee-Bapty, S. (1992) Methyl bromide: its atmospheric science, technology and economics. Montreal Protocol Assessment Supplement. Nairobi, Kenya, United Nations Environmental Programme on Behalf of the Contracting Parties to the Montreal Protocol.Google Scholar
White, J.D., Southgate, E., Thompson, J.N. & Brenner, S. (1986) The structure of the nervous system of Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London, Series B 314, 1–340.Google ScholarPubMed
Yew, J.Y., Kutz, K.K., Dikler, S., Messinger, L., Li, L. & Stretton, A.O. (2005) Mass spectrometric map of neuropeptide expression in Ascaris suum. Journal of Comparative Neurology 488, 396–413.CrossRefGoogle ScholarPubMed