Abstract
The regulatory constraints imposed on use of chemical control agents in agriculture are rendering crops increasingly vulnerable to plant parasitic nematodes. Thus, it is important that new control strategies which meet requirements for low toxicity to non-target species, vertebrates and the environment are pursued. This would be greatly facilitated by an improved understanding of the physiology and pharmacology of these nematodes, but to date, these microscopic species of the Phylum Nematoda have attracted little attention in this regard. In this review, the current information available for neurotransmitters and neuromodulator in the plant parasitic nematodes is discussed in the context of the more extensive literature for other species in the phylum, most notably Caenorhabditis elegans and Ascaris suum. Areas of commonality and distinctiveness in terms of neurotransmitter profile and function between these species are highlighted with a view to improving understanding of to what extent, and with what level of confidence, this information may be extrapolated to the plant parasitic nematodes.
Similar content being viewed by others
References
Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L et al (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotech 26:909–915
Alford DV (2011) Plant pests. HarperCollins, London
Alkharouf NW, Klink VP, Matthews BF (2007) Identification of Heterodera glycines (soybean cyst nematode [SCN]) cDNA sequences with high identity to those of C. elegans having lethal mutant or RNAi phenotypes. Expt Parasitol 115:247–258
Atkinson HJ, Isaac RE, Harris PD, Sharpe CM (1988) FMRFamide-like immunoreactivity within the nervous system of the nematodes Panagrellus redivivus, Caenorhabditis elegans and Heterodera glycines. J Zool 216:663–671
Avery L (1993) Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. J Exp Biol 175:283–297
Bakhetia M, Charlton WL, Urwin PE, McPherson MJ, Atkinson HJ (2005) RNA interference and plant parasitic nematodes. Trends Plant Sci 10:362–367
Benson JA (1988) Bicuculline blocks the response to acetylcholine and nicotine but not to muscarine or GABA in isolated insect neuronal somata. Brain Res 458:65–71
Bessou C, Giugia JB, Franks CJ, Holden-Dye L, Ségalat L (1998) Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission. Neurogenetics 2:61–72
Bird AF (1974) Plant response to root-knot nematode. Phytopath 12:69–85
Blaxter ML (2003) Nematoda: genes, genomes and the evolution of parasitism. Adv Parasitol 54:101–195
Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75
Bridge J, Starr JL (2007) Plant nematodes of agricultural importance. Manson, London
Brownlee DJ, Holden-Dye L, Fairweather I, Walker RJ (1995) The action of serotonin and the nematode neuropeptide KSAYMRFamide on the pharyngeal muscle of the parasitic nematode, Ascaris suum. Parasitology 111:379–384
Chang S, Opperman CH (1991) Characterization of Acetylcholinesterase molecular forms of the root-knot nematode, Meloidogyne. Mol Biochem Parasitol 49:205–214
Chiang JT, Steciuk M, Shtonda B, Avery L (2006) Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes. J Exp Biol 209:1859–1873
Costa JC, Lilley CJ, Atkinson HJ, Urwin PE (2009) Functional characterization of a cyst nematode acetylcholinesterase gene using Caenorhabditis elegans as a heterologous system. Inter J Parasitol 39:849–858
Cowden C, Stretton AO (1995) Eight novel FMRFamide-like neuropeptides isolated from the nematode Ascaris suum. Peptides 16:491–500
Cully DF, Vassilatis DK, Liu KK, Paress PS, Van der Ploeg LH, Schaeffer JM, Arena JP (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371:707–711
Dalzell JJ, Warnock ND, Stevenson MA, Mousley A, Fleming CC, Maule AG (2010) Short interfering RNA-mediated knockdown of drosha and pasha in undifferentiated Meloidogyne incognita eggs leads to irregular growth and embryonic lethality. Int J Parasitol 40:1303–1310
Faske TR, Starr JL (2006) Sensitivity of Meloidogyne incognita and Rotylenchulus reniformis to Abamectin. J Nematol 38:240–244
Fleming CC, McKinney S, McMaster S, Johnston MJG, Donnelly P, Kimber MJ, Maule AG (2007) Getting to the root of neuronal signalling in plant parasitic nematodes using RNA interference. Nematology 9:301–315
Franks CJ, Holden-Dye L, Bull K, Luedtke S, Walker RJ (2006) Anatomy, physiology and pharmacology of Caenorhabditis elegans pharynx: a model to define gene function in a simple neural system. Invert Neurosci 6:105–122
Goverse A, Davis EL, Hussey RS (1994) Monoclonal antibodies to the oesophageal glands and stylet secretions of Heterodera glycines. J Nematol 26:251–259
Goverse A, de Engler JA, Verhees J, van der Krol S, Helder JH, Gheysen G (2000) Cell cycle activation by plant parasitic nematodes. Plant Mol Biol 43:747–761
Gowen SR (1997) Chemical control of nematodes: efficiency and side-effects. In: Plant nematode problems and their control in the North East region (FAO Plant Production and Protection Paper 144). Corporate Documentary Repository, USA
Hallem EA, Dillman AR, Hong AV, Zhang Y, Yano JM, Demarco SF, Sternberg PW (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21:377–383
Holden-Dye L, Krogsgaard-Larsen P, Nielsen L, Walker RJ (1989) GABA receptors on the somatic muscle cells of the parasitic nematode, Ascaris suum: stereoselectivity indicates similarity to a GABAA-type agonist recognition site. Br J Pharmacol 98:841–850
Huang Q-X, Cheng X-Y, Mao Z-C, Wang Y-S, Zhao L-L, Yan X, Ferris VR, Xu R-M, Xie B-Y (2010) MicroRNA discovery and analysis of pinewood nematode Bursaphelenchus xylophilus. PLoS One 5:e13271
Johnston MJG, McVeigh P, McMaster S, Fleming CC, Maule AG (2010) FMRFamide-like peptides in root knot nematodes and their potential role in nematode physiology. J Helminth 84:253–265
Jones AK, Davis P, Hodgkin J, Sattelle DB (2007) The nicotinic acetylcholine receptor gene family of the nematode Caenorhabditis elegans: an update on nomenclature. Invert Neurosci 7:129–131
Jonz MG, Rigga E, Mercier AJ, Potter JW (2001) Effect of 5-HT (serotonin) on reproductive behaviour in Heterodera schachtii (Nematoda). Can J Zool 79:1727–1732
Kaminsky R, Ducray P, Jung M, Clover R, Rufener L, Bouvier J, Weber SS, Wenger A, Wieland-Berghausen S, Goebel T, Gauvry N, Pautrat F, Skripsky T, Froelich O, Komoin-Oka C, Westlund B, Sluder A, Mäser P (2008) A new class of anthelmintics effective against drug-resistant nematodes. Nature 452(7184):176–180
Kang JS, Lee H, Moon IS, Lee Y, Koh YH, Je YH, Lim KJ, Lee SH (2009) Construction and characterization of subtractive stage-specific expressed sequence tag (EST) libraries of the pinewood nematode, Bursaphelenchus xylophilus. Genomics 94:70–77
Keating CD, Kriek N, Daniels M, Ashcroft NR, Hopper NA, Siney EJ, Holden-Dye L, Burke JF (2003) Whole-genome analysis of 60 G protein-coupled receptors in Caenorhabditis elegans by gene knockout with RNAi. Curr Biol 13:1715–1720
Kimber MJ, Fleming CC, Bjourson AJ, Halton DW, Maule AG (2001) FMRFamide-related peptides in potato cyst nematodes. Mol Biochem Parasitol 116:199–208
Kimber MJ, Fleming CC, Prior A, Jones JT, Halton DW, Maule AG (2002) Localization of Globodera pallida FMRFamide related peptide encoding genes using in situ hybridisation. Inter J Parasitol 32:1095–1105
Kimber MJ, McKinney S, McMaster S, Day TA, Fleming CC, Maule AG (2007) flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB J 21:1233–1243
Laffaire J, Jaubert S, Abad P, Rosso M (2003) Molecular cloning and life stage expression pattern of a new acetylcholinesterase gene from the plant nematode Meloidogyne incognita. Nematol 5:213–217
Li C, Kim K (2008) Neuropeptides. In: WormBook (ed) The C. elegans research community, WormBook. doi:10.1895/wormbook.1.142.1, http://www.wormbook.org
Li C, Kim K (2010) Neuropeptide gene families in Caenorhabditis elegans. In: Geary TG, Maule AG (eds) Neuropeptide systems as targets for parasite and pest control. Landes Bioscience, TX, pp 98–137
Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, Clardy J, Bargmann CI (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458:1171–1175
Marks NJ, Maule AG (2010) Neuropeptides in helminths: occurrence and distribution. Adv Exp Med Biol 692:49–77
Martin RJ, Robertson AP (2007) Mode of action of levamisole and pyrantel, anthelmintic resistance, E153 and Q57. Parasitology 134:1093–1104
Martin RJ, Pennington AJ, Duittoz AH, Robertson S, Kusel JR (1991) The physiology and pharmacology of neuromuscular transmission in the nematode parasite, Ascaris suum. Parasitol 102:S41–S58
Masler EP (2007) Responses of Heterodera glycines and Meloidogyne incognita to exogenously applied neuromodulators. J Helminth 81:421–427
Masler EP (2008) Responses of Heterodera glycines and Meloidogyne incognita to exogenously applied biogenic amines. Nematology 10:911–917
Masler EP (2010) In vitro comparison of protease activity in preparations from free-living (Paragrellus redivivus) and plant-parasitic (Meloidogyne incognita) nematodes using FMRFa and FMRFa-like peptides as substrates. J Helminth 84:425–433
Masler EP, Kovaleva ES, Sardanelli S (1999a) FMRFamide-like immunoreactivity in Heterodera glycines (Nematoda: Tylenchida). J Nematol 31:224–231
Masler EP, Kovaleva ES, Sardanelli S (1999b) Comparison of FaRP immunoreactivity in free-living nematodes and in the plant-parasitic nematode Heterodera glycines. Ann NY Acad Sci 897:253–263
Masler EP, Zasada IA, Sardanelli S, Rogers ST, Halbrendt JM (2010) Effects of benzyl isothiocyanate on the reproduction of Meloidogyne incognita on Glycine max and Capsicum annum. Nematol 12:693–699
Mbeunkui F, Scholl EH, Opperman CH, Goshe MB, Bird MKD (2010) Proteomic and bioinformatic analysis of the root-knot nematode Meloidogyne hapla: the basis for plant parasitism. J Proteome Res 9:5370–5381
McClure MA, von Mende N (1987) Induced salivation in plant-parasitic nematodes. Phytopath 77:1463–1469
McVeigh P, Leech S, Mair GR, Marks NJ, Geary TG, Maule AG (2005) Analysis of FMRFamide-like peptide (FLP) diversity in phylum Nematoda. Int J Parasitol 35:1043–1060
Opperman CH, Bird DM, Williamson VM, Rohksar DS, Burke M, Cohn J, Cromer J et al (2008) Sequence and genetic map of Meloidogyne hapla, a compact nematode genome for plant parasitism. Proc Natl Acad Sci USA 105:1402–1407
Papaioannou S, Marsden D, Franks CJ, Walker RJ, Holden-Dye L (2005) Role of a FMRFamide-like family of neuropeptides in the pharyngeal nervous system of Caenorhabditis elegans. J Neurobiol 65:304–319
Papaioannou S, Holden-Dye L, Walker RJ (2008a) Evidence for a role for cyclic AMP in modulating the action of 5-HT and an excitatory neuropeptide, FLP17A, in the pharyngeal muscle of Caenorhabditis elegans. Invert Neurosci 8:91–100
Papaioannou S, Holden-Dye L, Walker RJ (2008b) The actions of Caenorhabditis elegans neuropeptide-like peptides (NLPs) on body wall muscle of Ascaris suum and pharyngeal muscle of C. elegans. Acta Biol Hung 59(Suppl):189–197
Perry RN, Moens M, Starr JL (2009) Root-knot nematodes. CAB International, Oxford
Piotte C, Arthaud L, Abad P, Rosso MN (1999) Molecular cloning of an acetylcholinesterase gene from the plant parasitic nematodes, Meloidogyne incognita and Meloidogyne javanica. Mol Biochem Parasitol 99:247–256
Robertson L, Robertson WM, Jones JT (1999) Direct analysis of the secretions of the potato cyst nematode Globodera rostochiensis. Parasitol 119:167–176
Robertson AP, Clark CL, Burns TA, Thompson DP, Geary TG, Trailovic SM, Martin RJ (2002) Paraherquamide and 2-deoxy-paraherquamide distinguish cholinergic receptor subtypes in Ascaris muscle. J Pharmacol Exp Ther 302:853–860
Rogers CM, Franks CJ, Walker RJ, Burke JF, Holden-Dye L (2001) Regulation of the pharynx of Caenorhabditis elegans by 5-HT, octopamine, and FMRFamide-like neuropeptides. J Neurobiol 49:235–244
Rolfe RN, Perry RN (2001) Electropharyngeograms and stylet activity of second stage juveniles of Globodera rostochiensis. Nematology 3:31–34
Rosso MN, Dubrana MP, Cimbolini N, Jaubert S, Abad P (2005) Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Mol Plant Microb Interact 18:615–620
Rosso MN, Jones JT, Abad P (2009) RNAi and functional genomics in plant parasitic nematodes. Annu Rev Phytopathol 47:207–232
Rufener L, Baur R, Kaminsky R, Mäser P, Sigel E (2010) Monepantel allosterically activates DEG-3/DES-2 channels of the gastrointestinal nematode Haemonchus contortus. Mol Pharmacol 78:895–902
Sasser JN (1980) Root-knot nematodes: a global menace to crop production. Plant Dis 64:36–41
Schaller G (2004) The molecular cloning of an acetylcholinesterase class 2 gene from the plant nematode Globodera pallida. Univ Leeds, UK
Sharpe MJ, Atkinson HJ (1980) Improved visualization of dopaminergic-neurons in nematodes using the glyoxylic-acid fluorescence method. J Zool 190:273–284
Stewart GR, Perry RN, Wright DJ (1994) Immunocytochemical studies on the occurrence of gamma-aminobutyric acid in the nervous system of the nematodes Panagrellus redivivus, Meloidogyne incognita and Globodera rostochiensis. Fund Appl Nematol 17:433–439
Stewart GR, Perry RN, Wright DJ (2001) Occurrence of dopamine in Panagrellus redivivus and Meloidogyne incognita. Nematol 3:843–848
Stretton AO, Cowden C, Sithigorngul P, Davis RE (1991) Neuropeptides in the nematode Ascaris suum. Parasitology 102(Suppl):S107–S116
Trim JE, Holden-Dye L, Willson J, Lockyer M, Walker RJ (2001) Characterization of 5-HT receptors in the parasitic nematode, Ascaris suum. Parasitology 122:207–217
Tsalik EL, Niacaris T, Wenick AS, Pau K, Avery L, Hobert O (2003) LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Dev Biol 263:81–102
Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double-stranded RNA by pre-parasitic juvenile cyst nematodes leads to RNA interference. Mol Plant-Microbe Interact 15:747–752
van de Cappelle E, Plovie E, Kyndt T, Grunewald W, Cannoot B, Gheysen G (2008) AtCDKA;1 silencing in Arabidopsis thaliana reduces reproduction of sedentary plant-parasitic nematodes. Plant Biotech J 6:749–757
Welz C, Krüger N, Schniederjans M, Miltsch SM, Krücken J, Guest M, Holden-Dye L, Harder A, von Samson-Himmelstjerna G (2011) SLO-1-channels of parasitic nematodes reconstitute locomotor behaviour and emodepside sensitivity in Caenorhabditis elegans slo-1 loss of function mutants. PLoS Pathog 7:e1001330
Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745
Wright DJ, Birtle AJ, Roberts IT (1984) Triphasic locomotor response of a plant-parasitic nematode to avermectin: inhibition by the GABA antagonists bicuculline and picrotoxin. Parasitology 88:375–382
Yan Y, Davis EL (2002) Characterization of guanylyl cyclise genes in the soybean cyst nematode Heterodera glycines. Inter J Parasitol 32:65–72
Yu S, Avery L, Baude E, Garbers DL (1997) Guanylyl cyclise expression in specific sensory neurons: a new family of chemosensory receptors. Proc Natl Acad Sci USA 94:3384–3387
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Holden-Dye, L., Walker, R.J. Neurobiology of plant parasitic nematodes. Invert Neurosci 11, 9–19 (2011). https://doi.org/10.1007/s10158-011-0117-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10158-011-0117-2