Neuromuscular Function in Plant Parasitic Nematodes: a Target for Novel Control Strategies? M
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Biomedical Sciences Publications Biomedical Sciences 10-2005 Neuromuscular function in plant parasitic nematodes: a target for novel control strategies? M. J. Kimber Iowa State University, [email protected] C. C. Fleming Queen's University Belfast Follow this and additional works at: http://lib.dr.iastate.edu/bms_pubs Part of the Computational Biology Commons, Neuroscience and Neurobiology Commons, Parasitology Commons, and the Plant Pathology Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ bms_pubs/19. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Biomedical Sciences at Iowa State University Digital Repository. It has been accepted for inclusion in Biomedical Sciences Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Neuromuscular function in plant parasitic nematodes: a target for novel control strategies? Abstract Over the last decade the need for new strategies and compounds to control parasitic helminths has become increasingly urgent. The neuromuscular systems of these worms have been espoused as potential sources of target molecules for new drugs which may address this need. One facet of helminth neuromuscular biology which has garnered considerable research interest is that of neuropeptidergic neurotransmission, particularly regarding parasites of humans and animals, as well as free-living nematode model species. This research interest has been piqued by the fact that neuropeptides have been demonstrated to be fundamentally important to nematode biology and thus may be of utility in this search for new drug targets. This review focuses on the neuropeptide biology of plant parasitic nematodes, a subject which has been comparatively neglected despite the fact that the search for alternative control measures also extends to these economically important parasites. We focus on the FMRFamide-like peptide (FLP) neuropeptides and the complexity and distribution of this peptide family in plant parasitic nematodes. Possible roles for FLPs in plant parasitic nematode behaviour, as elucidated by a combination of molecular imaging techniques and RNA interference (RNAi), are discussed. We propose that disruption of FLP neurosignalling in plant parasitic nematodes represents a novel form of pest control and speculate as to how this may be achieved. Keywords Nematode, Plant parasitic nematode, Neuropeptide, FMRFamide-like peptide, FLP, Indirect immunocytochemistry, in situ hybridization, RNAi Disciplines Computational Biology | Neuroscience and Neurobiology | Parasitology | Plant Pathology Comments This article is from Parasitology 131 (2005): S129–S142, doi:10.1017/S0031182005009157. Posted with permission. This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/bms_pubs/19 S129 Neuromuscular function in plant parasitic nematodes: a target for novel control strategies? M. J. KIMBER1* and C. C. FLEMING2,3 1 Department of Biomedical Sciences, Iowa State University, Ames, IA. 50011, USA 2 Applied Plant Science, Queen’s University Belfast, Newforge Lane, Belfast. BT9 5PX, UK 3 Department of Agriculture and Rural Development for Northern Ireland, Newforge Lane, Belfast, BT9 5PX, UK SUMMARY Over the last decade the need for new strategies and compounds to control parasitic helminths has become increasingly urgent. The neuromuscular systems of these worms have been espoused as potential sources of target molecules for new drugs which may address this need. One facet of helminth neuromuscular biology which has garnered considerable research interest is that of neuropeptidergic neurotransmission, particularly regarding parasites of humans and animals, as well as free-living nematode model species. This research interest has been piqued by the fact that neuropeptides have been demonstrated to be fundamentally important to nematode biology and thus may be of utility in this search for new drug targets. This review focuses on the neuropeptide biology of plant parasitic nematodes, a subject which has been com- paratively neglected despite the fact that the search for alternative control measures also extends to these economically important parasites. We focus on the FMRFamide-like peptide (FLP) neuropeptides and the complexity and distribution of this peptide family in plant parasitic nematodes. Possible roles for FLPs in plant parasitic nematode behaviour, as elucidated by a combination of molecular imaging techniques and RNA interference (RNAi), are discussed. We propose that disruption of FLP neurosignalling in plant parasitic nematodes represents a novel form of pest control and speculate as to how this may be achieved. Key words: Nematode, plant parasitic nematode, neuropeptide, FMRFamide-like peptide, FLP, indirect immuno- cytochemistry, in situ hybridization, RNAi. INTRODUCTION and by facilitating fungal and bacterial infection. This damage is often non-specific and symptoms Many of the compounds used to control nematode of infection may be difficult to detect such that the parasites of medical and veterinary importance have detrimental economic effects of plant parasitism molecular targets within the neuromuscular system. tend to be underestimated; reported annual losses It is reasonable to conject, therefore, that targets for of US$100 billion to world agriculture (Sasser & new generations of nematicidal agents may also be Freckman, 1987) testify to the significance of the found within the nematode neuromuscular system. problem caused by plant parasitic nematodes. From a parasitology perspective, this hypothesis Over 50 genera of plant parasitic nematodes has driven the study of nematode neurobiology are found parasitizing all parts of plants but the and muscle control in human and animal parasitic most frequent target is the root system. The Order species, as well as those free-living nematodes which Dorylaimida (Class Adenophora) includes the are deemed good models for parasitic nematodes. families Longidoridae and Trichodoridae, both of This has been a profitable endeavour as it has greatly which comprise migratory species that are ecto- advanced our understanding of nematode neuro- parasitic on plant roots. Within these families are muscular function and in the process has thrown several important nematode vectors of soil-borne up several promising leads for parasiticide targets. viruses. The Order Tylenchida (Class Secernentea) Very little research, however, has been devoted to contains genera exhibiting a much wider range of the study of plant parasitic nematode neuromuscular host-parasite relationships in which an increased function. This is surprising given the impact that complexity in the host-parasite interaction is plant parasitic nematodes have on crop production reflected in an enhanced ability of the parasite to and the lack of effective control strategies to combat modify and regulate host plant gene expression. nematode attack. Phytoparasitic nematodes damage Thus, appearing within these genera are migratory crops by direct feeding, transmission of viruses ectoparasites, sedentary ectoparasites, migratory ecto-endoparasites, migratory endoparasites and * To whom correspondence should be addressed: sedentary endoparasites. The sedentary endopara- Tel: +1 (515) 294 5833. Fax: +1 (515) 294 2315. E-mail: sites represent the apex of intricacy with regard to [email protected] the plant-nematode interaction and their ability to Parasitology (2005), 131, S129–S142. f 2005 Cambridge University Press doi:10.1017/S0031182005009157 Printed in the United Kingdom M. J. Kimber and C. C. Fleming S130 regulate host plant genes is most pronounced. These granted that plant parasitic nematodes have similar nematodes can reorganise plant root morphology neuromuscular biology to their free-living and and physiology at the site of interaction and establish animal parasitic cousins. The main nematode excit- complex cellular structures that provide nutrients atory and inhibitory neurotransmitters are acetyl- for nematode development and reproduction. Most choline (ACh) and c-aminobutyric acid (GABA); the plant parasitic nematode life cycles comprise six potent acitivity of acetylcholinesterase inhibitors stages: the undifferentiated egg, four juvenile stages suggests ACh is critical to phytoparasitic nematode (J1 to J4) and the adult. Invasion of the host plant biology and immunocytochemical studies confirm by these sedentary endoparasites is by the J2 stage the presence of GABA (Stewart, Perry & Wright, and the modification of plant tissues allows for 1994) in the phytoparasitic nematode nervous progression of the life cycle. These sedentary endo- system. Our review is concerned, however, not with parasites, the most highly adapted parasites, cause these classical neurotransmitters for which there severe economic damage to forestry, horticultural has been a paucity of research with regard to plant and agricultural crops. parasitic nematodes, but with the neuropeptidergic Plant parasitic nematode control strategies tra- component of phytoparasitic nematode nervous ditionally involve the use of plant health legislation, systems, particularly in the cyst-forming genera. The crop rotation, resistant plant varieties and treatment aim of this review is to demonstrate not only the with nematicidal chemicals. Intensive agricultural abundance and