Basic research in molecular plant nematology is expanding the inventory of knowledge that can be applied to provide crop resistance to parasitic nematodes in an economically and environmentally beneficial manner. Approaches to trans-genic nematode control can be classified as acting (1) on nematode targets, (2) at the nematode—plant interface, and (3) in the plant response. Strategies aimed at nematode targets include disruption of nematode intestinal function through recombinant plant expression of protease inhibitors orBacillus thuringiensis(BT) toxins, expression of double-stranded RNAs (dsRNAs) that cause silencing of essential nematode genes, disruption of sensory nervous system function, and generation of nematicidal metabolites. Methods directed at disruption of the nematode—plant interface include expression of proteins, or dsRNAs, that block the function of nematode parasitism gene products involved in migration through the plant vasculature or feeding site establishment, production of molecules repellent to the nematode, or conversion of the plant to a non-host. Approaches acting through the plant response include expression of a cloned plant resistance gene triggering a hypersensitive response, expression of gene(s) deleterious to the feeding site with a feeding site-specific promoter, and conversion of the plant from sensitive to tolerant. Degrees of resistance have been demonstrated through recombinant expression of protease inhibitors, dsRNAs, and cloned plant resistance genes, although none of these discoveries has yet reached commercialization. The focus of molecular plant nematology on root-knot and cyst nematodes makes it likely that transgenic technology will first be commercially applied to these sedentary endoparasites with eventual application to other species. Successful commercialization of biotechnology-derived crops with nematode resistance that result in large yield benefits for producers as well as environmental benefits will be an important milestone for the discipline of molecular plant nematology and should accelerate further progress.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Adkisson P, Abraham S, Baenzinger S, Betz F, Carrington JC, Goldburg RJ, Gould F, Hodgson E, Jones T, Levin M, Lichtenberg E, Snow A, Kuzma J, Phillips MJ (2000) Genetically modified pest-protected plants, science and regulation. National Research Council, Washington DC.
Atkinson HJ, Lilley CJ, Urwin PE, McPherson MJ (1998a) Engineering resistance in the potato to potato cyst nematodes. In: Marks RJ, Brodie BB (eds) Potato cyst nematodes, biology, distribution and control. CAB International, Wallingford, pp 209–236
Atkinson HJ, Lilley CJ, Urwin PE, McPherson MJ (1998b) Engineering resistance to plant-parasitic nematodes. In: Perry RN, Wright DJ (eds) The physiology and biochemistry of free-living and plant-parasitic nematodes. CABI Publishing, Wallingford pp 381–405
Atkinson HJ, Green J, Cowgill S, Levesley A (2001) The case for genetically modified crops with a poverty focus. Trends Biotech 19:91–96
Atkinson HJ, Urwin PE, McPherson MJ (2003) Engineering plants for nematode resistance. Annu Rev Phytopathol 41:615–639
Atkinson HJ, Grimwood S, Johnston K, Green J (2004) Prototype demonstration of transgenic resistance to the nematodeRadopholus similisconferred on banana by a cystatin. Transgenic Res 13:135–142
Bakhetia M, Charlton W, Atkinson HJ, McPherson MJ (2005a) RNA Interference of dual oxidase in the plant nematodeMeloidogyne incognita. Mol Plant Microbe Interact 18:1099–1106
Bakhetia M, Charlton WL, Urwin PE, McPherson MJ, Atkinson HJ (2005b) RNA interference and plant-parasitic nematodes. Trends Plant Sci 10:362–367
Baldridge GD, O'Neill NR, Samac DA (1998) Alfalfa (Medicago sativaL) resistance to the root- lesion nematode,Pratylenchus penetrans: defense-response gene mRNA and isoflavonoid phytoalexin levels in roots. Plant Mol Biol 38:999–1010
Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction inC elegans. Cell 74:515–27
Baum TJ, Hiatt A, Parrot WA, Pratt H, Hussey RS (1996) Expression in tobacco of a functional monoclonal antibody specific to stylet secretions of the root-knot nematode. Mol Plant Microbe Interact 9:382–387
Beachy RN (2003) IP policies and serving the public. Science 299:473
Berg RH, Fester T, Taylor CG (2008) Development of the root-knot nematode feeding cell. Plant Cell Monogr., doi:10.1007/7089_2008_30
Bergamasco C, Bazzicalupo P (2006) Chemical sensitivity inCaenorhabditis elegans. Cell Mol Life Sci 63:1510–1522
Bertioli DJ, Smoker M, Burrows PR (1999) Nematode-responsive activity of the cauliflower mosaic virus 35S promoter and its subdomains. Mol Plant Microbe Interact 12:189–196
Bertioli DJ, Guimaraes PM, Jones JDG, Thomas CM, Burrows PR, Monte DC, Leal-Bertioli SCDeM (2001) Expression of tomatoCfgenes and their corresponding avirulence genes in transgenic tobacco plants using nematode responsive promoters. Ann Appl Biol 138:333–342
Bird DMcK, Opperman CH, Williamson VM (2008) Plant infection by roo-knot nematode. Plant Cell Monogr., doi:10.1007/7089_2008_31
Bockenhoff A, Grundler FM (1994) Studies on the nutrient uptake by the beet cyst nematodeHeterodera schachtiibyin situmicroinjection of fluorescent probes into the feeding structure inArabidopsis thaliana. Parasitol 109:249–254
Bockenhoff A, Prior DA, Grundler FM, Oparka KJ (1996) Induction of phloem unloading inArabidopsis thalianaroots by the parasitic nematodeHeterodera schachtii. Plant Physiol 112:1421–1427
Brady EB, Duffy M (1982) The value of plant resistance to soybean cyst nematodes: a case study of Forrest soybean. US Department of Agriculture, Natural Resources Economics Division, Washington DC
Bridge J, Plowright RA, Peng D (2005) Nematode parasites of rice. In: Luc M, Sikora RA, Bridge J (eds) Plant-parasitic nematodes in subtropical and tropical agriculture, pp 87–130. CAB International, Wallingford
Brookes G, Barfoot P (2005) GM crops: the global economic and environmental impact — the first nine years 1996–2004. Ag Bio Forum 8:187–196
Burrows PR, De Waele D (1997) Engineering resistance against plant-parasitic nematodes using anti-nematode genes. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant—nematode interactions, pp 217–236. Kluwer, Dordrecht
Cai D, Kleine M, Kifle S, Harloff H-J, Sandal NN, Marcker KA, Klein-Lankhorst RM, Salentijn EMJ, Lange W, Stiekema WJ, Wyss U, Grundler FMW, Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–834
Chen Q, Rehman S, Smant G, Jones JT (2005) Functional analysis of pathogenicity proteins of the potato cyst nematodeGlobodera rostochiensisusing RNAi. Mol Plant Microbe Interact 18:621–625
Chitwood DJ (2002) Phytochemical based strategies for nematode control. Annu Rev Phytopathol 40:221–249
Conkling MA, Opperman CH, Taylor CG Pathogen-resistant transgenic plants. United States Patent #5,750,386, May 12, 1998
Dale MFB, De Scurrah MM (1998) Breeding for resistance to the potato cyst nematodesGlobodera rostochiensisandGlobodera pallida: strategies, mechanisms, and genetic resources. In: Marks RJ, Brodie BB (eds) Potato cyst nematodes, biology, distribution, and control. CAB International, Wallingford, pp 167–195
Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A, Rosso MN, Abad P (2000) Nematode parasitism genes. Annu Rev Phytopathol 38:365–396
Davis EL, Hussey RS, Baum T (2004) Getting to the root of parasitism by nematodes. Trends Parasitol 20:134–141
Davis EL, Hussey RS, Baum TJ (2008) Parasitism genes: what they reveal about parasitism. Plant Cell Monogr., doi:10.1007/7089_2008_29
de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JL Jr, Inze D, Van Montagu M, Engler G, Gheysen G (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793–808
de Almeida Engler J, Favery B, Engler G, Abad P (2005) Loss of susceptibility as an alternative for nematode resistance. Curr Opin Biotechnol 16:112–117
De Meutter J, Robertson L, Parcy F, Mena M, Fenoll C, Gheysen G (2005) Differential activation ofABI3andLEAgenes upon plant-parasitic nematode infection.Mol Plant Path6:321–325
Doyle EA, Lambert KN (2002) Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematodeMeloidogyne javanica. Molec Plant-Microbe Interacts 15:549–56
Doyle EA, Lambert KN (2003)Meloidogyne javanicachorismate mutase 1 alters plant cell development. Mol Plant Microbe Interact 16:123–131
Dropkin VH (1989) Introduction to plant nematology. Wiley, New York
Dusenbery DB (1983) Chemotactic behavior of nematodes. J Nematol 15:168–173
Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136
Escobar C, Barcala M, Portillo M, Almoguera C, Jordano J, Fenoll C (2003) Induction of theHahsp177G4promoter by root-knot nematodes: involvement of heat-shock elements in promoter activity in giant-cells. Mol Plant Microbe Interact 12:1062–1068
Fanelli E, Di Vito M, Jones JT, De Giorgi C (2005) Analysis of chitin synthase function in a plant- parasitic nematode,Meloidogyne artellia. Gene 349:87–95
Favery B, Lecomte P, Gil N, Bechtold N, Bouchez D, Dalmasso A, Abad P (1998)RPE, a plant gene involved in early developmental steps of nematode feeding cells. Embo J 17:6799–6811
Fioretti L, Porter A, Haydock PJ, Curtis R (2002) Monoclonal antibodies reactive with secreted-excreted products from the amphids and the cuticle surface ofGlobodera pallidaaffect nema- tode movement and delay invasion of potato roots. Int J Parasitol 32:1709–1718
Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA inCaenorhabditis elegans. Nature 391:806–811
Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J (2000) Functional genomic analysis ofC eleganschromosome I by systematic RNA interference.Nature 408:325–330
Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001) Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematodeHeterodera glycines. Mol Plant Microbe Interact 14:1247–1254
Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2003) The parasitome of the phytone-matodeHeterodera glycines. Mol Plant Microbe Interact 16:720–726
Gao B, Allen R, Davis EL, Baum TJ, Hussey RS (2004) Developmental expression and biochemical properties of a beta-1,4-endoglycanase family in the soybean cyst nematode,Heterodera glycines. Mol Plant Path 5:93–104
Gheysen G, Fenoll C (2002) Gene expression in nematode feeding sites. Annu Rev Phytopathol 40:191–219
Gheysen G, Mitchum MG (2008) Molecular insights in the susceptible plant response to nematode infection. Plant Cell Monogr., doi:10.1007/7089_2008_35
Gilbert J, McGuire D (1956) Inheritance of resistance to severe root-knot fromMeloidogyne incognitain commercial type tomatoes. Proc Am Soc Hort Sci 68:437–442
Gleason CA, Liu QL, Williamson VM (2008) Silencing a candidate nematode effector gene corresponding to the tomato resistance geneMi-1leads to acquisition of virulence. Mol Plant Microbe Interact 21:576–585
Goddijn OJ, Lindsey K, van der Lee FM, Klap JC, Sijmons PC (1993) Differential gene expression in nematode-induced feeding structures of transgenic plants harbouring promoter-gusAfusion constructs. Plant J 4:863–873
Goellner M, Wang X, Davis E (2001) Endo-beta-1,4-glucanase expression in compatible plant—nematode interactions. Plant Cell 13:2241–2255
Goggin FL, Jia L, Shah G, Hebert S, Williamson VM, Ullman DE (2006) Heterologous expression of theMi-12 gene from tomato confers resistance against nematodes but not aphids in eggplants. Mol Plant Microbe Interact 19:383–388
Gonczy P, Echeverri C, Oegema K, Coulson A, Jones SJ, Copley RR, Duperon J, Oegema J, Brehm M, Cassin E, Hannak E, Kirkham M, Pichler S, Flohrs K, Goessen A, Leidel S, Alleaume AM, Martin C, Ozlu N, Bork P, Hyman AA (2000) Functional genomic analysis of cell division inC elegansusing RNAi of genes on chromosome III. Nature 408:331–336
Goverse A, Biesheuvel GJ, Gommers FJ, Bakker J, Schots A, Helder J (1998) In planta monitoring of the activity of two constitutive promoters, CaMV 35S and TR2, in developing feedingcells induced byGlobodera rostochiensisusing green fluorescent protein in combination with confocal laser scanning microscopy. Physiolog Mol Plant Path 52:275–284
Griffitts JS, Whitacre JL, Stevens DE, Aroian RV (2001) Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 293:860–863
Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B, Morris H, Cremer PS, Dell A, Adang MJ, Aroian RV (2005) Glycolipids as receptors forBacillus thuringiensiscrystal toxin.Science 307:922–925
Hammes UZ, Schachtman DP, Berg RH, Nielsen E, Koch W, McIntyre LM, Taylor CG (2005) Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol Plant Microbe Interact 12:1247–1257
Haydock PPJ, Woods SR, Grove IG, Hare MC (2006) Chemical control of nematodes. In: Perry RN, Moens M (eds) Plant nematology. CAB International, Wallingford, pp 392–410
Hilliard MA, Bargmann CI, Bazzicalupo P (2002)C elegansresponds to chemical repellents by integrating sensory inputs from the head and the tail. Curr Biol 12:730–740
Hoth S, Schneidereit A, Lauterbach C, Scholz-Starke J, Sauer N (2005) Nematode infection triggers the de novo formation of unloading phloem that allows macromolecular trafficking of green fluorescent protein into syncytia. Plant Physiol 138:383–392
Huang G, Allen R, Davis EL, Baum TJ, Hussey RS (2006a) Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc Natl Acad Sci USA 103:14302–14306
Huang G, Dong R, Allen R, Davis EL, Baum TJ, Hussey RS (2006b) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe Interact 19:463–470
Huang G, Gao B, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematodeMeloidogyne incognita. Mol Plant Microbe Interact 16:376–381
James C (2005) Executive summary of global status of commercialized biotech/GM crops: ISAAA briefs. International service for the acquisition of agri-biotech applications, Ithaca,NY, pp 1–12
Jammes F, Lecomte P, de Almeida Engler J, Bitton F, Martin-Magniette M-L, Renou JP, Abad P,Favery B (2005) Genome-wide expression profiling of the host response to root-knot nema-tode infection in Arabidopsis. Plant J 44:447–458
Jaubert S, Ledger TN, Laffaire JB, Piotte C, Abad P, Rosso MN (2002) Direct identification of stylet secreted proteins from root-knot nematodes by a proteomic approach. Mol Biochem Parasitol 121:205–211
Jaubert S, Milac AL, Petrescu AJ, de Almeida Engler J, Abad P, Rosso MN (2005) In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Mol Plant Microbe Interact 12:1277–1284
Jobling S, Jarman C, Teh M, Holmberg N, Blake C, Verhoeyen M (2003) Immunomodulcation of enzyme function in plants by single-domain antibody fragments. Nat Biotechnol 21:77–80
Johnson AW (1985a) The role of nematicides in nematode management. In: Sasser JN, Carter CC (eds) An advanced treatise onMeloidogyne. North Carolina State University Graphics,Raleigh, North Carolina, pp. 249–267
Johnson AW (1985b) Specific crop rotation effects combined with cultural practices and nemati-cides. In: Sasser JN, Carter CC (eds) An advanced treatise onMeloidogyne. North Carolina State University Graphics, Raleigh, North Carolina, pp. 283–301
Juergensen K, Scholz-Starke J, Sauer N, Hess P, van Bel AJE, Grundler FMW (2003) The companion cell-specific Arabidopsis disaccharide carrier AtSUC2 is expressed in nematode-induced syncytia. Plant Physiol 131:61–69
Jung C, Cai D, Kleine M (1998) Engineering nematode resistance in crop species. Trends Plant Sci 3:266–271
Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of theCaenorhabditis elegansgenome using RNAi. Nature 421:231–237
Kaplan DT, Keen NT (1980) Mechanisms conferring plant incompatibility to nematodes. Revue de Nematologie 3:123–134
Klink VP, Alkharouf N, MacDonald M, Matthews B (2005) Laser capture microdissection (LCM) and expression analyses ofGlycine max(soybean) syncytium containing root regions formed by the plant pathogenHeterodera glycines(soybean cyst nematode). Plant Mol Biol 59:965–979
Koenning SR, Overstreet C, Noling JW, Donald PA, Becker JO, Fortnum BA (1999) Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J Nematol 31:587–618
Li X-Q, Wei J-Z, Tan A, Aroian RV (2007) Resistance to root-knot nematode in tomato roots expressing a nematicidalBacillus thuringiensiscrystal protein. Plant Biotech J 5:455–464
Li L, Fester T, Taylor CG (2008) Transcriptomic analysis of nematode infestation. Plant Cell Monogr., doi:10.1007/7089_2008_36
Lilley CJ, Devlin P, Urwin PE, Atkinson HJ (1999a) Parasitic nematodes, proteinases and trans- genic plants. Parasitol Today 15:414–417
Lilley CJ, Urwin PE, Atkinson HJ (1999b) Characterization of plant nematode genes: identifying targets for a transgenic defence. Parasitol 118:S63–S72
Lilley CJ, Goodchild SA, Atkinson HJ, Urwin PE (2005) Cloning and characterization of aHeterodera glycinesaminopeptidase cDNA. Int J Parasitol 35:1577–1585
Liu B, Hibbard JK, Urwin PE, Atkinson HJ (2005) The production of synthetic chemodisruptive peptides in planta disrupts the establishment of cyst nematodes. Plant Biotech J 3:487–496
Luc M, Bridge J, Sikora RA (2005a) Reflections on nematology in subtropical and tropical agriculture. In: Luc M, Sikora RA, Bridge J (eds) Plant-parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp. 1–10
Luc M, Sikora RA, Bridge J (2005b) Plant-parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford
Maeda I, Kohara Y, Yamamoto M, Sugimoto A (2001) Large-scale analysis of gene function inCaenorhabditis elegansby high-throughput RNAi. Curr Biol 11:171–176
Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ (2003) Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol 53:513–530
Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ (2004) Homologous soybean and Arabidopsis genes share responsiveness to cyst nematode infection. Mol Plant Path 5:409–423
McCarter JP (2004) Genomic filtering: an approach to discovering novel antiparasitics. Trends Parasitol 20:462–468
McCarter J, Dautova Mitreva M, Martin J, Dante M, Wylie T, Rao U, Pape D, Bowers Y, Theising B, Murphy CV, Kloek AP, Chiapelli BJ, Clifton SW, Bird DMcK, Waterston R (2003) Analysis and functional classification of transcripts from the nematodeMeloidogyne incognita. Genome Biol. 4:R26:1–19
McCarter JP, Bird DM, Mitreva M (2005) Nematode gene sequences: update for December 2005. J Nematol 37:417–421
McClure MA (1988) Lectin binding sites on the amphidial exudates ofMeloidogyne. J Nematol 20:321–326
McDonald AH, Nicol JM (2005) Nematode parasites of cereals. In: Luc M, Sikora RA, Bridge J (eds) Plant-parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp. 131–191
McPherson MJ, Urwin PE, Lilley CJ, Atkinson HJ (1997) Engineering plant nematode resistance by antifeedants. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant—nematode interactions. Kluwer, Dordrecht, pp 237–249.
McSorley R, Arnett JD, Bost SC, Carter WW, Hafez S, Johnson AW, Kirkpatrick T, Nyczepir AP, Radewald JD, Robinson AF, Schmitt DP (1987) Bibliography of estimated crop losses in the United States due to plant-parasitic nematodes. Ann Appl Nem 1:6–12
Mello CC, Conte D (2004) Revealing the world of RNA interference.Nature431:338–342
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root-knot nematode resistance geneMifrom tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319
Mitreva M, Elling AA, Dante M, Kloek AP, Kalyanaraman A, Aluru S, Clifton SW, Bird DMcK, Baum TJ, McCarter JP (2004) A survey of SL1-spliced transcripts from the root-lesion nema-todePratylenchus penetrans. Mol Gen Genomics 272:138–148
Mitreva M, Blaxter ML, Bird DMcK, McCarter JP (2005) Comparative genomics of nematodes. Trends Genet 21:573–581
Mitreva-Dautova M, Roze E, Overmars H, de Graaff L, Schots A, Helder J, Goverse A, Bakker J, Smant G (2006) A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematodeMeloidogyne incognita. Mol Plant Microbe Interact 19:521–529
Monson M, Schmitt DP (2004) Economics. In: Schmitt DP, Wrather JA, Riggs RD (eds) Biology and management of soybean cyst nematode. Schmitt and Associates, Marceline, pp 41–53
Ohl SA, van der Lee FM, Sijmons PC (1997) Anti-feeding structure approaches to nematode resistance. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant—nematode interactions. Kluwer, Dordrecht, pp 250–261
Olsen AN, Skriver K (2003) Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends Plant Sci 8:55–57
Opperman CH, Taylor CG, Conkling MA (1994) Root-knot nematode directed expression of a plant root-specific gene. Science 263:221–223
Opperman CH, Bird DMcK, Schaff JE (2008) Genomic analysis of the root-knot nematode genome. Plant Cell Monogr., doi:10.1007/7089_2008_37
Paal J, Henselewski H, Muth J, Meksem K, Menendez CM, Salamini F, Ballvora A, Gerbhardt C (2004) Molecular cloning of the potatoGro1-4gene conferring resistance to pathotype Ro1 of the root cyst nematodeGlobodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297
Padgham JL, Duxbury JM, Mazid AM, Abawi GS, Hossain M (2004) Yield loss caused byMeloidogyne graminicolaon lowland rainfed rice in Bangladesh. J Nematol 36:42–48
Parkinson J, Mitreva M, Whitton C, Thomson M, Daub J, Martin J, Hall N, Barrell B, Waterston RH, McCarter JP, Blaxter M (2004) A transcriptomic analysis of the phylum Nematoda. Nature Genetics 36:1259–1267
Perry RN (1998) The physiology and sensory perception of potato cyst nematodes,Globoderaspecies. In: Marks RJ, Brodie BB (eds) Potato cyst nematodes, biology, distribution and control. CAB International, Wallingford
Perry RN, Moens M (2006) Plant nematology. CAB International, Wallingford
Popeijus H, Overmars HA, Jones JT, Blok VC, Goverse A, Helder J, Schots A, Bakker J, Smant G (2000) Degradation of plant cell walls by a nematode. Nature 406:36–37
Prins M, Lohuis D, Schots A, Goldbach R (2005) Phage display-selected single-chain antibodies confer high levels of resistance against tomato spotted wilt virus. J Gen Virology 86:2107 – 2113
Prot JC (1980) Migration of plant-parasitic nematodes toward plant roots. Revue de Nematologie 3:305–318
Qin L, Overmars H, Helder J, Popeijus H, van der Voort JR, Groenink W, van Koert P, Schots A, Bakker J, Smant G (2000) An efficient cDNA-AFLP-based strategy for the identification of putative pathogenicity factors from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact 13:830–836
Qin L, Kudla U, Roze EH, Goverse A, Popeijus H, Nieuwl J, Overmars H, Jones JT, Schots A,Smant G, Bakker J, Helder J (2004) Plant degradation: a nematode expansin acting on plants. Nature 427:30
Rasmann S, Kollner T, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings T (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737
Rich JR, Kavitha PG (2006) Evaluation of Avicta and N-Hibit seed treatments for management of reniform nematodes on cotton in north Florida, 2005. Fungicide and Nematicide Tests 61
Rich JR, Keen NT, Thomason IJ (1977) Association of coumestans with the hypersensitivity of lima bean roots toPratylenchus scribneri. Physio Plant Path 10:105–116
Riddle DL, Bird AF (1985) Responses of the plant-parasitic nematodesRotylenchulus reniformis,Anguina agrostis, andMeloidogyne javanicato chemical attractants. Parasitol 91:185–195
Risher JF, Mink FL, Stara JF (1987) The toxicologic effects of the carbamate insecticide aldicarb in mammals: a review. Environ Health Perspect 72:267–281
Roberts PA (2002) Concepts and consequences of resistance. In: Starr JL, Cook R, Bridge J (eds) Plant resistance to parasitic nematodes. CAB International, Wallingford, pp 23–41
Robinson AF (1995) Optimal release rates for attractingMeloidogyne incognita,Rotylenchulus reniformis, and other nematodes to carbon dioxide in sand. J Nematol 27:42–50
Robinson AF (2002) Reniform nematodes:Rotylenchulusspecies. In: Starr JL, Cook R, Bridge J (eds) Plant resistance to parasitic nematodes. CAB International, Wallingford, pp 153–174
Rosso M, Schouten A, Roosien J, Borst-Vrenssen T, Hussey RS, Gommers F, Bakker J, Schots A, Abad P (1996) Expression and functional characterization of a single chain Fv antibody directed against secretions involved in plant nematode infection process. Biochem Biophys Res Commun 220:255–263
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 Microbe Interact 18:615–620
Ruben E, Jamai A, Afzal J, Njiti VN, Triwitayakorn K, Iqbal MJ, Yaegashi S, Bashir R, Kazi S, Arelli P, Town CD, Ishihara H, Meksem K, Lightfoot DA (2006) Genomic analysis of therhg1locus: candidate genes that underlie soybean resistance to the cyst nematode. Mol Genet Genomics 276:503–516
Sankula S, Marmon G, Blumenthal E (2005) Biotechnology-derived crops planted in 2004—Impacts on US Agriculture. National Center for Food and Agricultural Policy, Washington DC
Sasser JN, Freckman DW (1987) A world perspective on nematology: the role of the society. In: Veech JA, Dickson DW (eds) Vistas on nematology. Society of Nematology, Hyattsville, Maryland, pp 7–14
Schneider SM, Rosskopf EN, Leesch JG, Chellemi DO, Bull CT, Mazzola M (2003) United States Department of Agriculture – Agricultural Research Service research on alternatives to methyl bromide: pre-plant and post-harvest. Pest Manag Sci 59:814–826
Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Fieitelson J, Zeigler DR, Dean DH (1998)Bacillus thuringiensisand its pesticidal crystal proteins. Microbiol Molec Biol Rev 62:775–806
Schnepf EH, Schwab GE, Payne J, Narva KE, Foncerrada L (2003) Nematicidal proteins. Mycogen Corporation, USA
Scholl EH, Thorne JL, McCarter JP, Bird DMcK (2003) Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach. Genome Biol 4:R39
Serageldin I (1999) Biotechnology and food security in the 21st century.Science285:387–389
Shurtleff MC, Averre CW (2000) Diagnosing plant diseases caused by nematodes. American Phytopatholog Soci Press, St Paul
Sikora RA, Bridge J, Starr JL (2005) Management practices: an overview of integrated nematode management technologies. In: Luc M, Sikora RA, Bridge J (eds) Plant-parasitic nematodes in subtropical and tropical agriculture. CAB International, Wallingford, pp 793–825
Slutsky M, Levin JL, Levy BS (1999) Azoospermia and oligospermia among a large cohort of DBCP applicators in 12 countries. Int J Occup Environ Health 5:116–122
Smant G, Stokkermans JP, Yan Y, de Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA 95:4906–4911
Soriano IR, Asenstorfer RE, Schmidt O, Riley IT (2004a) Inducible flavone in oats (Avena sativa) is a novel defense against plant-parasitic nematodes. Phytopathol 94:1207–1214
Soriano IR, Riley IT, Potter MJ, Bowers WS (2004b) Phytoecdysteroids: a novel defense against plant-parasitic nematodes. J Chem Ecol 30:1885–1899
Starr JL, Bridge J, Cook R (2002a) Resistance to plant-parasitic nematodes: history, current use and future potential. In: Starr JL, Cook R, Bridge J (eds) Plant resistance to parasitic nema- todes. CAB International, Wallingford, pp 1–22
Starr JL, Cook R, Bridge J (2002b) Plant resistance to parasitic nematodes. CAB International, Wallingford
Stepek G, Behnke JM, Buttle DJ, Duce IR (2004) Natural plant cysteine proteinases as anthelmintics? Trends Parasitol 20:322–327
Stiekema WJ, Bosch D, Wilmink A, de Boer JM, Schouten A, Roosien J, Goverse A, Smant G, Stokkermans J, Gommers FJ, Schots A, Bakker J (1997) Towards plantibody-mediated resistance against nematodes. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant—nematode interactions. Kluwer, Dordrecht, pp 262–271
Stoger E, Sack M, Fischer R, Christou P (2002) Plantibodies: applications, advantages, and bottlenecks. Curr Opin Biotechnol 13:161–166
Taylor AL (1978) Nematocides and nematicides — history http://flnemifasufledu/HISTORY/ nematicide_hishtm TheC. elegansSequencing Consortium (1998) Genome sequence of the nematodeC elegans: A platform for investigating biology. Science 282:2012–2018
Thomas CM, Cottage A (2006) Genetic engineering for resistance. In: Perry RN, Moens M (eds) Plant nematology. CAB International, Wallingford, pp 255–272
Thurau T, Kifle S, Jung C, Cai D (2003) The promoter of the nematode resistance geneHs1pro-1activates a nematode-responsive and feeding site specific gene expression in sugar beet (Beta vulgarisL) andArabidopsis thaliana. Plant Mol Biol 52:643–660
Tilman D, Fargione J, Wolff B, D'Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284
Tomczak A, Koropacka K, Smant G, Goverse A, Bakker E (2008) Resistant plant responses. Plant Cell Monogr., doi:10.1007/7089_2008_39
Trudgill DL, Evans K, Phillips MS (1998) Potato cyst nematodes: damage mechanisms and tolerance in potato. In: Marks RJ, Brodie BB (eds) Potato cyst nematodes, biology, distribution, and control. CAB International, Wallingford, pp 117–133
Tytgat T, Vanholme B, De Meutter J, Claeys M, Couvreur M, Vanhoutte I, Gheysen G, Van Criekinge W, Borgonie G, Coomans A, Gheysen G (2004) A new class of ubiquitin extension proteins secreted by the dorsal pharyngeal gland in plant-parasitic cyst nematodes. Mol Plant Microbe Interact 17:846–852
Urwin PE, Atkinson HJ, Waller DA, McPherson MJ (1995) Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance toGlobodera pallida. Plant J 8:121–131
Urwin PE, Lilley CJ, McPherson MJ, Atkinson HJ (1997a) Resistance to both cyst and root-knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant J 12:455–461
Urwin PE, Moller SG, Lilley CJ, McPherson MJ, Atkinson HJ (1997b) Continual green-fluorescent protein monitoring of cauliflower mosaic virus 35S promoter activity in nematode-induced feeding cells inArabidopsis thaliana. Mol Plant Microbe Interact 10:394–400
Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference.Molec Plant-Microbe Interacts15:747–752
Vaghchhipawala ZE, Schlueter JA, Shoemaker RC, Mackenzie SA (2004) SoybeanFGAMsyn-thase promoters direct ectopic nematode feeding site activity. Genome 47:404–413
Valette C, Andary C, Geiger JP, Sarah JL, Nicole M (1998) Histochemical and cytochemical investigations of phenols in roots of banana infected by the burrowing nematodeRadopholus similis. Phytopathol 88:1141–1148
van der Vossen EA, van der Voort JN, Kanyuka K, Bendahmane A, Sandbrink H, Baulcombe DC,Bakker J, Stiekema WJ, Klein-Lankhorst RM (2000) Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J 23:567–576
Van Pouche K, Karimi M, Gheysen G (2001) Analysis of nematode-responsive promoters in sugar beet hairy roots. Meded Rijksuniv Gent Fak Landbouwkd Toegep Biol Wet 66:591–598
Vanholme B, De Meutter J, Tytgat T, Van Montagu M, Coomans A, Gheysen G (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332:13–27
Vanholme B, Mitreva M, Van Criekinge W, Logghe M, Bird DMcK, McCarter JP, Gheysen G (2006) Detection of putative secreted proteins in the plant-parasitic nematodeHeterodera schachtii. Parasitol Res 98:414–424
Veech JA, McClure MA (1977) Terpenoid aldehydes in cotton roots susceptible and resistant to the root-knot nematode,Meloidogyne incognita. J Nematol 9:225–229
Vishnudasan D, Tripathi MN, Rao U, Khurana P (2005) Assessment of nematode resistance in wheat transgenic plants expressing potato proteinase inhibitor (PIN2) gene. Transgenic Res 14:665–675
Vogel J, Raab TK, Schiff C, Somerville SC (2002)PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14:2095–2106
Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomatoMi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16:1365–1369
Wang X, Mitchum MG, Gao B, Li C, Diab H, Baum TJ, Hussey RS, Davis EL (2005) A parasitism gene from a plant-parasitic nematode with function similar toCLAVATA3/ESR(CLE) ofArabidopsis thaliana. Mol Plant Path 6:187–191
Waterhouse PM, Graham MW, Wang MB (1998) Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA 95:13959–13964
Watts V (1947) The use ofLycopersicon peruvianumas a source of nematode resistance in tomatoes. Proc Am Soc Hort Sci 49:233
Weerasinghe RR, Bird DM, Allen NS (2005) Root-knot nematodes and bacterial Nod factors elicit common signal transduction events inLotus japonicusroot hair cells. Proc Natl Acad Sci USA 102:3147–3152
Wei J-Z, Hale K, Carta L, Platzer E, Wong C, Fang S-C, Aroian RV (2003)Bacillus thuringiensiscrystal proteins that target nematodes. Proc Natl Acad Sci USA 100:2760–2765
Whitehead AG (1998) Plant nematode control. CABI International, New York
Williamson VM (1999) Plant nematode resistance genes. Curr Opin Plant Biol 2:327–331
Williamson VM, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745
Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403
Winter MD, McPherson MJ, Atkinson HJ (2002) Neuronal uptake of pesticides disrupts chemo-sensory cells of nematodes. Parasitol 125:561–565
Wyss U (1997) Root parasitic nematodes: an overview. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant—nematode interactions. Kluwer, Dordrecht, pp 5–22
Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 148:219–222
Yoon Y, Kim E, Hwang Y, Choi C (2004) Avermectin: biochemical and molecular basis of its biosynthesis and regulation. Appl Microbiol Biotechnol 63:626–634
Young ND, Mudge J (2002) Marker-assisted selection for soybean cyst nematode resistance. In: Starr JL, Cook R, Bridge J (eds) Plant resistance to parasitic nematodes. CAB International, Wallingford, pp 241–252
Zijlstra C, Blok VC, Phillips MS (1997) Natural resistance: the assessment of variation in virulence in biological and molecular terms. In: Fenoll C, Grundler FMW, Ohl SA (eds) Cellular and molecular aspects of plant—nematode interactions. Kluwer, Dordrecht, pp 153–166
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
McCarter, J.P. (2009). Molecular Approaches Toward Resistance to Plant-Parasitic Nematodes. In: Berg, R.H., Taylor, C.G. (eds) Cell Biology of Plant Nematode Parasitism. Plant Cell Monographs, vol 15. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-85215-5_9
Download citation
DOI: https://doi.org/10.1007/978-3-540-85215-5_9
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-85213-1
Online ISBN: 978-3-540-85215-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)