Engineering Plants for Nematode Resistance

Annual Review of Phytopathology

Volumn 41, Issue , 2003, Pages 615-639

  Atkinson, Howard J ^a   Urwin, Peter E ^a   McPherson, Michael J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Inhibitor; Promoter; Protease; RNAi; Transgenic

Indexed keywords

ANIMALS; NEMATODA; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEASE INHIBITORS; RNA INTERFERENCE;

EID: 0242406734     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.phyto.41.052002.095737     Document Type: Review

References (138)

1. Abe K, Emori Y, Kondo H, Suzuki K, Arai S. 1987. Molecular cloning of a cysteine protease inhibitor of rice (Oryzacystatin). J. Biol. Chem. 262:16793-97
2. Arai S, Matsumoto I, Emori Y, Abe K. 2002. Plant seed cystatins and their target enzymes of endogenous and exogenous origin. J. Agric. Food Chem. 50:6612-61
3. Astwood JD, Leach JN, Fuchs RL. 1996. Stability of food allergens to digestion in vitro. Nat. Biotech. 14:1269-73
4. Atkinson HJ. 1993 Opportunities for improved control of plant parasitic nematodes via plant biotechnology. In Opportunities for Molecular Biology in Crop Production, ed. DJ Beadle, DHL Bishop, LG Copping, GK Dixon, DW Holloman, pp. 257-66. Bracknell, UK: Br. Crop Prot. Counc.
5. Awade AC. 1996. On hen egg fractionation: application of liquid chromatography to the isolation and purification of hen egg white and egg yolk proteins. Z. Lebensm. Unters. Forsch. 202:1-14
6. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP. 1997. Signaling in plant-microbe interactions. Science 276: 726-33
7. Barthels N, van der Lee FM, Klap J, Goddijn OJM, Karimi M, et al. 1997. Regulatory sequences of Arabidopsis drive reporter gene expression in nematode feeding structures Plant Cell 9:2119-34
8. Baulcombe D. 1999. Viruses and gene silencing in plants. Arch. Virol. Suppl. 15:189-201
9. Baulcombe D. 2002. RNA silencing. Curr. Biol. 12:R82-84
10. Benfey PN, Chua N-H. 1989. Regulated genes in transgenic plants. Science 24:174-81
11. Benfey PN, Ren L, Chua N-H. 1989. The CaMV35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J. 8:2195-202
12. Betz FS, Hammond BG, Fuchs RL. 2000. Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regul. Toxicol. Pharmacol. 32:156-73
13. Birch ANE, Geoghegan IE, Majerus MEN, McNicol JW, Hackett CA, et al. 1999. Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol. Breed. 5:75-83
14. Böckenhoff A, Grundler FMW. 1994. Studies on the nutrient uptake of the beet cyst nematode H. schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana. Parasitology 109:249-54
15. Bonas U, Lahaye T. 2002. Plant disease resistance triggered by pathogenderived molecules: refined models of specific recognition. Curr. Opin. Microbiol. 5:44-50
16. Borgonie G, Claeys M, Leyns F, Arnaut G, De Waele, Coomans DA. 1996. Effect of nematicidal Bacillus thuringiensis strains on free-living nematodes. 1. Light microscopic observations, species and biological stage specificity and identification of resistant mutants of Caenorhabditis elegans. Fund. Appl. Nematol. 19:391-98
17. Breviario D, Nick P. 2000. Plant tubulins: a melting pot for basic questions and promising applications. Transgenic Res. 9:383-93
18. Broadway RM. 1995. Are insects resistant to plant protease inhibitors? J. Insect Physiol. 41:107-16
19. Burrows PR, de Waele D. 1997. Engineering resistance against plant parasitic nematodes using antinematode genes. See Ref. 36a, pp. 217-36
20. Burrows RP, Barker ADP, Newell CA, Hamilton WDO. 1998. Plant-derived enzyme inhibitors and lectins for resistance against plant-parasitic nematodes in transgenic crops. Pestic. Sci. 52:176-83
21. Cai DG, Kleine M, Kifle S, Harloff HJ, Sandal NN. et al. 1997. Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832-34
22. Christensen AH, Quail PH. 1996. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants Transgenic Res. 5:213-18
23. Couty A, Down RE, Gatehouse AMR, Kaiser L, Pham-Delegue MH, Poppy GM. 2001. Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae). J. Insect Physiol. 47:1357-66
24. Cowgill SE, Atkinson HJ. 2003. A sequential approach to risk assessment of transgenic plants expressing protease inhibitors: effects on non-target herbivorous insects. Transgenic Res. In press
25. Cowgill SE, Bardgett RD, Kiezebrink DT, Atkinson HJ. 2002. The effect of transgenic nematode resistance on nontarget organisms in the potato rnizosphere. J. Appl. Ecol. 39:915-923
26. Cowgill SE, Wright C, Atkinson HJ. 2002. Transgenic potatoes with enhanced levels of nematode resistance do not have altered susceptibility to nontarget aphids. Mol. Ecol. 11:821-27
27. Devidas P, Rehberger LA. 1992. The effects of exotoxin Thuringiensin from Bacillus thuringiensis on Meloidogyne incognita and Caenorhabditis elegans. Plant Soil 145:115-20
28. Douches DS, KishaTJ, Coombs JJ, Li W, Pett WL, Grafius EJ. 2001. Effectiveness of natural and engineered host plant resistance in potato to the Colorado potato beetle. Hortscience 36:967-70
29. Down RE, Ford L, Woodhouse SD, Raemaekers RJM, Leitch B, et al. 2000. Snowdrop lectin (GNA) has no acute toxic effects on a beneficial insect predator, the 2-spot ladybird (Adalia bipunctata L.). J. Insect Physiol. 46:379-91
30. Dure L. 1993. The Lea proteins of higher plants. In Control of Plant Gene Expression ed. DPS Verma, pp. 325-35. Boca Raton, FL: CRC Press
31. Dürschner-Pelz U, Atkinson HJ. 1988. Recognition of Ditylenchus and other nematodes by spores of the endoparasitic fungus Verticillium balanoides. J. Invertebr. Pathol. 51:97-106
32. Ellis JG, Lawrence GJ, Luck JE, Dodds PN. 1999. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11:495-506
33. Environ. Prot. Agency (EPA). 1999. International Pesticide Notice. http://www. epa.gov/oppfead1/17b/aldicarb.htm
34. Environ. Prot. Agency (EPA). 2001. FIFRA Scientific Advisory Panel (SAP) open meeting, July 17-18. http://www. epa.gov/oscpmont/sap/2001/july/agency positionpaper.pdf
35. 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. 31:127-36
36. Deleted in proof
37. 36a. Fenoll C, Grundler FMW, Ohl SA, eds. 1997. Cellular and Molecular Aspects of Plant-Nematode Interactions. Dordrecht: Kluwer
38. Fernandes KVS, Sabelli PA, Barratt DHP, Richardson M. 1993. The resistance of cowpea seeds to bruchid beetles is not related to levels of cysteine protease inhibitors. Plant Mol. Biol. 23:215-19
39. Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-11
40. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J. 2000. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408:325-30
41. Fu T-J. 2002. Digestion stability as a criterion for protein allergenicity assessment. Ann. NY Acad. Sci. 964:99-110
42. Goddijn OJM, Lindsey K, van der Lee FM, Klap JC, Sijmons PC. 1993. Differential gene expression in nematode-induced feeding structures of transgenic plants harbouring promoter-gusA fusion constructs. Plant J. 4:863-73
43. Goggin FL, Williamson VM, Ullman DE. 2001. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environ. Entomol. 30:101-6
44. Gonczy P, Echeverri C, Oegema K, Coulson A, Jones SJM, et al. 2000. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408:331-36
45. Goverse A, Biesheuvel J, Wijers GJ, Gommers FJ, Bakker J, et al. 1998. In planta monitoring of the activity of two constitutive promoters, CaMV 35S and TR2′, in developing feeding cells induced by Globodera rostochiensis using green fluorescent protein in combination with confocal laser scanning microscopy. Physiol. Mol. Plant Pathol. 52:275-84
46. Green J, Vain P, Fearnehough MT, Worland B, Snape JW, Atkinson HJ. 2002. Analysis of the expression patterns of the Arabidopsis thaliana tubulin-1 and Zea mays ubiquitin-1 promoters in rice plants in association with nematode infection. Physiol. Mol. Plant Pathol. 60:197-205
47. Grundler FMW, Böckenhoff A. 1997. Physiology of nematode feeding and feeding sites. See Ref. 36a, pp. 107-19
48. Gubba A, Gonsalves C, Stevens MR, Tricoli DM, Gonsalves D. 2002. Combining transgenic and natural resistance to obtain broad resistance to tospovirus infection in tomato (Lycopersicon esculentum mill). Mol. Breed. 9:13-23
49. Hamilton AJ, Baulcombe DC. 1999. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950-52
50. Hammond-Kosack KE, Jones JDG. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:575-607
51. Hansen E, Harper G, McPherson MJ, Atkinson HJ. 1996. Differential expression patterns of the wound-inducible transgene wun1-uidA in potato roots following infection with either cyst or root-knot nematodes. Physiol. Mol. Plant Pathol. 48:161-70
52. Harkett P. 1996. Commercial prospects of the PCN problem. SOEFD Rev. Meet. Potato Nematode, Feb. 1-2. (Abstr.)
53. Hartley MR, Chaddock JA, Bonness MS. 1996. The structure and function of ribosome-inactivating proteins. Trends Plant Sci. 1:254-60
54. Hartley MR, Lord JM. 1993. Structure, function and applications of ricin related cytotoxic proteins. In Biosynthesis and Manipulation of Plant Products, ed. D Grierson, pp. 210-39. Glasgow: Chapman & Hall
55. Hartley RW. 1988. Barnase and barstar - expression of its cloned inhibitor permits expression of a cloned ribonuclease. J. Mol. Biol. 202:913-15
56. Hepher A, Atkinson HJ. 1992. Nematode Control with Protease Inhibitors. Eur. Patent No. 0 502 730 A1
57. Hilder VA, Gatehouse AMR, Sheerman SE, Barker RF, Boulter D. 1987. A novel mechanism of insect resistance engineered into tobacco. Nature 330:160-63
58. Hilder VA, Powell KS, Gatehouse AMR, Gatehouse JA, Shi Y, et al. 1995. Expression of snowdrop lectin in transgenic tobacco plants results in added protection against aphids. Transgenic Res. 4:18-25
59. Hoffmann MP, Zalom FG, Wilson LT, Smilanick JM, Malyj LD, et al. 1992. Field evaluation of transgenic tobacco containing genes encoding Bacillus thuringiensis δ endotoxin or cowpea trypsin inhibitor: efficacy against Helicoverpera zea (Lepidoptera: Noctuidae). J. Econ. Entomol. 85:2516-22
60. Holm H, Jorgensen A, Hanssen LE. 1991. Raw soy and purified protease inhibitors induce the appearance of inhibitor-resistant trypsin and chymotrypsin activities in Wistar rat duodenal juice. J. Nutr. 121:532-38
61. Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM. 2000. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12:1319-29
62. Hwang I, Goodman HM. 1995. An Arabidopsis thaliana root-specific kinase homolog is induced by dehydration, ABA and NaCl. Plant J. 8:37-43
63. Jongsma M, Jung A, Bakker PL, Peters J, Bosch D, Stiekema WJ. 1995. Adaptation of Spodoptera exigua larvae to plant protease inhibitors by induction of gut protease activity insensitive to inhibition. Proc. Natl. Acad. Sci. USA 92:8041-45
64. Jongsma MA, Stiekema WJ, Bosch D. 1996. Combating inhibitor-insensitive proteases of insect pests. Trends Biotechnol. 14:331-33
65. Kaplan DT, Davis EL. 1991. A bioassay to estimate root penetration by nematodes. J. Nematol. 23:446-50
66. Keller B, Baumgartner C. 1991. Vascular-specific expression of the bean GRP 1.8 gene is negatively regulated. Plant Cell 3:1051-61
67. Kobe B, Deisenhofer J. 1995. Proteins with leucine-rich repeats. Curr. Opin. Struct. Biol. 5:409-16
68. Kondo H, Abe K, Emori Y, Arai S. 1991. Gene organisation of oryzacystatin-II, a new cystatin superfamily member of plant origin, is closely related to that of oryzacystatin-I but different from those of animal cystatins. FEBS Lett. 278:87-90
69. Kondo H, Abe K, Nishimura I, Watanabe H, Emori Y, Arai S. 1990. Two distinct cystatin species in rice seeds with different specificities against cysteine proteases. J. Biol. Chem. 265:15832-37
70. Koritsas VM, Atkinson HJ. 1994. Proteases of females of the phytoparasite Globodera pallida (potato cyst nematode). Parasitology 109:357-65
71. Kouzuma Y, Kawano K, Kimura M, Yamasaki N, Kadowaki T, Yamamoto K. 1996. Purification characterization, and sequencing of two cysteine protease inhibitors, Sea and Scb, from sunflower (Helianthus annuus) seeds. J. Biochem. 119:1106-13
72. Kraus TW, Eble MJ, Raeth U. 1994. Developments and current status of adjuvant chemo-and radiotherapy for colorectal cancer. Langenbecks Arch. Chir. 379:353-57
73. Kuiper HA, Kleter GA, Noetborn HPJM, Kok EJ. 2001. Assessment of the food safety issues related to genetically modified foods. Plant J. 27:503-28
74. Lambert KN, Ferrie BJ, Nombela G, Brenner ED, Williamson VM. 1999. Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection. Physiol. Mol. Plant Pathol. 55:341-48
75. Lilley CJ, Atkinson HJ. 1997. Promoters for control of root-feeding nematodes. UK Patent Applic. No. 9524395.2
76. Lilley CJ, Urwin, PE, Atkinson HJ, McPherson MJ. 1997. Characterisation of cDNAs encoding serine proteases from the soybean cyst nematode Hetemdera glycines. Mol. Biochem. Parasitol. 89:195-207
77. Lilley CJ, Urwin PE, McPherson MJ, Atkinson HJ. 1996. Characterisation of intestinally active proteases of cystnematodes. Parasitology 113:415-24
78. Logemann J, Schell J. 1989. Nucleotide sequence and regulated expression of a wound-inducible potato gene. Mol. Gen. Genet. 219:81-88
79. Losey J, Raynor L, Carter ME. 1999. Transgenic pollen harms Monarch larvae. Nature 399:214
80. Maeda I, Kohara Y, Yamamoto M, Sugimoto A. 2001. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 11:171-76
81. Marban-Mendoza N, Jeyaprakash A, Jansson H-B, Damon RA Jr, Zuckerman BM. 1987. Control of root-knot nematodes on tomato by lectins. J. Nematol. 19:331-35
82. Mariani C, Debeuckeleer M, Truettner J, Leemans J, Goldberg RB. 1990. Induction of male-sterility in plants by a chimeric ribonuclease gene. Nature 347:737-41
83. Mariani C, Gossele V, Debeuckeleer M, Deblock M, Goldberg RB, et al. 1992. A chimeric ribonuclease-inhibitor gene restores fertility to male sterile plants. Nature 357:384-87
84. Marroquin LD, Elyassnia D, Griffitts JS, Feitelson JS, Aroian RV. 2000. Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics 155:1693-99
85. Martin GB, Brommonsschenkel SH, Chunwongse J, Frary A, Ganal MW, et al. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432-36
86. Martin RJ. 1997. Modes of action of anthelmintic drugs. Vet. J. 154:11-34
87. Michaud D, Cantin L, Bonade-Bottino M, Jouanin L, Vrain TC. 1996. Identification of stable plant cystatin/nematode protease complexes using mildly denaturing gelatin/polyacrylamide gel electrophoresis. Electrophoresis 17:1373-79
88. Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. 1998. The root-knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307-19
89. Moore RC, Zhang M, Cassimeris L, Cyr RJ. 1997. In vitro assembled plant microtubules exhibit a high state of dynamic instability. Cell Motil. Cytoskel. 38:278-86
90. Morse RJ, Yamamoto T, Stroud RM. 2001. Structure of Cry2Aa suggests an unexpected receptor binding epitope. Structure 9:409-17
91. Naot D, Benhayyim G, Eshat Y, Holland D. 1995. Drought, heat and salt stress induce the expression of a citrus homologue of an atypical late embryogenesis Lea5 gene. Plant Mol. Biol. 27:619-22
92. Niebel A, Engler JD, Tiré C, Engler G, van Montagu M, Gheysen G. 1993. Induction patterns of an extensin gene in tobacco upon nematode infection. Plant Cell 5:1697-710
93. Oehlschlager S, Reece P, Brown A, Hughson E, Hird H, et al. 2001. Food allergy - towards predictive testing for novel foods. Food Addit. Contam. 18:1099-107
94. Ohl SA, van de Lee FM, Sijmons PC. 1997. Anti-feeding structure approaches to nematode resistance. See Ref. 36a, pp. 250-61
95. Oppenheimer DG, Haas N, Silflow CD, Snustad DP. 1988. The β-tubulin gene family of Arabidopsis thaliana: preferential accumulation of the β1 transcript in roots. Gene 63:87-102
96. Opperman CH, Taylor CG, Conkling MA. 1994. Root-knot nematode-directed expression of a plant root-specific gene. Science 263:221-23
97. Perry RN. 1996. Chemoreception in plant parasitic nematodes. Annu. Rev. Phytopathol. 34:181-99
98. Piano F, Schetter AJ, Mangone M, Stein L, Kemphues KJ. 2000. RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans. Curr. Biol. 10:1619-22
99. Pusztai A, Koninkx J, Hendriks H, Kok W, Hulscher S, et al. 1996. Effect of the insecticidal Galanthus nivalis agglutinin on metabolism and the activities of brush border enzymes in the rat small intestine. J. Nutr. Biochem. 7:677-82
100. Pusztai A, Grant G, Brown DJ, Stewart C, Bardocz S. 1992. Nutritional evaluation of the trypsin (EC 3.4.21.4) inhibitor from cowpea (Vigna unguiculata Walp.) Br. J. Nutr. 68:783-91
101. Puzio PS, Cai D, Ohl S, Wyss U, Grundler FMW. 1998. Isolation of regulatory DNA regions related to differentiation of nematode feeding structures in Arabidopsis thaliana. Physiol. Mol. Plant Pathol. 53:177-93
102. Puzio PS, Lausen J, Almeida-Engler J, Cai D, Gheysen G, Grundler FMW. 1999. Isolation of a gene from Arabidopsis thaliana related to nematode feeding structures. Gene 239:163-72
103. Riddle DL, Blumenthal T, Meyer BJ, Priess JR. 1997. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Lab.
104. Roberts PA. 1992. Current status of the availability of the availability, development and use of host plant resistance to nematodes. J. Nematol. 24:213-27
105. Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM. 1998. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci. USA 95:9750-54
106. Ryan CA. 1990. Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425-49
107. Sasser JN, Freckman DW. 1987. A world perspective on nematology: the role of the society. In Vistas on Nematology, ed. JA Veech, DW Dickerson, pp. 7-14. Marceline, MO: Soc. Nematol.
108. Saxena D, Stotzky G. 2001. Bt toxin uptake from soil by plants. Nat. Biotech. 19:199-99
109. Senchenko VN, Dianova MV, Kanevskii VY, Bocharova AL, Karpeiskii MY. 1993. Formation and properties of S-protein complexes with S-peptide-containing hybrid polypeptides. Mol. Biol. 27:565-69
110. Sheehy BA, Ho NFH, Burton PS, Day JS, Geary TG, Thompson DP. 2000. Transport of model peptides across Ascaris suum cuticle. Mol. Biochem. Parasitol. 105:39-49
111. Shelton AM, Sears MK. 2001. The monarch butterfly controversy: scientific interpretations of a phenomenon. Plant J. 27:483-88
112. Snustad DP, Haas N, Kopczak SD, Silflow CD. 1992. The small genome of Arabidopsis contains at least nine expressed β-tubulin genes. Plant Cell 4:549-56
113. Tabara H, Grishok A, Mello CC. 1998. RNAi in C-elegans: soaking in the genome sequence. Science 282:430-31
114. Timmons L, Court DL, Fire A. 2001. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263:103-12
115. Tzortzakakis EA, Gowen SR. 1996. Occurrence of a resistance breaking pathotype of Meloidogyne javanica on tomatoes in Crete, Greece. Fundam. Appl. Nematol. 19:283-88
116. Urwin PE, Atkinson HJ, Waller DA, McPherson MJ. 1995. Engineered oryzacystatin-I expressed in transgenic hairy roots confers resistance to Globodera pallida. Plant J. 8:121-31
117. 115a. Urwin PE, Green J, Atkinson HJ. 2003. Title will be supplied in proof. Mol. Breed. In press
118. Urwin PE, Levesley A, McPherson MJ, Atkinson HJ. 2000. Transgenic resistance to the nematode Rotylenchulus reniformis conferred by A. thaliana plants expressing protease inhibitors. Mol. Breed. 6:257-64
119. Urwin PE, Lilley CJ, McPherson MJ, Atkinson HJ. 1997. Characterisation of two cDNAs encoding cysteine proteases from the soybean cyst nematode Heterodera glycines. Parasitology 114:605-13
120. Urwin PE, Lilley CJ, Atkinson HJ. 2002. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant-Microbe Interact. 15:747-52
121. Urwin PE, Lilley CJ, McPherson MJ, Atkinson HJ 1997. Resistance to both cyst-and root-knot nematodes conferred by transgenic Arabidopsis expressing a modified plant cystatin. Plant J. 12:455-61
122. Urwin PE, McPherson MJ, Atkinson HJ. 1998. Enhanced transgenic plant resistance to nematodes by dual protease inhibitor constructs. Planta 204:472-79
123. Urwin PE, Møller SG, Lilley CJ, Atkinson HJ, McPherson MJ. 1997. Continual GFP monitoring of CaMV35S promoter activity in nematode induced feeding cells in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 10:394-400
124. Urwin PE, Troth KM, Zubko EI, Atkinson HJ. 2001. Effective transgenic resistance to Globoderapallida in potato field trials. Mol. Breed. 8:95-101
125. Urwin PE, Yi I, Martin H, Atkinson HJ, Gilmartin PM. 2000. Cross kingdom conservation of IRES function: the Encephalomyocarditis virus internal ribosome entry site works in plants. Plant J. 24:583-89
126. Urwin PE, Zubko EI, Atkinson HJ. 2002. The biotechnological application and limitation of IRES to deliver multiple defense genes to plant pathogens. Physiol. Mol. Plant Pathol. 61:103-8
127. Vain P, Worland B, Clarke MC, Richard G, Beavis M, et al. 1998. Expression if an engineered cysteine protease inhibitor (Oryzacystatin- IΔD86) for nematode resistance in transgenic rice plants. Theor. Appl. Genet. 96:266-71
128. van der Eycken W, Engler JD, Inzé D, van Montagu M, Gheysen G. 1996. Molecular study of root-knot nematode-induced feeding sites. Plant J. 9:45-54
129. van der Vossen EAG, van der Voort J, Kanyuka K, Bendahmane A, Sandbrink H, et al. 2000. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 23:567-76
130. Veerman ECI, van den Keybus PAM, Vissink A, Amerongen AVN. 1996. Human glandular salivas: their separate collection and analysis. Eur. J. Oral Sci. 104:346-52
131. Waldron C, Wegrich LM, Merlo PAO, Walsh TA. 1993. Characterization of a genomic sequence coding for potato multicystatin, an 8-domain cysteine protease-inhibitor. Plant Mol. Biol. 23: 801-12
132. Walker AJ, Urwin PE, Atkinson HJ, Brain P, Glen DM, Shewry PR. 1999. Transgenic Arabidopsis leaf tissue expressing a modified oryzacystatin shows resistance to the field slug Deroceras reticulatum (Muller). Transgenic Res. 8:95-103
133. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, et al. 2001. Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27:581-90
134. Whitehead AG. 1998. Plant Nematode Control, pp. 384. Wallingford, UK: CAB Int.
135. Williams ME, Sussex IM. 1995. Developmental regulation of ribosomal protein L16 genes in Arabidopsis thaliana. Plant J. 8:65-76
136. Winter M, McPherson MJ, Atkinson HJ. 2002. Neuronal uptake of pesticides disrupts chemosensory cells of nematodes. Parasitology 125:561-65
137. Wolfenbarger LL, Phifer PR. 2000. The ecological risks and benefits of genetically engineered plants. Science 290:2088-93
138. Zuckerman BM, Jansson HB. 1984. Nematode chemotaxis and possible mechanisms of host/prey interactions. Annu. Rev. Phytopathol. 22:95-113