Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions

Archives of Insect Biochemistry and Physiology

Volumn 51, Issue 4, 2002, Pages 182-203

  Moran, Patrick J ^a,c   Cheng, Youfa ^b   Cassell, Jeffery L ^b   Thompson, Gary A ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b Department of Information Science   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Aphid; DNA microarray; Gene expression profiling; Phloem; Plant insect

Indexed keywords

ALEYRODIDAE; APHIDIDAE; ARABIDOPSIS; ARABIDOPSIS THALIANA; HEXAPODA; INSECTA;

ARABIDOPSIS PROTEIN;

ANIMAL; APHID; ARABIDOPSIS; BIOSYNTHESIS; BRASSICACEAE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETIC PROCEDURES; GENETICS; HOST PARASITE INTERACTION; INNATE IMMUNITY; METABOLISM; METHODOLOGY; OLIGONUCLEOTIDE PROBE; PARASITOLOGY; PHYSIOLOGY; PLANT DISEASE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APHIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BRASSICACEAE; GENE EXPRESSION PROFILING; HOST-PARASITE RELATIONS; IMMUNITY, NATURAL; MOLECULAR PROBE TECHNIQUES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OLIGONUCLEOTIDE PROBES; PLANT DISEASES; SIGNAL TRANSDUCTION;

EID: 0036886719     PISSN: 07394462     EISSN: None     Source Type: Journal    
DOI: 10.1002/arch.10064     Document Type: Article

References (130)

1. Argandoña VH. 1994. Effect of aphid infestation on enzyme activities in barley and wheat. Phytochemistry 35:313-315.
2. Argandoña VH, Chaman M, Cardemil L, Munoz O, Zuñiga GE, Corcuera LJ. Ethylene production and peroxidase activity in aphid-infested barley. J Chem Ecol 27:53-68.
3. Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J. 2000. Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277:305-310.
4. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. 2002. MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977-983.
5. Barbosa P. 1991. Plant pathogens and nonvector herbivores. In: Barbosa P, Krischik VA, Jones CG, editors. Microbial mediation of plant-herbivore interactions. New York: Wiley and Sons. p 341-382.
6. Belefant-Miller H, Porter DR, Pierce ML, Mort AJ. 1994. An early indicator of resistance in barley to russian wheat aphid. Plant Physiol 105:1289-1294.
7. Bell E, Mullet JE. 1993. Chracterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol 103:1133-1137.
8. Bergey DR, Ryan CA. 1999. Wound- and systemin-inducible gene expression in tomato leaves. Plant Mol Biol 40:815-823.
9. Bi JL, Felton GW. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J Chem Ecol 21:1511-1530.
10. Bolwell GP, Wojtaszek P. 1997. Mechanisms for the generation of reactive oxygen species in plant defence- a broad perspective. Physiol Mol Plant Pathol 51:347-366.
11. Botha A-M, Nagel MAC, Van der Westhuizen AJ, Botha FC. 1998. Chitinase isozymes in near-isogenic wheat lines challenged with Russian wheat aphid, exogenous ethylene, and mechanical wounding. Bot Bull Acad Sin 39:99-106.
12. Bradbourne RP, Mithen R. 2000. Glucosinolate genetics and the attraction of the aphid parasitoid Diaretiella rapae. Proc R Soc London Ser B 267:89-95.
13. Brotman Y, Silberstein L, Kovalski I, Perin C, Dogimont C, Pitrat M, Klingler J, Thompson G, Perl-Treves R. 2002. Resistance gene homologues in melon and their linkage to genetic loci conferring disease and pest resistance. Theor Appl Genet 104:1055-1063.
14. + symporter of Arabidopsis thaliana. Plant Cell Env 23:175-184.
15. Campbell BC, Dreyer DL. 1990. The role of plant matrix polysaccharides in aphid-plant interactions. In: Campbell RK, Eikenbary RD, editors. Aphid-plant genotype interactions. Amsterdam: Elsevier. p 149-169.
16. Campbell P, Braam J. 1999. In vitro activities of four xyloglucan endotransglycosylases from Arabidopsis. Plant J 18:371-382.
17. Chaman ME, Corcuera LJ, Zuñiga GE, Cardemil L, Argandoña VH. 2001. Induction of soluble and cell wall peroxidases by aphid infestation in barley. J Agric Food Chem 49: 2249-2253.
18. Chester KS. 1933. The problem of acquired immunity in plants (continued). Q Rev Biol 8:275-340.
19. Ciepiela AP, Sempruch C, Kaszyñski W. 1994. Participation of chosen nonprotein amino acids in constitutive resistance of winter triticale to grain aphid. Rocz Nauk Rol E 24:99-104.
20. Cole RA. 1994. Isolation of a chitin-binding lectin, with insecticidal activity in chemically-defined synthetic diets, from two wild brassica species with resistance to cabbage aphid Brevicoryne brassicae. Entomol Exp Appl 72: 181-187.
21. Cole RA. 1996. Abiotic induction of changes to glucosinolate profiles in Brassica species and increased resistance to the specialist aphid Brevicoryne brassicae. Entomol Exp Appl 80:228-230.
22. Cole RA. 1997a. Comparison of feeding behaviour on two Brassica pests Brevicoryne brassicae and Myzus persicae on wild and cultivated brassica species. Entomol Exp Appl 85:135-143.
23. Cole RA. 1997b. The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated brassica species. Entomol Exp Appl 85:121-133.
24. Coley PD, Bryant JP, Chapin FSI. 1985. Resource availability and plant anitherbivore defense. Science 230:895-899.
25. de Nooij MP, Bière A, Linders EGA. 1992. Interaction of pests and pathogens through host disposition. In: Ayres PG, editor. Pests and pathogens: plant responses to foliar attack. Oxford: BIOS Scientific Publishers, p 142-160.
26. Dillwith JW, Berberet RC, Bergman DK, Neese PA, Edwards RM, McNew RW. 1991. Studies on the spotted alfalfa aphid, Therioaphis maculata. Arch Ins Biochem Physiol 17:235-251.
27. Dixon AFG. 1998. Aphid ecology: An optimization approach, 2nd ed. New York: Chapman and Hall, 300 p.
28. Douglas AE. 1998. Nutritional interactions in insect-plant microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17-37.
29. Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM. 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355-1369.
30. Edwards R, Dixon DP, Walbot V. 2000. Plant glutathione-S-transferases: enzymes with multiple functions in sickness and in health. Trend Plant Sci 5:193-198.
31. Ellis PR, Pink DAC, Phelps K, Jukes PL, Breeds SE, Pinnegar AE. 1998. Evaluation of a core collection of Brassica oleracea accessions for resistance to Brevicoryne brassicae, the cabbage aphid. Euphytica 103:149-160.
32. Ellis PR, Kift NB, Pink DAC, Jukes PL, Lynn J, Tatchell GM. 2000. Variation in resistance to the cabbage aphid (Brevicoryne brassicae) between and within wild and cultivated Brassica species. Genet Res Crop Evol 47:395-401.
33. Evert R. 1990. Dicotyledons. In: Behnke HD, Sjölund RD, editors. Sieve elements: comparative structure, induction and development. Berlin: Springer, p 103-137.
34. Felton GW, Eichneseer H. 1999. Herbivore saliva and its effects on plant defense against herbivores and pathogens. In: Agrawal AA, Tuzun S, Bent, editors. Induced plant defenses against pathogens and herbivores. St Paul, MN: American Phytopathological Society, p 19-36.
35. Felton GW, Summers CB, Mueller AJ. 1994. Oxidative responses in soybean foliage to herbivory by bean leaf beetle and three-cornered alfalfa hopper. J Chem Ecol 20:639-650.
36. Fidantsef AL, Stout MJ, Thaler JS, Duffey SS, Bostock RM. 1999. Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiol Mol Plant Pathol 54:97-114.
37. Forslund K, Pettersson J, Bryngelsson T, Jonsson L. 2000. Aphid infestation induces PR-proteins differently in barley susceptible or resistant to the birdcherry-oat aphid (Rhopalosiphum padi). Physiol Plant 110:496-502.
38. Gan S, Amasino RM. 1997. Making sense of senescence. Plant Physiol 113:313-319.
39. Gianoli E. 2000. Competition in cereal aphids (Homoptera: Aphididae) on wheat plants. Environ Entomol 29:213-219.
40. Gianoli E, Niemeyer HM. 1998. No risk, no gain? Limited benefits of a non-costly herbivory induced defense in wheat. Ecoscience 5:480-485
41. Glazebrook J. 2001. Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr Opin Plant Biol 4:301-308.
42. Gomez-Lin, MA, Valdes-Lopez V, Cruz-Hernandez A, Saucedo-Arias AJ. 1993. Isolation and characterization of a gene involved in ethylene biosynthesis from Arabidopsis thaliana. Gene 134:217-221.
43. Guerrieri E, Poppy GM, Powell W, Tremblay E, Pennacchio F. 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J Chem Ecol 25:1247-1261.
44. Hahn MG. 1996. Microbial elicitors and their receptors in plants. Annu Rev Phytopathol 34:387-412.
45. Haile FJ, Higley LG, Ni X, Quisenberry SS. 1999. Physiological and growth tolerance in wheat to Russian wheat aphid (Homoptera: Aphididae) injury. Environ Entomol 28: 787-794.
46. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuate. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711-717.
47. Harrewijn P. 1990. Resistance mechanisms of plant genotypes to various aphid species. In: Campbell RK, Eikenbary RD, editors. Aphid-plant-genotype interactions. Amsterdam: Elsevier, p 117-130.
48. Havíicková H, Cvikrová M, Eder J, Hrubcová M. 1998. Alterations in the levels of phenolics and peroxidase activities induced by Rhopalosiphum padi (L.) in two winter wheat cultivars. J Plant Dis Prot 105:140-148.
49. Hervé C, Serres J, Dabos P, Canut H, Barre A, Rouge P, Lescure B. 1999. Characterization of the Arabidopsis lecRK-α genes: members of a superfamily encoding putative receptors with an extracellular domain homologous to legume lectins. Plant Mol Biol 39:671-682.
50. Howe GA, Lightner J, Browse J, Ryan CA. 1996. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067-2077.
51. Inbar M, Doostdar H, Gerling D, Mayer RT. 2001. Induction of systemic acquired resistance in cotton by BTH has a negligible effect on phytophagous insects. Entomol Exp Appl 99:65-70.
52. Jiang Y, Miles PW. 1993. Responses of a compatible lucerne variety to attack by spotted alfalfa aphid: changes in the redox balance in infested tissues. Entomol Exp Appl 67:263-274.
53. Johnson KA, Sistrunk ML, Polisensky DH, Braam J. 1998. Arabidopsis thaliana responses to mechanical stimulation do not require ETR1 or EIN2. Plant Physiol 116:643-649.
54. Jones JDG. 2001. Putting knowledge of plant disease resistance genes to work. Curr Op Plant Biol 4:281-287.
55. Kaakeh W, Pfeiffer DG, Marini RP. 1992. Combined effects of spirea aphid (Homptera: Aphididae) and nitrogen fertilization on net photosynthesis, total chlorophyll content, and greenness of leaves. J Econ Entomol 85:939-946.
56. Karban R. Baldwin IT. 1997. Induced responses to herbivory. Chicago: University of Chicago Press. 319 p.
57. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ. 2001. Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889-905.
58. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299-328.
59. Kliebenstein DJ, Dietrich RA, Martin CA, Last RL, Dangl JL. 1999. LSD1 regulates salicylic acid induction of copper-zinc superoxide dismutase in Arabidopsis thaliana. Mol Plant-Microbe Int 12:1022-1026
60. Klingler J, Powell G, Thompson GA, Isaacs R. 1998. Phloem specific aphid resistance in Cucumis melo line AR5: effects on feeding behaviour and performance of Aphis gossypii. Entomol Exp Appl 86:79-88.
61. Kohler A, Schwindling S, Conrath U. 2002. Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128:1046-1056.
62. Kramer KJ, Muthukrishnan S. 1997. Insect chitinases: molecular biology and potential use as biopesticides. Insect Biochem Mol Biol 27:887-900.
63. Krischik VA. 1991. Specific or generalized plant defense: reciprocal interactions between herbivores and pathogens. In: Barbosa P, Krischik VA, Jones CG, editors. Microbial mediation of plant-herbivore interactions. New York: John Wiley and Sons, p 309-340.
64. Krishnaveni S, Muthukrishan S, Liang GH, Wilde G, Manickam A. 1999. Induction of chitinases and β-1,3-glucanases in resistant and susceptible cultivars of sorghum in response to insect attack, fungal infection and wounding. Plant Sci 144:9-16.
65. Lapointe SL, Tingey WM. 1984. Feeding response of the green peach aphid (Homoptera:Aphididae) to potato glandular trichomes. J Econ Entomol 77:386-389.
66. León J, Rojo E, Titarenko E, Sánchez-Serrano JJ. 1998. Jasmonic acid-dependent and -independent wound signal transduction pathways are differentially regulated by Ca2+/calmodulin in Arabidopsis thaliana. Mol Gen Genet 258: 412-419.
67. Leszczynski B. 1985. Changes in phenols content and metabolism in leaves of susceptible and resistant wheat cultivars infested by Rhopalosiphum padi (L.) (Hom., Aphididae). Z Ang Entomol 100:343-348
68. Loper GM. 1968. Effect of aphid infestation on the coumesterol content of alfalfa varieties differing in aphid resistance. Crop Sci 8:104-106.
69. Madhusudhan W, Miles PW. 1998. Mobility of salivary components as a possible reason for differences in the responses of alfalfa aphid and pea aphid. Entomol Exp Appl 86:25-39.
70. Marrs KA. 1996. The function and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127-158.
71. Mattiaci L, Dicke M, Posthumus MA. β-glucosidase: An elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92: 2036-2040.
72. Mattson WJ Jr. 1980. Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119-161.
73. Mayer RT, McCollum TG, McDonald RE, Polston JE, Doostdar H. 1996. Bemisia feeding induces pathogenesis-related proteins in tomato. In: Gerling D, Mayer RT, editors. Bemisia 1995: taxonomy, biology, damage control and management. Andover, UK: Intercept Ltd. p 179-188.
74. McConn M, Creelman RA, Bell E, Mullet JE, Browse J. 1997. Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA 94:5473-5477.
75. McElhany P, Real LA, Power AG. 1995. Vector preference and disease dynamics: a study of barley yellow dwarf virus. Ecology 76:444-457.
76. Miles PW. 1990. Aphid salivary secretions and their involvement in plant toxicoses. In: Campbell RK, Eikenbary RD, editors. Aphid-plant genotype interactions. Amsterdam: Elsevier. p 131-147.
77. Miles PW. 1999. Aphid saliva. Biol Rev 74:41-85.
78. Miles PW, Oertli JJ. 1993. The significance of antioxidants in the aphid-plant interaction: the redox hypothesis. Entomol Exp Appl 67:273-285
79. Mittler TE. 1971. Dietary amino acid requirements of the aphid M. persicae affected by antibiotic uptake. J Nutrition 101:1023-1028
80. Montllor CB. 1991. The influence of plant chemistry on aphid feeding behavior. In: Bernays EA, editor. Insect-plant interactions, Vol III. Boca Raton, FL: CRC Press. p 125-173.
81. Moran PJ, Thompson GA. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074-1085.
82. Nault NR. 1997. Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 90:521-541.
83. Ni X, Quisenberry SS, Heng-Moss T, Markwell J, Sarath G, Klucas R, Baxendale F. 2001. Oxidative responses of resistant and susceptible cereal leaves to symptomatic and nonsymptomatic cereal aphid (Hemiptera: Aphididae) feeding. J Econ Entomol 94:743-751.
84. Nurnberger T, Scheel D. 2001. Signal transduction in the plant immune response. Trend Plant Sci 6:372-379.
85. Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux J-P, Broekaert WF. 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103-2113.
86. Pilson D, Rausher MD. 1995. Clumped distribution patterns in goldenrod aphids: genetic and ecological mechanisms. Ecol Entomol 2075-2083.
87. Pollard DG. 1973. Plant penetration by feeding aphids (Hemiptera, Aphidoidea): a review. Bull Entomol Res 62: 631-714.
88. Potter I, Uknes S, Lawton K, Winter AM, Chandler D, DiMaio J, Novitsky R, Ward E, Ryals J. 1993. Regulation of a hevein-like gene in Arabidopsis. Mol Plant-Microbe Int 6:680-685.
89. Prado E, Tjallingii WF. 1997. Effects of previous plant infestation on sieve element acceptance by two aphids. Entomol Exp Appl 82:189-200.
90. Purcell AH, Nault LR. 1991. Interactions among plant pathogenic prokaryotes and insect vectors. In: Barbosa P, Krischik VA, Jones CG, editors. Microbial mediation of plant-herbivore interactions. New York: Wiley and Sons, p 383-405.
91. Raychaudhuri SS. 2000. The role of superoxide dismutase in combating oxidative stress in higher plants. Bot Rev 66:89-98.
92. Reymond P, Weber H, Damond M, Farmer EE. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707-719.
93. Rhodes JD, Thain JF, Wildon DC. 1996. The pathway for systemic electrical signal conduction in the wounded tomato plant. Planta 200:50-57.
94. Rojo E, León J, Sánchez-Serrano I. 1999. Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant J 20:135-142.
95. Ross AF. 1961. Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340-358.
96. 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 95:9750-9754.
97. Ryals J, Ward E, Ahl-Goy P, Métraux JP. 1992. Systemic acquired resistance: an inducible defence mechanism in plants. In: Wray JE, editor. Inducible plant proteins. Cambridge, UK: Cambridge University Press, p 205-229.
98. Ryan JD, Morgham AT, Richardson PE, Johnson RC, Mon AJ, Eikenbary RD. 1990. Greenbugs and wheat: a model system for the study of phytotoxic Homoptera. In: Campbell RK, Eikenbary RD, editors. Aphid-plant genotype interactions. Amsterdam: Elsevier, p 171-186.
99. Sandström J, Moran N. 1999. How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91:203-210.
100. Sauge, M-H, Lacroze, J-P, Poëssel J-L, Pascal T, Kervella J. 2002. Induced resistance by Myzus persicae in the peach cultivar 'Rubira'. Entomol Exp Appl 102:29-37.
101. Sauvion N, Rahbé Y, Peumans WJ, Van Damme EJM, Gatehouse JA, Gatehouse AMR. 1996. Effects of GNA and other mannose binding lectins on development and fecundity of the peach-potato aphid Myzus persicae. Entomol Exp Appl 79:285-293.
102. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655-11660.
103. Shinoda T. 1993. Callose reaction induced in melon leaves by feeding of melon aphid, Aphis gossypii Glover, as possible aphid-resistant factor. Jpn J Appl Entomol Zool 37:145-152.
104. Spiteller D, Dettner K, Boland W. 2000. Gut bacteria may be involved in interactions between plants, herbivores and their predators: microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles. Biol Chem 381: 755-762.
105. Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, Bauke A, Mitchell-Olds T. 2000. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol 124: 1007-1017.
106. Stout MJ, Bostock RM. 1999. Specificity of induced responses to arthropods and pathogens. In: Agrawal AA, Tuzun S, Bent E, editors. Induced plant defenses against pathogens and herbivores: biochemistry, ecology and agriculture. St Paul, MN: American Phytopathological Society Press, p 183-210.
107. Telang A, Sandström J, Dyreson E, Moran NA. 1999. Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol Exp Appl 91:403-412.
108. Thaler JS, Stout MJ, Karban R, Duffey SS. 2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol Entomol 26:312-324
109. Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107-15111.
110. Tjallingii WF. 1995. Regulation of phloem sap feeding by aphids. In: Chapman RF, de Boer G, editors. Regulatory mechanisms in insect feeding. New York: Chapman and Hall, p 190-209.
111. Tjallingii WF, Hogen Esch T. 1993. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol Entomol 18:317-328
112. Tosh CR, Walter KFA, Douglas AE. 2001. On the mechanistic basis of plant affiliation in the black bean aphid (Aphis fabae) complex. Entomol Exp Appl 99:121-125.
113. Tran P, Cheesebrough TM, Keichefer RW. 1997. Plant proteinase inhibitors are potential anticereal aphid compounds. J Econ Entomol 90:1672-1677.
114. Turlings TCJ, Alborn HT, Loughrin JH, Tumlinson JH. 2000. Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: isolation and bioactivity. J Chem Ecol 26:189-202.
115. van der Westhuizen AJ, Qian X-M, Botha A-M. 1998a. β-1,3-glucanase in wheat and resistance to the Russian wheat aphid. Physiol Plant 103:125-131.
116. van der Westhuizen AJ, Qian X-M, Botha A-M. 1998b. Differential induction of apoplastic peroxidase and chitinase activities in susceptible and resistant wheat cultivars by Russian wheat aphid infestation. Plant Cell Rep 18: 132-137.
117. Van Loon LC, Van Strien EA. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85-97.
118. van Wees SCM, Luijendijk M, Smoorenburg I, van Loon LC, Pieterse CMJ. 1999. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene AtVsp upon challenge. Plant Mol Biol 41:537-549.
119. Vancanneyt G, Sanz C, Farmaki T, Paneque M, Ortego F, Castañera P, Sánchez-Serrano JJ. 2001. Hydroxperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proc Natl Acad Sci USA 98:8139-8144.
120. Walling LL. 2000. The myriad plants responses to herbivores. J Plant Growth Reg 19:195-216.
121. Wanner LA, Li G, Ware D, Somssich IE, Davis KR. 1995. The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana. Plant Mol Biol 27:327-338.
122. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate mutase is required to synthesize salicylic acid for plant defence. Nature 414:562-565.
123. Wood BW, Tedders WL, Thompson JM. 1985. Feeding influence of three pecan aphid species on carbon exchange and phloem integrity of seedling pecan foliage. J Am Soc Hort Sci 110:393-397.
124. Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG. 1998. COII1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091-1094.
125. Yahraus T, Chandra S, Legendre L, Low PS. 1995. Evidence for a mechanically induced oxidative burst. Plant Physiol 109:1259-1266.
126. Zehnder GW, Nichols AJ, Edwards OR, Ridsill-Smith TJ. 2001. Electronically monitored cowpea aphid feeding behavior on resistant and susceptible lupins. Entomol Exp Appl 98:259-269.
127. Zhang H, Zhang R, Liang P. 1996. Differential screening of gene expression difference enriched by differential display. Nucleic Acid Res 24:2454-2455.
128. Zhang Y, Fan W, Kinkema M, Dong X. 1999. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96: 6523-6528.
129. Zhao J, Williams CC, Last RL. 1998. Induction of Arabidopsis tryptophan pathway enzymes and camalexin by amino acid starvation, oxidative stress, and an abiotic elicitor. Plant Cell 10:359-370
130. Zhou N, Tootle TL, Glazebrook J. 1999. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11:2419-2428.