Molecular strategies of plant defense and insect counter-defense

Insect Science

Volumn 12, Issue 1, 2005, Pages 3-15

  Zhu Salzman, Keyan ^a   Bi, Jian Long ^b   Liu, Tong Xian ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Coevolution; Insect plant interaction; Molecular biology; Plant resistance

Indexed keywords

EID: 35348939909     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1672-9609.2005.00002.x     Document Type: Article

References (108)

1. Ahn, J-E., Salzman, R.A., Koiwa, H. and Zhu-Salzman, K. (2004) Functional roles of specific bruchid protease isoforms in adaptation to a soybean protease inhibitor. Insect Molecular Biology, 13, 649–657.
2. Alborn, T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. and Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science, 276, 945–949.
3. Alvarez, M.E., Pennell, R.I., Meijer, P.J., Ishikawa, A., Dixon, R. A. and Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 92, 773–784.
4. Ament, K., Kant, M.R., Sabelis, M.W., Haring, M.A. and Schuurink, R.C. (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiology, 135, 2025–2037.
5. Argandona, V.H., Chaman, M., Cardemil, L., Munoz, O., Zuniga, G.E. and Corcuera, L.J. (2001) Ethylene production and peroxidase activity in aphid-infested barley. Journal of Chemical Ecology, 27, 53–68.
6. Arimura, G., Tashiro, K., Kuhara, S., Nishioka, T., Ozawa, R. and Takabayashi, J. (2000) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochemistry and Biophysiological Research Communication, 277, 305–310.
7. Baldwin, I.T. (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proceedings of National Academy of Sciences, 95, 8113–8118.
8. Baldwin, I.T. (2001) An ecologically motivated analysis of plant-herbivore interactions in native tobacco. Plant Physiology, 127, 1449–1458.
9. Bergey, D.R., Orozco-Cardenas, M., de Moura, D.S. and Ryan, C.A. (1999) A wound-and systemin-inducible polygalacturonase in tomato leaves. Proceedings of National Academy of Sciences, 96, 1756–1760.
10. Bi, J.L. and Felton, G.W. (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondarymetabolites and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology, 21, 1151–1530.
11. Bi, J.L., Felton, G.W. and Mueller, A.J. (1994) Induced resistance in soybean to Helicoverpa zea: role of plant protein quality. Journal of Chemical Ecology, 20, 183–197.
12. Bi, J.L, Murphy, J.B. and Felton, G.W. (1997a) Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. Journal of Chemical Ecology, 23, 97–117.
13. Bi, J.L., Murphy, J.B. and Felton, G.W. (1997b) Does salicylicacid act as a signal for induced resistance in cotton to Helicoverpa zea Journal of Chemical Ecology, 23, 1805–1818.
14. Bi, J.L., Felton, G.W. and Murphy, J.B. (1997c) Biochemical aspects of induced resistance in cotton to the cotton bollworm. Proceedings of Beltwide Cotton Conferences, 1997. National Cotton Council, USA. pp. 1279–1281.
15. Bi, J.L., Felton, G.W., Murphy, J.B., Howles, P.A., Dixon, R.A. and Lamb, C.J. (1997d) Do plant phenolics confer resistance to specialist and generalist insect herbivores Journal of Agricultural and Food Chemistry, 45, 4500–4504.
16. Bogre, L., Ligterink, W., Meskiene, I., Barker, P.J., Heberle-Bors, E., Huskisson, N.S. and Hirt, H. (1997) Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell, 9, 75–83.
17. Bolter, C.J. (1993) Methyl jasmonate induces papain inhibitor(s) in tomato leaves. Plant Physiology, 103, 1347–1353.
18. Bolter, C.J. and Jongsma, M.A. (1995) Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase-inhibitors induced in potato leaves by methyl jasmonate. Journal of Insect Physiology, 41, 1071–1078.
19. Bones, A.M. and Rossiter, J.T. (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiologia Plantarum, 97, 194–208.
20. Bown, D.P., Wilkinson, H.S. and Gatehouse, J.A. (1997) Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochemistry and Molecular Biology, 27, 625–638.
21. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X.N. (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell, 88, 57–63.
22. Cao, H., Li, X. and Dong, X.N. (1998) Generation of broad-spectrum disease resistance by over expression of an essential regulatory gene in systemic acquired resistance. Proceedings of National Academy of Sciences, 95, 6531–6536.
23. 2 in transgenic tobacco. Proceedings of National Academy of Sciences, 95, 5818–5823.
24. Cloutier, C., Jean, C., Fournier, M., Yelle, S. and Michaud, D. (2000) Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Archives of Insect Biochemistry and Physiology, 44, 69–81.
25. de Bruxelles, G.L. and Roberts, M.R. (2001) Signals regulating multiple responses to wounding and herbivores. Critical Reviews in Plant Science, 20, 487–521.
26. De Leo, F., Bonade-Bottino, M.A., Ceci, L.R., Gallerani, R. and Jouanin, L. (1998) Opposite effects on Spodoptera littoralis larvae of high expression level of a trypsin proteinase inhibitor in transgenic plants. Plant Physiology, 118, 997–1004.
27. De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. and Tumlinson, J.H. (1998) Herbivore-infested plants selectively attract parasitoids. Nature, 393, 570–573.
28. Dempsey, D.A., Shah, J. and Klessig, D.F. (1999) Salicylic acid and disease resistance in plants. Critical Reviews in Plant Science, 18, 547–575.
29. Doarse, S.H., Narvaez-Vasquez, J., Conconi, A., Ryan, C.A. (1995) Salicylic acid inhibits synthesis of proteinase inhibitor in tomato leaves induced by systemin and jasmonic acid. Plant Physiology, 108, 1741–1746.
30. Doss, R.P., Oliver, J.E., Proebsting, W.M., Potter, S.W., Kuy, S. R., Clement, S.L., Williamson, R.T., Carney, J.R. and DeVilbiss, E.D. (2000) Bruchins: Insect-derived plant regulators that stimulate neoplasm formation. Proceedings of National Academy of Sciences, 97, 6218–6223.
31. Eichenseer, H., Mathews, M.C., Bi, J.L., Murphy, J.B. and Felton, G.W. (1999) Salivary glucose oxidase-Multifunctional roles for Helicoverpa zea? Archive of Insect Biochemistry and Physiology, 42, 99–109.
32. Farmer, E.E., Ryan, C.A. (1990) Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proceedings of National Academy of Sciences, 87, 7713–7716.
33. Farmer, E.E., Ryan, C.A. (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound inducible proteinase inhibitors. Plant Cell, 4, 129–134.
34. Felton, G.W., Bi, J.L., Summers, C.B., Mueller, A.J. and Duffey, S.S. (1994) Potential role of lipoxygenases indefense against insect herbivory. Journal of Chemical Ecology, 20, 651–666.
35. Felton, G.W. and Eichenseer, H. (1999) Herbivore saliva and its effect on plant defense against herbivores and pathogens. Induced Plant Defenses Against Pathogens and Herbivores (eds. A.A. Agrawal, S. Tuzun & E. Bent), pp. 19–36. APS Press, Minnesota.
36. Felton, G.W., Korth, K.L., Bi, J.L., Wesley, S.V., Hulman, D.V., Mathews, M.C., Murphy, J.B., Lamb, C.J. and Dixon, R.A. (1999) Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Current Biology, 9, 317–320.
37. Felton, G.W., Mathews, M.C., Bi, J.L., Murphy, J.B. (2001) Insect salivary enzyme triggers systemic resistance. Official Gazette of the Unites States Patents & Trademark Office Patents, 1251(3).
38. Feys, B.J., Moisan, L.J., Newman, M.A. and Parker, J.E. (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. European Molecular Biology Organization Journal, 20, 5400–5411.
39. Fidantsef, A.L., Stout, M.J., Thaler, J.S., Duffey, S.S. and Bostock, R.M. (1999) Signal interactions in pathogen and insect attack: expression of lipoxygenase, proteinase inhibitor II, and pathogenesis-related protein P4 in the tomato, Lycopersicon esculentum. Physiological and Molecular Plant Pathology, 54, 97–114.
40. Giri, A.P., Harsulkar, A.M., Deshpande, V.V., Sainani, M.N., Gupta, V.S. and Ranjekar, P.K. (1998) Chickpea defensive proteinase inhibitors can be inactivated by podborer gut proteinases. Plant Physiology, 116, 393–401.
41. Halitschke, R., Schittko, U., Pohnert, G., Boland, W. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oralsecretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiology, 125, 711–717.
42. Hermsmeier, D., Schittko, U. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth and defense-related plant mRNAs. Plant Physiology, 125, 683–700.
43. Hilder, V.A., Gatehouse, A.M.R., Sheerman, S.E., Barker, R.F. and Boulter, D. (1987) A novel mechanism of insect resistance engineered into tobacco. Nature, 330, 160–163.
44. Howe, G.A., Lightner, J., Browse, J. and Ryan, C.A. (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell, 8, 2067–2077.
45. Illy, C., Quraishi, O., Wang, J., Purisima, E., Vernet, T. and Mort, J.S. (1997) Role of the occluding loop in cathepsin B activity. Journal of Biological Chemistry, 272, 1197–1202.
46. John, M., Schmidt, J., Walden, R., Czaja, I., Dulz, M., Schell, J. and Rohrig, H. (1997) Lipochitooligosaccharide-induced tobacco cells release a peptide as mediator of the glycolipid signal. Proceedings of National Academy of Sciences, 94, 10178–10182.
47. Jongsma, M.A. and Bolter, C. (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology, 43, 885–895.
48. Jongsma, M.A., Bakker, P.L., Peters, J., Bosch, D. and Stiekema, W.J. (1995) Adaptation of Spodoptera exigua larvae to plant proteinase-inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of National Academy of Sciences, 92, 8041–8045.
49. Kessler, A. and Baldwin, I.T. (2002) Plant responses toinsect herbivory: The emerging molecular analysis. Annual Review of Plant Biology, 53, 299–328.
50. Kessler, A., Halitschke, R. and Baldwin, I.T. (2004) Silencing the jasmonate cascade: Induced plant defenses and insect populations. Science, 305, 665–668.
51. Koiwa, H., Shade, R.E., Zhu-Salzman, K., Subramanian, L., Murdock, L.L., Nielsen, S.S., Bressan, R.A. and Hasegawa, P. M. (1998) Phage display selection can differentiate insecticidal activity of soybean cystatins. Plant Journal, 14, 371–379.
52. Korth, K.L. and Dixon, R.A. (1997) Evidence for chewing insectspecific molecular events distinct from a general wound response in leaves. Plant Physiology, 115, 1299–1305.
53. Krishnaveni, S., Muthukrishnan, S., Liang, G.H., Wilde, G. and Manickam, A. (1999) Induction of chitinases and beta-1, 3-glucanases in resistant and susceptible cultivars of sorghum in response to insect attack, fungal infection and wounding. Plant Science, 144, 9–16.
54. Li, X., Schuler, M.A. and Berenbaum, M.R. (2002) Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature, 419, 712–715.
55. Ma, R., Reese, J.C., Black, W.C. and Bramel-Cox, P. (1990) Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera, Aphididae). Journal of Insect Physiology, 36, 507–512.
56. Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J. and Cameron, R.K. (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature, 419, 399–403.
57. Mattiacci, L., Dicke, M. and Posthumus, M.A. (1995) β-Glucosidase: An elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of National Academy of Sciences, 92, 2036–2040.
58. Mazumdar-Leighton, S. and Broadway, R.M. (2001) Transcriptional induction of diverse midgut trypsins in larval Agrotisipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochemistry and Molecular Biology, 31, 645–657.
59. McConn, M., Creelman, R.A., Bell, E., Mullet, J.E. and Browse, J. (1997) Jasmonate is essential for insect defense in Arabidopsis. Proceedings of National Academy of Sciences, 94, 5473–5477.
60. McGurl, B., Orozco-Cardenas, M., Pearce, G. and Ryan, C.A. (1994) Over expression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proceedings of National Academy of Sciences, 91, 9799–9802.
61. McKenzie, C.L., Shatters, R.G., Doostdar, H., Lee, S.D., Inbar, M. and Mayer, R.T. (2002) Effect of geminivirus infection and Bemisia infestation on accumulation of pathogenesis-related proteins in tomato. Archives of Insect Biochemistry and Physiology, 49, 203–214.
62. Memelink, J., Verpoorte, R. and Kijne, J.W. (2001) ORC Anization of jasmonate-responsive gene expression in alkaloid metabolism. Trends in Plant Science, 6, 212–219.
63. Michaud, D., Cantin, L. and Vrain, T.C. (1995) Carboxy-terminal truncation of oryzacysatin-II by oryzacytatin-insensitive insect digestive proteinases. Archives of Biochemistry and Biophysics, 322, 469–474.
64. Miles, P.W. (1999) Aphid saliva. Biological Review, 74, 41–85.
65. Moon, J., Salzman, R.A., Ahn, J-E., Koiwa, H. and Zhu-Salzman, K. (2004) Transcriptional regulation in cowpea bruchid guts during adaptation to a plant defense protease inhibitor. Insect Molecular Biology, 13, 283–291.
66. Moran, P.J., Cheng, Y.F., Cassell, J.L. and Thompson, G.A. (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Archives of Insect Biochemistry and Physiology, 51, 182–203.
67. Moran, P.L. and Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology, 125, 1074–1085.
68. Mosolov, V.V., Grigor'eva, L.I. and Valueva, T.A. (2001) Involvement of proteolytic enzymes and their inhibitors in plant protection (review). Applied Biochemistry and Microbiology, 37, 115–123.
69. Musil, D., Zucic, D., Turk, D., Engh, R.A., Mayr, I., Huber, R., Popovic, T., Turk, V., Towatari, T., Katunuma, N. and Bode, W. (1991) The refined 2.15A X-ray crystal-structure of human liver cathepsin-B: The structural basis for its specificity. European Molecular Biology Organization Journal, 10, 2321–2330.
70. Musser, R.A., Hum-Musser, S.M., Eichenseer, H., Peifer, M., Ervin, G., Murphy, J.B. and Felton, G.W. (2002) Caterpillar saliva beats plant defences. Nature, 416, 560–560.
71. Narvaez-Vasquez, J., Pearce, G., Orozco-Cardenas, M., Fracheschi, V. and Ryan, C.A. (1995) Autoradiographic and biochemical evidence for the systemic translocation of systemin in tomato plants. Planta, 195, 593–600.
72. Niki T., Mitsuhara, I., Seo, S., Ohtsubo, N. and Ohashi, Y. (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiology, 39, 500–507.
73. Orozco-Cardenas, M. and Ryan, C.A. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proceedings of National Academy of Science, 96, 6553–6557.
74. Orozco-Cardenas, M.L., Narvaez-Vasquez, J. and Ryan, C.A. (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell, 13, 179–191.
75. Orr, G.L., Strickland, J.A. and Walsh, T.A. (1994) Inhibition of Diabrotica larval growth by a multicystatin from potatotubers. Journal of Insect Physiology, 40, 893–900.
76. Pare, P.W. and Tumlinson, J.H. (1997) De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiology, 114, 1161–1167.
77. Prado, E., Tjallingii, W.F. (1997) Effects of previous plant infestation on sieve element acceptance by two aphids. Entomologia Experimentalis et Applicata, 82, 189–200.
78. Rahbe, Y. and Febvay, G. (1993) Protein toxicity to aphidsan in vitro test on Acyrthosiphon pisum. Entomologia Experimentalis et Applicata, 67, 149–160.
79. Ratzka, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T. and Kroymann, J. (2002) Disarming the mustard oil bomb. Proceedings of National Academy of Sciences, 99, 11223–11228.
80. Reymond, P. and Farmer, E.E. (1998) Jasmonate and salicylate as global signals for defense gene expression. Current Opinion in Plant Biology, 1, 404–411.
81. Reymond, P., Weber, H., Damond, M. and Farmer, E.E. (2000) Differential gene expression in response tomechanical wounding and insect feeding in Arabidopsis. Plant Cell, 12, 707–720.
82. Rojo, E., Leon, J. and Sanchez-Serrano, J.J. (1999) Crosstalk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana. Plant Journal, 20, 135–142.
83. Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, J., Ullman, D. E. and Williamson, V.M. (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of National Academy of Sciences, 95, 9750–9754.
84. Ryan, C.A. (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochemistry and Biophysiology Acta, 1477, 112–121.
85. Ryan, C.A. and Pearce, G. (1998) Systemin: A polypeptide signal for plant defensive genes. Annual Review of Cell and Developmental Biology, 14, 1–17.
86. Schittko, U., Hermsmeier, D. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNAs in response to insect-derived cues. Plant Physiology, 125, 701–710.
87. Schuler, M. (1996) The role of cytochrome P450 monooxygenases in plant-insect interactions. Plant Physiology, 112, 1411–1419.
88. Schuler, T.H., Poppy, G.M., Kerry, B.R. and Denholm, I. (1998) Insect-resistant transgenic plants. Trends in Biotechnology, 16, 168–175.
89. Stennis, M.J., Chandra, S., Ryan, C.A. and Low, P.S. (1998) Systemin potentiates the oxidative burst incultured tomato cells. Plant Physiology, 117, 1031–1036.
90. Steppuhn, A., Gase, K., Krock, B., Halitschke, R. and Baldwin, I.T. (2004) Nicotine's defensive function in nature. Public Library of Science – Biology, 2, 1074–1080.
91. Sticher, L., Mauch-Mani, B. and Métraux, J.B. (1997) Systemic acquired resistance. Annual Review of Phyatopathology, 35, 235–270.
92. Stintzi, A., Weber, H., Reymond, P., Browse, J. and Farmer, E.E. (2001) Plant defense in the absence of jasmonic acid: The role of cyclopentenones. Proceedings of National Academy of Sciences, 98, 12837–12842.
93. Stotz, H.U., Pittendrigh, B.R., Kroymann, J., Weniger, K., Fritsche, J., Bauke, A. and Mitchell-Olds, T. (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against ehyptian cotton worm but not diamondback moth. Plant Physiology, 124, 1007–1017.
94. Stratmann, J.W. and Ryan, C.A. (1997) Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and olig osaccharide elicitors. Proceedings of National Academy of Sciences, 94, 11085–11089.
95. Terra, W.R. and Ferreira, C. (1994) Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology, 109B, 1–62.
96. Thaler, J.S. (1999) Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature, 399, 686–688.
97. Tran, P., Cheesbrough, T.M. and Keickhefer, R.W. (1997) Plant proteinase inhibitors are potential anticereal aphid compounds. Journal of Economic Entomology, 90, 1672–1677.
98. van de Ven, W.T.G., LeVesque, C.S., Perring, T.M. and Walling, L.L. (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell, 12, 1409–1423.
99. van Wees, S.C.M. and Glazebrook, J. (2003) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. The Plant Journal, 33, 733–742.
100. 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., Pelican, J., Liharska, T., Hontelez, J. and Zabeau, M. (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology, 16, 1365–1369.
101. Walling, L.L. (2000) The myriad plant responses to herbivores. Journal of Plant Growth Regulation, 19, 195–216.
102. Winz, R.A. and Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiology, 125, 2189–2202.
103. 2 in transgenic plants. Plant Physiology, 115, 427–435.
104. Zhang, Y.L., Fan, W.H., Kinkema, M., Li, X. and Dong, X.N. (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proceedings of National Academy of Sciences, 96, 6523–6528.
105. Zhao, Y., Botella, M.A., Subramanian, L., Niu, X.M., Nielsen, S. S., Bressan, R.A. and Hasegawa, P.M. (1996) Two wound-inducible soybean cysteine proteinase inhibitors have greater insect digestive proteinase inhibitory activities than a constitutive homolog. Plant Physiology, 111, 1299–1306.
106. Zhu-Salzman, K., Koiwa, H., Salzman, R.A., Shade, R.E. and Ahn, J-E. (2003) Cowpea Bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Molecular Biology, 12, 135–145.
107. Zhu-Salzman, K., Salzman, R.A., Ahn, J-E. and Koiwa, H. (2004) Transcriptional regulation of sorghum defens determinants against a phloem-feeding aphid. Plant Physiology, 134, 420–431.
108. Zhu-Salzman, K., Salzman, R.A., Koiwa, H., Murdock, L.L., Bressan, R.A. and Hasegawa, P.M. (1998) Ethylene negatively regulates local expression of plant defense lectin genes. Physiologia Plantarum, 104, 365–372.