Plant defense against herbivores: Chemical aspects

Annual Review of Plant Biology

Volumn 63, Issue , 2012, Pages 431-450

  Mithöfer, Axel ^a   Boland, Wilhelm ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

arms race; coevolution; direct indirect defense; metabolic plasticity; mode of action; specialized metabolites

Indexed keywords

ALKALOID; CYANOGENIC GLYCOSIDES; GLUCOSINOLATE; GLYCOSIDE; LATEX; TERPENE;

ADAPTATION; ANIMAL; CHEMISTRY; FOOD CHAIN; HERBIVORY; HOST PARASITE INTERACTION; INSECT; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ALKALOIDS; ANIMALS; FOOD CHAIN; GLUCOSINOLATES; GLYCOSIDES; HERBIVORY; HOST-PARASITE INTERACTIONS; INSECTS; LATEX; PLANTS; TERPENES;

EID: 84872223595     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-042110-103854     Document Type: Review

References (136)

1. Agrawal AA. 2000. Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804-13
2. Agrawal AA, Konno K. 2009. Latex: a model for understanding mechanism s, ecolog y, and evolution of plant defense against herbivory. Annu. Rev. Ecol. Evol. Syst. 40:311-31
3. Agrawal AA, Strauss SY, Stout MJ. 1999. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Ecology 53:1093-104
4. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel WJ, et al. 2003. Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866-84
5. Amirhusin B, Shade RE, Koiwa H, Hasegawa PM, Bressan RA, et al. 2004. Soyacystatin N inhibits proteolysis of wheat alpha-amylase inhibitor and potentiates toxicity against cowpea weevil. J. Econ. Entomol. 97:2095-100
6. Arrendale RF, Severson RF, Sisson VA, Costello CE, Leary JA, et al. 1990. Characterization of the sucrose ester fraction from Nicotiana glutinosa. J. Agric. Food Chem. 38:75-85
7. Asano N, Nash RJ, Molyneux RJ, Fleet GWJ. 2000. Sugar-mimic glycosidase inhibitors: natural occurrenc e, biological activity and prospects for therapeutic application. Tetrahedron Asymmetry 11:1645-80
8. Bakkali F, Averbeck S, Averbeck D, Waomar M. 2008. Biological effects of essential oils: a review. Food Chem. Toxicol. 46:446-75
9. Ballare CL. 2009. Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant Cell Environ. 32:713-25
10. Ballhorn DJ, Lieberei R, Ganzhorn JU. 2005. Plant cyanogenesis of Phaseolus lunatus and its relevance for herbivore-plant interaction: the importance of quantitative data. J. Chem. Ecol. 31:1445-73
11. Bazzaz FA. 1997. Allocation of resources in plants: state of the science and critical questions. In Plant Resource Allocatio n, ed. FA Bazza z, J Grac e, pp 1-37. San Dieg o, CA: Academic
12. Braun K, Romero J, Liddell C, Creamer R. 2003. Production of swainsonine by fungal endophytes of locoweed. Mycol. Res. 107:980-88
13. Becerra JX, Noge K, Venable DL. 2009. Macroevolutionary chemical escalation in an ancient plantherbivore arms race. Proc. Natl. Acad. Sci. USA 27:18062-66
14. Bennett AE, Bever JD, Bowers MD. 2009. Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160:771-79
15. Berenbaum M. 1983. Coumarins and caterpillars: a case for coevolution. Evolution 37:163-79
16. Berenbaum M, Feeny P. 1981. Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race. Science 212:927-29
17. Berenbaum MR, Zangerl AR. 1998. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl. Acad. Sci. USA 95:13743-48
18. Bezemer TM, van Dam NM. 2005. Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol. Evol. 20:617-24
19. Bones AM, Rossiter JT. 1996. The myrosinase-glucosinolate syste m, its organization and biochemistry. Physiol. Plant. 97:194-208
20. Borek V, Elberson LR, McCaffrey JP, Morra MJ. 1997. Toxicity of rapeseed meal and methyl isothiocyanate to larvae of the black vine weevil (Coleopter a, Curculionidae). J. Econ. Entomol. 90:109-12
21. Brown KK, Hampton MB. 2011. Biological targets of isothiocyanates. Biochim. Biophys. Acta 1810:888-94
22. Bruce TJ A, Pickett JA. 2007. Plant defence signaling induced by biotic attacks. Curr. Opin. Plant Biol. 10:387-92
23. Burse A, Frick S, Discher S, Tolzin-Banasch K, Kirsch R, et al. 2009. Always being well prepared for defense: the production of deterrents by juvenile Chrysomelina beetles (Chrysomelidae). Phytochemistry 70:1899-909
24. Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J. 66:212-29
25. Chew FS, Rodman JE. 1979. Plant resources for chemical defenses. In Herbivores: Their Interaction with Secondary Plant Metabolite s, ed. GA Rosentha l, DH Janze n, pp. 271-307. New York: Academic
26. Chow JK, Akhtar Y, Isman MB. 2005. The effects of larval experience with a complex plant latex on subsequent feeding and oviposition by the cabbage loopermoth: Trichoplusia ni (Lepidoptera: Noctuidae). Chemoecology 15:129-33
27. Coley PD. 1986. Costs and benefits of defense by tannins in a neotropical plant. Oecologia 70:238-41
28. Colegate SM, Dorling PR, Huxtable CR. 1979. A spectroscopic investigation of swainsonine: an α-mannosidase inhibitor isolated from Swainsona canescens. Aust. J. Chem. 32:2257-64
29. Cooke J, Leishman MR. 2010. Is plant ecology more siliceous than we realize? Trends Plant Sci. 16:61-68
30. Damle MS, Giri AP, Sainani MN, Gupta VS. 2005. Higher accumulation of proteinase inhibitors in flowers than leaves and fruits as a possible basis for differential feeding preference of Helicoverpa armigera on tomato (Lycopersiconesculentum Mil l, Cv. Dhanashree). Phytochemistry 66:2659-67
31. Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc. R. Soc. Lond. Ser. B 205:489-511
32. De Boer JG, Posthumus MA, Dicke M. 2004. Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J. Chem. Ecol. 30:2215-30
33. De Moraes CM, Lewis WJ, Paŕe PW, Alborn HT, Tumlinson JH. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570-73
34. De Vos M, van Zaanen W, Koorneef A, Korzelius JP, Dicke M, et al. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142:352-63
35. Detzel A, Wink M. 1993. Attractio n, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:8-18
36. Devine GJ, Harling ZK, Scarr AW, Devonshire AL. 1996. Lethal and sublethal effects of imidacloprid on nicotine-tolerant Myzus nicotinanae and Myzus persicae. Pestic. Sci. 48:57-62
37. Dhingra S. 1994. Development of resistance in the bean aphi d, Aphis craccivora Koch to various insecticides used for nearly a quarter century. J. Entomol. Res. 18:105-8
38. Dicke M, Sabelis MW. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:148-65
39. Dicke M, Vanbeek TA, Posthumus MA, Bendom N, Vanbokhoven H, et al. 1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions-involvement of host plant in its production. J. Chem. Ecol. 16:381-96
40. Dinan L. 2001. Phytoecdysteroids: biological aspects. Phytochemistry 57:325-39
41. Duke SO, Canel C, Rimando AM, Tellez MR, Duke MV, Paul RN. 2000. Current and potential exploitation of plant glandular trichome productivity. In Advances in Botanical Research Incorporating Advances in Plant Patholog y, ed. DL Hallaha n, JC Gra y, 31:121-51. New York: Academic
42. Dussourd DE. 1995. Entrapment of aphids and whiteflies in lettuce latex. Ann. Entomol. Soc. Am. 88:163-72
43. Dussourd DE, Eisner T. 1987. Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237:898-901
44. Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608
45. Felton GW. 2005. Indigestion is a plant's best defense. Proc. Natl. Acad. Sci. USA 102:18771-72
46. Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB. 2009. The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J. Chem. Ecol. 35:833-43
47. Gatehouse JA. 2002. Plant resistance towards insect herbivores: a dynamic interaction. New Phytol. 156:145-69
48. Gepner JI, Hall LM, Sattelle DB. 1978. Insect acetylcholine receptors as a site of insecticide action. Nature 276:188-90
49. Gershenzon J, Croteau R. 1991. Terpenoids. In Herbivores: Their Interactions with Secondary Plant Metabolites. The Chemical Participant s, ed. GA Rosentha l, MR Berenbau m, 1:165-219. San Diego: Academic
50. Gleadow RM, Woodrow IE. 2002. Constraints of effectiveness of cyanogenic glycosides in herbivore defense. J. Chem. Ecol. 28:1301-13
51. Green TR, Ryan CA. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776-77
52. Hartl M, Giri A, Kaur H, Baldwin IT. 2010. Serine protease inhibitors specifically defend Solanum nigrum against generalist herbivores but do not influence plant growth and development. Plant Cell 22:4158-75
53. Heil M. 2008. Indirect defence via tritrophic interactions. New Phytol. 178:41-61
54. Heil M, Greiner S, Meimberg H, Kr̈uger R, Noyer JL, et al. 2004. Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205-8
55. Hildreth SH, Gehman EA, Yang H, Lu R-H, Ritesh KC, et al. 2011. Tobacco nicotine uptake permease (NUP1) affects alkaloid metabolism. Proc. Natl. Acad. Sci. USA 108:18179-84
56. Hilker M, Meiners T. 2006. Early herbivore alert: insect eggs induce plant defense. J. Chem. Ecol. 32:1379-97
57. Hirayama C, Konno K, Wasano N, Nakamura M. 2007. Differential effects of sugar-mimic alkaloids in mulberry latex on sugar metabolism and disaccharidases of Eri and domesticated silkworms: enzymatic adaptation of Bombyx mori to mulberry defense. Insect Biochem. Mol. Biol. 37:1348-58
58. Holzinger F, Frick C, Wink M. 1992. Molecular basis for the insensitivity of the Monarch (Danaus plexippus) to cardiac glycosides. FEBS Lett. 314:477-80
59. Hopkins RJ, van Dam NM, van Loon JJA. 2009. Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54:57-83
60. Huang T, Jander G, de Vos M. 2011. Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72:1531-37
61. Ivie GW, Bull DL, Beier RC, Pryor NW, Oertli EH. 1983. Metabolic detoxification: mechanism of insect resistance to plant psoralens. Science 221:374-76
62. Jones AS, Lamont BB, Fairbanks MM, Rafferty CM. 2003. Kangaroos avoid eating seedlings with or near others with volatile essential oils. J. Chem. Ecol. 29:2621-35
63. Jones P, Vogt T. 2001. Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 3:164-74
64. Kappers IF, Aharoni A, vanHerpenTWJ M, Luckerhoff LL P, Dicke M, et al. 2005. Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070-72
65. Katoh A, Ohki H, Inai K, Hashimoto T. 2005. Molecular regulation of nicotine biosynthesis. Plant Biotechnol. 22:389-92
66. Kessler A, Baldwin IT. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141-44
67. Khan ZR, James DG, Midega CA O, Pickett JA. 2007. Chemical ecology and conservation biological control. Biol. Control 45:210-24
68. Kniep H. 1905. Über die Bedeutung des Milchsafts der Pflanzen. Flora Allg. Bot. Z. ( Jena) 94:129-205
69. Korth KL, Doege SJ, Park SH, Goggin FL, Wang Q, et al. 2005. Medicago truncatula mutants demonstrate the role of plant calcium oxalate crystals as an effective defense against chewing insects. Plant Physiol. 141:188-95
70. Kost C, Heil M. 2005. Increased availability of extrafloral nectar reduces herbivory in Lima bean plants (Phaseolus lunatu s, Fabaceae). Basic Appl. Ecol. 6:237-48
71. Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J. 2001. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13:2793-807
72. Langenheim JH. 1994. Higher plant terpenoids: a phytocentric overview of their ecological roles. J. Chem. Ecol. 20:1223-80
73. Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor JE, et al. 2008. Isoprene emissions influence herbivore-feeding decisions. Plant Cell Environ. 31:1410-15
74. Leitner M, Boland W, Mithöfer A. 2005. Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol. 167:597-606
75. Leitner M, Kaiser R, Hause B, Boland W, Mithöfer A. 2010. Does mycorrhiza influence herbivoreinduced volatile emission in Medicago truncatula? Mycorrhiza 20:89-101
76. Loivam̈aki M, Mumm R, Dicke M, Schnitzler JP. 2008. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc. Natl. Acad. Sci. USA 105:17430-35
77. Maffei ME. 2010. Sites of synthesi s, biochemistry and functional role of plant volatiles. S. Afr. J. Bot. 76:612-31
78. Maffei ME, Gertsch J, Appendino G. 2011. Plant volatiles: productio n, function and pharmacology. Nat. Prod. Rep. 28:1359-80
79. Maffei ME, Mithöfer A, Boland W. 2007. Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:2946-59
80. Maffei ME, Mithöfer A, Boland W. 2007. Before gene expression: early events in plant-herbivore interactions. Trends Plant Sci. 12:310-16
81. Malcolm SB. 1991. Cardenolide-mediated interactions between plants and herbivores. In Herbivores: Their Interaction with Secondary Plant Metabolite s, ed. GA Rosentha l, MR Berenbau m, 1:251-96. San Diego: Academic. 2nd ed.
82. Matsuki S, Sano Y, Koike T. 2004. Chemical and physical defence in early and late leaves in three heterophyllous birch species native to northern Japan. Ann. Bot. 93:141-47
83. McNaughton SJ, Tarrants JL. 1983. Grass leaf silicification: natural selection for an inducible defense against herbivores. Proc. Natl. Acad. Sci. USA 80:790-91
84. McNaughton SJ, Tarrants JL, McNaughton MM, Davis RH. 1985. Silica as a defense against herbivory and a growth promotor in African grasses. Ecology 66:528-35
85. Mitḧofer A, Boland W, Maffei ME. 2009. Chemical ecology of plant-insect interactions. In Plant Disease Resistanc e, ed. J Parke r, pp. 261-91. Chichester: Wiley-Blackwell
86. Mitḧofer A, Wanner G, Boland W. 2005. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137:1160-68
87. Mooney EH, Tiedeken EJ, Muth NZ, Niesenbaum RA. 2009. Differential induced response to generalist and specialist herbivores by Lindera benzoin (Lauraceae) in sun and shade. Oikos 118:1181-89
88. Moore BD, Foley WJ. 2005. Tree use by koalas in a chemically complex landscape. Nature 435:488-90
89. Morita M, Shitan N, Sawada K, Van Montague MC E, Inze D, et al. 2009. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc. Natl. Acad. Sci. USA 106:2447-52
90. Mumm R, Hilker M. 2006. Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci. 11:351-58
91. Nathanson J. 1984. Caffeine and related methylxanthines: possible naturally occurring pesticides. Science 226:184-87
92. Opitz SE W, M̈uller C. 2009. Plant chemistry and insect sequestration. Chemoecology 19:117-54
93. Osbourn A. 1996. Saponins and plant defence: a soap story. Trends Plant Sci. 1:4-9
94. Ozawa R, Shimoda T, Kawaguchi M, Arimura G, Horiuchi J, et al. 2000. Lotus japonicus infested with herbivorous mites emits volatile compounds that attract predatory mites. J. Plant Res. 113:427-33
95. Phillips MA, Croteau RB. 1999. Resin-based defenses in conifers. Trends Plant Sci. 4:184-90
96. Pichersky E, Lewinsohn E. 2011. Convergent evolution in plant specialized metabolism. Annu. Rev. Plant Biol. 62:549-66
97. Quinn CF, Freeman JL, Reynolds RJ B, Cappa JJ, Fakra SC, et al. 2010. Selenium hyperaccumulation offers protection from cell disruptor herbivores. BMC Ecol. 10:19
98. Radhika V, Kost C, Mithöfer A, Boland W. 2010. Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proc. Natl. Acad. Sci. USA 107:17228-33
99. Raffa KF, Berryman AA. 1983. The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleopter a, Scolytidae). Ecol. Monogr. 53:27-49
100. Rask L, Andreasson E, Ekbom B, Eriksson S, Pontoppidan B, et al. 2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42:93-113
101. Rasmann S, K̈ollner TG, Degenhardt J, Hiltpold I, Toepfer S, et al. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732-37
102. Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J. 2002. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. USA 99:11223-28
103. Renwick JA A, Haribal M, Gouinguene S, Sẗadler E. 2006. Isothiocyanates stimulating oviposition by the diamondback mot h, Plutella xylostella. J. Chem. Ecol. 32:755-66
104. Reynolds OL, Keeoing MG, Meyer JH. 2009. Silicon-augmented resistance of plants to herbivorous insects: a review. Ann. Appl. Biol. 155:171-86
105. Robson F, Okamoto H, Patrick E, Harris S-R, Wasternack C, et al. 2010. Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 22:1143-60
106. R̈oseUS R, Manukian A, Heath RR, Tumlinson JH. 1996. Volatile semiochemicals released from undamaged cotton leaves: a systemic response of living plants to caterpillar damage. Plant Physiol. 111:487-95
107. Ryan CA. 1990. Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425-49
108. Sattelle DB. 1980. Acetylcholine receptors of insects. Adv. Insect Physiol. 15:215-315
109. Schwachtje J, Minchin PE H, Jahnke S, van Dongen JT, Schittko U, Baldwin IT. 2006. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. USA 103:12935-40
110. Scott JG, Wen ZM. 2001. Cytochromes P450 of insects: the tip of the iceberg. Pest Manag. Sci. 57:958-67
111. Self LS, Guthrie FE, Hodgson E. 1964. Metabolism of nicotine by tobacco-feeding insects. Nature 204:300-1
112. Soloway SB. 1976. Naturally occurring insecticides. Environ. Health Perspect. 14:109-17
113. Steppuhn A, Baldwin IT. 2007. Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol. Lett. 10:499-511
114. Stout MJ, Thaler JS, Thomma BPHJ. 2006. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu. Rev. Entomol. 51:663-89
115. Suzuki K, Nakahara T, Kanie O. 2009. 3, 4-Dihydroxypyrrolidine as glycoside inhibitor. Curr. Topics Med. Chem. 9:34-57
116. Textor S, Gershenzon J. 2009. Herbivore induction of the glucosinolate-myrosinase defense system: major trend s, biochemical bases and ecological significance. Phytochem. Rev. 8:149-70
117. Thompson JN. 1994. The Coevolutionary Process. Chicago: Univ. Chicago Press
118. Trewavas A. 1986. Understanding the control of plant development and the role of growth substances. Aust. J. Plant Physiol. 13:447-57
119. Turlings TC J, Tumlinson JH, Lewis WJ. 1990. Exploitation of herbivore-induced plant odors by hostseeking parasitic wasps. Science 250:1251-53
120. Unsicker SB, Kunert G, Gershenzon J. 2009. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 12:479-85
121. van Poecke RM P, Dicke M. 2004. Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biol. 6:387-401
122. Vetter J. 2000. Plant cyanogenic glycosides. Toxicon 38:11-36
123. Weinhold A, Baldwin IT. 2011. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. Natl. Acad. Sci. USA 108:7855-59
124. Winde I, Wittstock U. 2011. Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system. Phytochemistry 72:1566-75
125. Wink M, Schmeller T, Latz-Bruning B. 1998. Modes of action of allelochemical alkaloids: interaction with neuroreceptor s, DN A, and other molecular targets. J. Chem. Ecol. 24:1881-937
126. Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, et al. 2004. Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc. Natl. Acad. Sci. USA 101:4859-64
127. Wittstock U, Gershenzon J. 2002. Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 5:300-7
128. Wittstock U, Halkier BA. 2002. Glucosinolate research in the Arabidopsis era. Trends Plant Sci. 7:263-70
129. Wittstock U, Lichtnow KH, Teuscher ER. 1997. Effects of cicutoxin and related polyacetylenes from Cicuta virosa on neuronal action potentials: a comparative study on the mechanism of the convulsive action. Planta Med. 63:120-24
130. Wu JQ, Baldwin IT. 2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1-24
131. Yazaki K, Sugiyama A, Morita M, Shitan N. 2008. Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochem. Rev. 7:513-24
132. Zagrobelny M, Bak S, Møller BL. 2008. Cyanogenesis in plants and arthropods. Phytochemistry 69:1457-68
133. Zangerl AR, Bazzaz FA. 1992. Theory and pattern in plant defense allocation. In Plant Resistance to Herbivores and Pathogen s, ed. RS Frit z, EL Simm s, pp. 363-91. Chicag o, IL: Univ. Chicago Press
134. Zavala JA, Patankar AG, Gase K, Hui DQ, Baldwin IT. 2004. Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol. 134:1181-90
135. Zhu-Salzman K, Luthe DS, Felton GW. 2008. Arthropod-inducible proteins: broad-spectrum defenses against multiple herbivores. Plant Physiol. 146:852-58
136. Zinn AD, Ward D, Kirkman K. 2007. Inducible defences in Acacia sieberiana in response to giraffe browsing. Afr. J. Range For. Sci. 24:123-29