Plant interactions with multiple insect herbivores: From community to genes

Annual Review of Plant Biology

Volumn 65, Issue , 2014, Pages 689-713

  Stam, Jeltje M ^a   Kroes, Anneke ^a   Li, Yehua ^a   Gols, Rieta ^a   Van Loon, Joop J A ^a   Poelman, Erik H ^a   Dicke, Marcel ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

phenotypic plasticity; phytohormones; species interactions; systems biology; trait mediated interaction networks

Indexed keywords

ANIMAL; ECOSYSTEM; GENETICS; HERBIVORY; INSECT; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; REVIEW;

ANIMALS; ECOSYSTEM; HERBIVORY; INSECTS; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS;

EID: 84899725098     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-050213-035937     Document Type: Review

References (149)

1. Agrawal AA. 2000. Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493-500
2. Agrawal AA. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol. Ecol. Res. 7:651-67
3. Agrawal AA, Karban R, Colfer RG. 2000. Howleaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89:70-80
4. Ali JG, Agrawal AA. 2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17:293-302
5. Andow DA. 1991. Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36:561-86
6. Baldwin IT. 2012. Training a new generation of biologists: the genome-enabled field biologists. Proc. Am. Philos. Soc. 156:205-14
7. Barbour RC, O'Reilly-Wapstra JM, De Little DW, Jordan GJ, Steane DA, et al. 2009. A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology 90:1762-72
8. Benrey B, Denno RF. 1997. The slow growth highmortality hypothesis: a test using the cabbage butterfly. Ecology 78:987-99
9. Bidart-Bouzat MG, Kliebenstein D. 2011. An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167:677-89
10. Bonaventure G, Van Doorn A, Baldwin IT. 2011. Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci. 16:294-99
11. Braasch J, Wimp GM, Kaplan I. 2012. Testing for phytochemical synergism: arthropod community responses to induced plant volatile blends across crops. J. Chem. Ecol. 38:1264-75
12. Broekgaarden C, Poelman EH, Voorrips RE, Dicke M, Vosman B. 2010. Intraspecific variation in herbivore community composition and transcriptional profiles in field-grown Brassica oleracea cultivars. J. Exp. Bot. 61:807-19
13. Bukovinszky T, Gols R, Kamp A, de Oliveira-Domingues F, Hambäck PA, et al. 2010. Combined effects of patch size and plant nutritional quality on local densities of insect herbivores. Basic Appl. Ecol. 11:396-405
14. Bukovinszky T, Gols R, Smid HM, Bukovinskiné Kiss G, Dicke M, Harvey JA. 2012. Consequences of constitutive and induced variation in the host's food plant quality for parasitoid larval development. J. Insect Physiol. 58:367-75
15. Bukovinszky T, Poelman EH, Gols R, Prekatsakis G, Vet LEM, et al. 2009. Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299-308
16. Bukovinszky T, van Veen FJF, Jongema Y, Dicke M. 2008. Direct and indirect effects of resource quality on food web structure. Science 319:804-7
17. Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M, et al. 2012. Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol. 158:2042-52
18. D'Alessandro M, Turlings TCJ. 2006. Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24-32
19. De Rijk M, Dicke M, Poelman EH. 2013. Foraging behaviour by parasitoids in multiherbivore communities. Anim. Behav. 85:1517-28
20. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, et al. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18:923-37
21. De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M, et al. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142:352-63
22. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 2011. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156
23. Denno RF, McClure MS, Ott JR. 1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu. Rev. Entomol. 40:297-331
24. Dicke M, Baldwin IT. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the "cry for help." Trends Plant Sci. 15:167-75
25. Dicke M, van Loon JJA, Soler R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5:317-24
26. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT. 2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150:1576-86
27. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard Ja, Ross JJ, et al. 2007. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225-45
28. Durrant WE, Dong X. 2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185-209
29. Dussourd DE. 1995. Entrapment of aphids and whiteflies in lettuce latex. Ann. Entomol. Soc. Am. 88:163-72
30. Ehlting J, Chowrira SG, Mattheus N, Aeschliman DS, Arimura G, Bohlmann J. 2008. Comparative transcriptome analysis of Arabidopsis thaliana infested by diamond back moth (Plutella xylostella) larvae reveals signatures of stress response, secondary metabolism, and signalling. BMC Genomics 9:154
31. Erb M, Foresti N, Turlings TCJ. 2010. A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biol. 10:247
32. Erb M, Meldau S, Howe GA. 2012. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17:250-59
33. Erb M, Robert CAM, Hibbard BE, Turlings TCJ. 2011. Sequence of arrival determines plant-mediated interactions between herbivores. J. Ecol. 99:7-15
34. Felton GW, Tumlinson JH. 2008. Plant-insect dialogs: complex interactions at the plant-insect interface. Curr. Opin. Plant Biol. 11:457-63
35. Fritz RS, McDonough SE, Rhoads AG. 1997. Effects of plant hybridization on herbivore-parasitoid interactions. Oecologia 110:360-67
36. Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M. 2013. Cytokinins as key regulators in plantmicrobe-insect interactions: connecting plant growth and defence. Funct. Ecol. 27:599-609
37. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205-27
38. Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA. 2008. Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J. Chem. Ecol. 34:132-43
39. Gols R, Harvey JA. 2009. Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids. Phytochem. Rev. 8:187-206
40. Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke M, et al. 2008. Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89:1616-26
41. Hartley SE, Gange AC. 2009. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu. Rev. Entomol. 54:323-42
42. Harvey JA, van Dam NM, Raaijmakers CE, Bullock JM, Gols R. 2011. Tri-trophic effects of inter-and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea). Oecologia 166:421-31
43. Harvey JA, Wagenaar R, Bezemer TM. 2009. Interactions to the fifth trophic level: secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources. J. Anim. Ecol. 78:686-92
44. Haukioja E. 1980. On the role of plant defences in the fluctuation of herbivore populations. Oikos 35:202-13
45. Heidel AJ, Baldwin IT. 2004. Microarray analysis of salicylic acid-and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ. 27:1362-73
46. Heil M. 2008. Indirect defence via tritrophic interactions. New Phytol. 178:41-61
47. Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE. 2001. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc. Natl. Acad. Sci. USA 98:1083-88
48. Hilker M, Meiners T. 2010. How do plants "notice" attack by herbivorous arthropods? Biol. Rev. 85:267-80
49. 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
50. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41-66
51. Hunter MD, Price PW. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottomup and top-down forces in natural communities. Ecology 73:724-32
52. Johnson MTJ. 2008. Bottom-up effects of plant genotype on aphids, ants, and predators. Ecology 89:145-54
53. Johnson MTJ, Agrawal AA. 2005. Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874-85
54. Johnson MTJ, Agrawal AA. 2007. Covariation and composition of arthropod species across plant genotypes of evening primrose (Oenothera biennis). Oikos 116:941-56
55. Johnson MTJ, Lajeunesse MJ, Agrawal AA. 2006. Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol. Lett. 9:24-34
56. Kahl J, Siemens DH, Aerts RJ, Gabler R, Kuhnemann F, et al. 2000. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336-42
57. Kant MR, Sabelis MW, Haring MA, Schuurink RC. 2008. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc. R. Soc. B 275:443-52
58. Kaplan I, Denno RF. 2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett. 10:977-94
59. Karban R, Agrawal AA. 2002. Herbivore offense. Annu. Rev. Ecol. Syst. 33:641-64
60. Karban R, Agrawal AA, Mangel M. 1997. The benefits of induced defenses against herbivores. Ecology 78:1351-55
61. Karban R, Baldwin IT. 1997. Induced Responses to Herbivory. Chicago: Chicago Univ. Press
62. Kareiva P, Sahakian R. 1990. Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433-34
63. Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M, et al. 2012. Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Interact. 6:221-30
64. Kazana E, Pope TW, Tibbles L, Bridges M, Pickett JA, et al. 2007. The cabbage aphid: awalkingmustard oil bomb. Proc. R. Soc. B 274:2271-77
65. Keith AR, Bailey JK, Whitham TG. 2010. A genetic basis to community repeatability and stability. Ecology 91:3398-406
66. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299-328
67. Kessler A, Baldwin IT. 2004. Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J. 38:639-49
68. Kessler A, Halitschke R, Baldwin IT. 2004. Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665-68
69. Kessler A, Halitschke R, Poveda K. 2011. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769-80
70. Keurentjes JJB, Angenent GC, Dicke M, Dos Santos V, Molenaar J, et al. 2011. Redefining plant systems biology: from cell to ecosystem. Trends Plant Sci. 16:183-90
71. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, et al. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147:1358-68
72. Kos M, Broekgaarden C, Kabouw P, Lenferink KO, Poelman EH, et al. 2011. Relative importance of plant-mediated bottom-up and top-down forces on herbivore abundance on Brassica oleracea. Funct. Ecol. 25:1113-24
73. Kuśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM. 2008. Towards global understanding of plant defence against aphids-timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ. 31:1097-115
74. Leimu R, Koricheva J. 2006. Ameta-analysis of genetic correlations between plant resistances to multiple enemies. Am. Nat. 168:E15-37
75. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, et al. 2009. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149:1797-809
76. Lorenzo O, Chico JM, Sa JJ. 2004. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938-50
77. Lucas-Barbosa D, van Loon JJA, Dicke M. 2011. The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647-54
78. Maffei ME, Arimura G, Mithöfer A. 2012. Natural elicitors, effectors and modulators of plant responses. Nat. Prod. Rep. 29:1288-303
79. Maffei ME, Mithöfer A, Boland W. 2007. Before gene expression: early events in plant-insect interaction. Trends Plant Sci. 12:310-16
80. McCormick AC, Unsicker SB, Gershenzon J. 2012. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 17:303-10
81. Memelink J. 2009. Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560-70
82. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M, et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097-100
83. Miller-Pierce MR, Preisser EL. 2012. Asymmetric priority effects influence the success of invasive forest insects. Ecol. Entomol. 37:350-58
84. Mithöfer A, Boland W. 2012. Plant defense against herbivores: chemical aspects. Annu. Rev. Plant Biol. 63:431-50
85. Moran PJ, Cheng Y, Cassell JL, Thompson GA. 2002. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch. Insect Biochem. Physiol. 51:182-203
86. Müller C. 2009. Interactions between glucosinolate-and myrosinase-containing plants and the sawfly Athalia rosae. Phytochem. Rev. 8:121-34
87. Newton EL, Bullock JM, Hodgson DJ. 2009. Bottom-up effects of glucosinolate variation on aphid colony dynamics in wild cabbage populations. Ecol. Entomol. 34:614-23
88. Newton EL, Bullock JM, Hodgson DJ. 2009. Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63-76
89. Ode PJ. 2006. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51:163-85
90. Ohgushi T. 2005. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu. Rev. Ecol. Evol. Syst. 36:81-105
91. Ohgushi T. 2008. Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomol. Exp. Appl. 128:217-29
92. Pieterse CMJ, Dicke M. 2007. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci. 12:564-69
93. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SC. 2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308-16
94. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC. 2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489-521
95. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M. 2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15:507-14
96. Poelman EH, Broekgaarden C, van Loon JJA, Dicke M. 2008. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol. Ecol. 17:3352-65
97. Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, et al. 2012. Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol. 10:e1001435
98. Poelman EH, van Dam NM, van Loon JJA, Vet LEM, Dicke M. 2009. Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90:1863-77
99. Poelman EH, van Loon JJA, Dicke M. 2008. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13:534-41
100. Poelman EH, van Loon JJA, van Dam NM, Vet LEM, Dicke M. 2010. Herbivore-induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack. Ecol. Entomol. 35:240-47
101. Poelman EH, Zheng SJ, Zhang Z, Heemskerk NM, Cortesero AM, Dicke M. 2011. Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc. Natl. Acad. Sci. USA 108:19647-52
102. Ponzio C, Gols R, Pieterse CMJ, Dicke M. 2013. Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct. Ecol. 27:587-98
103. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. 1980. Interactions among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41-65
104. Reymond P. 2013. Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238:247-58
105. Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE. 2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132-47
106. Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 36: 1043-57
107. Romero GQ, Benson WW. 2005. Biotic interactions of mites, plants and leaf domatia. Curr. Opin. Plant Biol. 8:436-40
108. Sanders D, Sutter L, van Veen FJF. 2013. The loss of indirect interactions leads to cascading extinctions of carnivores. Ecol. Lett. 16:664-69
109. Schoonhoven LM, van Loon JJA, Dicke M. 2005. Insect-Plant Biology. Oxford, UK: Oxford Univ. Press
110. Schweitzer JA, Madritch MD, Bailey JK, LeRoy CJ, Fischer DG, et al. 2008. From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005-20
111. Scriber JM, Slansky F. 1981. The nutritional ecology of immature insects. Annu. Rev. Entomol. 26:183-211
112. Shiojiri K, Takabayashi J, Yano S, Takafuji A. 2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43:23-29
113. Smith DS, Bailey JK, Shuster SM, Whitham TG. 2011. A geographic mosaic of trophic interactions and selection: trees, aphids and birds. J. Evol. Biol. 24:422-29
114. Snoeren TAL, Mumm R, Poelman EH, Yang Y, Pichersky E, Dicke M. 2010. The herbivore-induced plant volatile methyl salicylate negatively affects attraction of the parasitoid Diadegma semiclausum. J. Chem. Ecol. 36:479-89
115. Soler R, Erb M, Kaplan I. 2013. Long distance root-shoot signalling in plant-insect community interactions. Trends Plant Sci. 18:149-56
116. Soler R, Badenes-Pérez FR, Broekgaarden C, Zheng S-J, David A, et al. 2012. Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription. Funct. Ecol. 26:156-66
117. Staswick PE, Tiryaki I. 2004. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117-27
118. Stireman JO, Nason JD, Heard SB, Seehawer JM. 2006. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc. R. Soc. Lond. B 273:523-30
119. Tack AJM, Dicke M. 2013. Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct. Ecol. 27:633-45
120. Thaler JS. 1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686-88
121. Thaler JS. 2002. Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J. Anim. Ecol. 71:141-50
122. Thaler JS, Fidantsef AL, Bostock RM. 2002. Antagonism between jasmonate-and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J. Chem. Ecol. 28:1131-59
123. Thaler JS, Humphrey PT, Whiteman NK. 2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17:260-70
124. Thaler JS, McArt SH, Kaplan I. 2012. Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging. Proc. Natl. Acad. Sci. USA 109:12075-80
125. Thaler JS, Stout MJ, Karban R, Duffey SS. 2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol. Entomol. 26:312-24
126. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, et al. 2007. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661-65
127. Tooker JF, DeMoraes CM. 2008. Gall insects and indirect plant defenses: a case of active manipulation? Plant Signal. Behav. 3:503-4
128. Underwood N. 2012. When herbivores come back: effects of repeated damage on induced resistance. Funct. Ecol. 26:1441-49
129. Utsumi S, Ando Y, Miki T. 2010. Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Popul. Ecol. 52:485-97
130. Utsumi S, Ohgushi T. 2008. Host plant variation in plant-mediated indirect effects: moth boring-induced susceptibility of willows to a specialist leaf beetle. Ecol. Entomol. 33:250-60
131. van Veen FJF, Morris RJ, Godfray HCJ. 2006. Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu. Rev. Entomol. 51:187-208
132. van Veen FJF, van Holland PD, Godfray HCJ. 2005. Stable coexistence in insect communities due to density-and trait-mediated indirect effects. Ecology 86:3182-89
133. Van Zandt PA, Agrawal AA. 2004. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616-29
134. Van Zandt PA, Agrawal AA. 2004. Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca. Oikos 104:401-9
135. Viswanathan DV, Lifchits OA, Thaler JS. 2007. Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389-99
136. Viswanathan DV, Narwani AJT, Thaler JS. 2005. Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886-96
137. Voelckel C, Baldwin IT. 2004. Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J. 38:650-63
138. Vrieling K, Smit W, van der Meijden E. 1991. Tritrophic interactions between aphids (Aphis jacobaeae Schrank), ant species, Tyria jacobaeae L., and Senecio jacobaea L. lead to maintenance of genetic variation in pyrrolizidine alkaloid concentration. Oecologia 86:177-82
139. Wang D, Amornsiripanitch N, Dong X. 2006. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathol. 2:e123
140. Wang X, Hu L, Zhou G, Cheng J, Lou Y. 2011. Salicylic acid and ethylene signaling pathways are involved in production of rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenée). Chin. Sci. Bull. 56:2351-58
141. Webster B, Bruce T, Pickett J, Hardie J. 2010. Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim. Behav. 79:451-57
142. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, et al. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7:510-23
143. Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM, et al. 2012. Community specificity: life and afterlife effects of genes. Trends Plant Sci. 17:271-81
144. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-65
145. Wu JQ, Baldwin IT. 2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1-24
146. Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L, et al. 2012. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol. Lett. 15:1130-39
147. Zarate SI, Kempema LA, Walling LL. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143:866-75
148. Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, van Loon JJA, et al. 2013. Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol. 197:1291-99
149. Zhang PJ, Zheng SJ, van Loon JJA, Boland W, David A, et al. 2009. Whiteflies interfere with volatile. indirect plant defense against spider mites in Lima bean. Proc. Natl. Acad. Sci. USA 106:21202-7