Herbivore-induced plant volatiles: Targets, perception and unanswered questions

New Phytologist

Volumn 204, Issue 2, 2014, Pages 297-306

  Heil, Martin ^a  

^a DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

Author keywords

Indirect defence; Induced defence; Induced resistance plant plant signalling; Plant volatiles; Tritrophic interaction

Indexed keywords

EID: 84923068070     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1111/nph.12977     Document Type: Review

References (105)

1. Ali M, Sugimoto K, Ramadan A, Arimura G-i. 2013. Memory of plant communications for priming anti-herbivore responses. Scientific Reports 3: art. no. 1872.
2. Alleyne M, Beckage NE. 1997. Parasitism-induced effects on host growth and metabolic efficiency in tobacco hornworm larvae parasitized by Cotesia congregata. Journal of Insect Physiology 43: 407-424.
3. Amo L, Jansen JJ, van Dam NM, Dicke M, Visser ME. 2013. Birds exploit herbivore-induced plant volatiles to locate herbivorous prey. Ecology Letters 16: 1348-1355.
4. Arimura G-I, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J. 2000. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406: 512-515.
5. Baldwin IT, Schultz JC. 1983. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221: 277-279.
6. Ballhorn DJ, Kautz S, Heil M. 2013. Distance and sex determine host plant choice by herbivorous beetles. PLoS ONE 8: e55602.
7. Bate NJ, Rothstein SJ. 1998. C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant Journal 16: 561-569.
8. Bedoya-Perez MA, Isler I, Banks PB, McArthur C. 2014. Roles of the volatile terpene, 1,8-cineole, in plant-herbivore interactions: a foraging odor cue as well as a toxin? Oecologia 174: 827-837.
9. Benrey B, Callejas A, Rios L, Oyama K, Denno RF. 1998. The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biological Control 11: 130-140.
10. Birkett MA, Campbell CAM, Chamberlain K, Guerrieri E, Hick AJ, Martin JL, Matthes M, Napier JA, Pettersson J, Pickett JA et al. 2000. New roles for cis-jasmone as an insect semiochemical and in plant defense. Proceedings of the National Academy of Sciences, USA 97: 9329-9334.
11. Blande JD, Holopainen JK, Li T. 2010. Air pollution impedes plant-to-plant communication by volatiles. Ecology Letters 13: 1172-1181.
12. Blassioli Moraes MC, Birket MA, Gordon-WeeksR, Smart LE, Martin JL, Pye BJ, Bromilow R, Pickett JA. 2007. cis-Jasmone induces accumulation of defence compounds in wheat, Triticum aestivum. Phytochemistry 69: 9-17.
13. Braasch J, Kaplan I. 2012. Over what distance are plant volatiles bioactive? Estimating the spatial dimensions of attraction in an arthropod assemblage. Entomologia Experimentalis et Applicata 145: 115-123.
14. Brillada C, Nishihara M, Shimoda T, Garms S, Boland W, Maffei ME, Arimura G-i. 2013. Metabolic engineering of the C16 homoterpene TMTT in Lotus japonicus through overexpression of (E,E)-geranyllinalool synthase attracts generalist and specialist predators in different manners. New Phytologist 200: 1200-1211.
15. Bruce TJA, Matthes MC, Chamberlain K, Woodcock CM, Mohib A, Webster B, Smart LE, Birkett MA, Pickett JA, Napier JA. 2008. cis-Jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proceedings of the National Academy of Sciences, USA 105: 4553-4558.
16. D'Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TCJ. 2014. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant, Cell&Environment 37: 813-826.
17. Dambolena JS, Lopez AG, Canepa MC, Theumer MG, Zygadlo JA, Rubinstein HR. 2008. Inhibitory effect of cyclic terpenes (limonene, menthol, menthone and thymol) on Fusarium verticillioides MRC 826 growth and fumonisin B1 biosynthesis. Toxicon 51: 37-44.
18. Dicke M, Sabelis MW. 1988. How plants obtain predatory mites as bodyguards. Netherlands Journal of Zoology 38: 148-165.
19. Dolch R, Tscharntke T. 2000. Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours. Oecologia 125: 504-511.
20. Drukker B, Scutareanu P, Sabelis MW. 1995. Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions? Entomologia Experimentalis et Applicata 77: 193-203.
21. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. 2004. Airborne signals prime plants against insect herbivore attack. Proceedings of the National Academy of Sciences, USA 101: 1781-1785.
22. Frost C, Appel H, Carlson J, De Moraes C, Mescher M, Schultz J. 2007. Within-plant signalling by volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecology Letters 10: 490-498.
23. García-Guzmán G, Heil M. 2014. Life histories of hosts and pathogens predict patterns in tropical fungal plant diseases. New Phytologist 201: 1106-1120.
24. Géneau CE, Wäckers FL, Luka H, Daniel C, Balmer O. 2012. Selective flowers to enhance biological control of cabbage pests by parasitoids. Basic and Applied Ecology 13: 85-93.
25. Girón-Calva PS, Molina-Torres J, Heil M. 2012. Volatile dose and exposure time impact perception in neighboring plants. Journal of Chemical Ecology 38: 226-228.
26. Glinwood R, Ninkovic V, Pettersson J, Ahmed E. 2004. Barley exposed to aerial allelopathy from thistles (Cirsium spp.) becomes less acceptable to aphids. Ecological Entomology 29: 188-195.
27. Goodrich-Tanrikulu M, Mahoney NE, Rodriguez SB. 1995. The plant growth regulator methyl jasmonate inhibits aflatoxin production by Aspergillus flavus. Microbiology 141: 2831-2837.
28. Gouinguené S, Degen T, Turlings TCJ. 2001. Variability in herbivore-induced odour emissions among maize cultivars and their wild ancestors (teosinte). Chemoecology 11: 9-16.
29. Halloran ST, Mauck KE, Fleisher SF, Tumlinson JH. 2013. Volatiles from intact and Lygus-damaged Erigeron annuus (L.) Pers. are highly attractive to ovipositing Lygus and its parasitoid Peristenus relictus Ruthe. Journal of Chemical Ecology 39: 1115-1128.
30. Harvey JA, Sano T, Tanaka T. 2010. Differential host growth regulation by the solitary endoparasitoid, Meteorus pulchricornis in two hosts of greatly differing mass. Journal of Insect Physiology 56: 1178-1183.
31. Hassanali A, Herren H, Khan ZR, Pickett JA, Woodcock CM. 2008. Integrated pest management: the push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philosophical Transactions of the Royal Society B 363: 611-621.
32. Heil M. 2009. Damaged-self recognition in plant herbivore defence. Trends in Plant Science 14: 356-363.
33. Heil M, Adame-Álvarez RM. 2010. Short signalling distances make plant communication a soliloquy. Biology Letters 6: 843-845.
34. Heil M, Karban R. 2010. Explaining evolution of plant communication by airborne signals. Trends in Ecology&Evolution 25: 137-144.
35. Heil M, Kost C. 2006. Priming of indirect defences. Ecology Letters 9: 813-817.
36. Heil M, Lion U, Boland W. 2008. Defence-inducing volatiles: in search for the active motif. Journal of Chemical Ecology 34: 601-604.
37. Heil M, Silva Bueno JC. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proceedings of the National Academy of Sciences, USA 104: 5467-5472.
38. HershMH, Vilgalys R, Clark JS. 2012. Evaluating the impacts ofmultiple generalist fungal pathogens on temperate tree seedling survival. Ecology 93: 511-520.
39. Himanen SJ, Blande JD, Klemola T, Pulkkinen J, Heijari J, Holopainen JK. 2010. Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants - a mechanism for associational herbivore resistance? New Phytologist 186: 722-732.
40. Holopainen JK, Blande JD. 2013. Where do herbivore-induced plant volatiles go? Frontiers in Plant Science 4: art. no 185.
41. James DG. 2003. Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environmental Entomology 32: 977-982.
42. Kaplan I. 2012a. Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biological Control 60: 77-89.
43. Kaplan I. 2012b. Trophic complexity and the adaptive value of damage-induced plant volatiles. PLoS Biology 10: e1001437.
44. Karban R, Baldwin I, Baxter K, Laue G, Felton G. 2000. Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125: 66-71.
45. Karban R, Shiojiri K. 2009. Self-recognition affects plant communication and defense. Ecology Letters 12: 502-506.
46. Karban R, Shiojiri K, Huntzinger M, McCall AC. 2006. Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87: 922-930.
47. Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY. 2013. Kin recognition affects plant communication and defence. Proceedings of the Royal Society B 280: art. no 20123062.
48. Karban R, Yang LH, Edwards KF. 2014. Volatile communication between plants that affects herbivory: a meta-analysis. Ecology Letters 17: 44-52.
49. Kessler A, Baldwin IT. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291: 2141-2144.
50. Kessler A, Halitschke R, Diezel C, Baldwin IT. 2006. Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148: 280-292.
51. Khan ZR, AmpongNyarko K, Chiliswa P, Hassanali A, Kimani S, Lwande W, Overholt WA, Pickett JA, Smart LE, Wadhams LJ et al. 1997. Intercropping increases parasitism of pests. Nature 388: 631-632.
52. Kishimoto K, Matsui K, Ozawa R, Takabayashi J. 2005. Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant and Cell Physiology 46: 1093-1102.
53. Knolhoff LM, Heckel DG. 2014. Behavioral assays for studies of host plant choice and adaptation in herbivorous insects. Annual Review of Entomology 59: 263-278.
54. Kost C, Heil M. 2006. Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. Journal of Ecology 94: 619-628.
55. Liu X, Liang M, Etienne RS, Wang Y, Staehelin C, Yu S. 2012. Experimental evidence for a phylogenetic Janzen-Connell effect in a subtropical forest. Ecology Letters 15: 111-118.
56. Loughrin J, Manukian A, Heath R, Tumlinson J. 1995. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. Journal of Chemical Ecology 21: 1217-1227.
57. Maffei M, Camusso W, Sacco S. 2001. Effect of Mentha9piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochemistry 58: 703-707.
58. Maffei ME, Bossi S. 2006. Electrophysiology and plant responses to biotic stress. In: Volkov A, ed. Plant electrophysiology - theory and methods. Berlin/ Heidelberg, Germany: Springer, 461-481.
59. Maffei ME, Mithöfer A, Boland W. 2007. Before gene expression: early events in plant-insect interaction. Trends in Plant Science 12: 310-316.
60. Mallinger RE, Hogg DB, Gratton C. 2011. Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. Journal of Economic Entomology 104: 115-124.
61. Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T, Piirtola P, Klemola T. 2008. From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 3: e2832.
62. Mäntylä E, Blande JD, Klemola T. 2014. Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? Arthropod-Plant Interactions 8: 143-153.
63. von Merey GE, Veyrat N, de Lange E, Degen T, Mahuku G, Lopez Valdez R, Turlings TCJ, D'Alessandro M. 2012. Minor effects of two elicitors of insect and pathogen resistance on volatile emissions and parasitism of Spodoptera frugiperda in Mexican maize fields. Biological Control 60: 7-15.
64. vonMérey G, Veyrat N, Mahuku G, Valdez RL, Turlings TCJ, D'Alessandro M. 2011. Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects. Phytochemistry 72: 1838-1847.
65. Mooney KA, Linhart YB. 2006. Contrasting cascades: insectivorous birds increase pine but not parasitic mistletoe growth. Journal of Animal Ecology 75: 350-357.
66. de Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393: 570-573.
67. de Moraes CM, Mescher MC, Tumlinson JH. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410: 577-580.
68. Ninkovic V, Al Abassi S, Pettersson J. 2001. The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biological Control 21: 191-195.
69. Olson DM, Wäckers FL. 2007. Management of field margins to maximize multiple ecological services. Journal of Applied Ecology 44: 13-21.
70. Orre-Gordon G, Wratten SD, Jonsson M, Simpson M, Hale R. 2013. 'Attract and reward': combining a herbivore-induced plant volatile with floral resource supplementation - multi-trophic level effects. Biological Control 64: 106-115.
71. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318: 113-116.
72. Penaflor MFGV, Bento JMS. 2013. Herbivore-induced plant volatiles to enhance biological control in agriculture. Neotropical Entomology 42: 331-343.
73. Peñuelas J, Llusiá J. 2004. Plant VOC emissions: making use of the unavoidable. Trends in Ecology&Evolution 19: 402-404.
74. Pineda A, Soler R, Weldegergis BT, Shimwela MM, Van Loon JJA, Dicke M. 2013. Non-pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid-induced plant volatiles via jasmonic acid signalling. Plant, Cell & Environment 36: 393-404.
75. Pineda A, Zheng S-J, van Loon JJA, Pieterse CMJ, Dicke M. 2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in Plant Science 15: 507-514.
76. Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, Jongema Y, van Loon JJA, Vet LEM, Harvey JA, Dicke M. 2012. Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biology 10: e1001435.
77. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiology 158: 854-863.
78. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737.
79. Rhoades DF. 1983. Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In: Hedin PA, ed. Plant Resistance to insects. Washington, DC, USA: American Chemical Society, 55-68.
80. Rodríguez-Saona CR, Rodríguez-Saona LE, Frost CJ. 2009. Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. Journal of Chemical Ecology 35: 163-175.
81. Rostas M, Maag D, Ikegami M, Inbar M. 2013. Gall volatiles defend aphids against a browsing mammal. BMC Evolutionary Biology 13: 193.
82. Runyon JB, Mescher MC, De Moraes CM. 2006. Volatile chemical cues guide host location and host selection by parasitic plants. Science 313: 1964-1967.
83. Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC. 2013. Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. International Journal of Molecular Sciences 14: 17 781-17 811.
84. Shiojiri K, Ozawa R, Matsui K, Sabelis MW, Takabayashi J. 2012. Intermittent exposure to traces of green leaf volatiles triggers a plant response. Scientific Reports 2: art. no 378.
85. Shulaev V, Silverman P, Raskin I. 1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385: 718-721.
86. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI, Orre GUS. 2011. Field evaluation of the 'attract and reward' biological control approach in vineyards. Annals of Applied Biology 159: 69-78.
87. Smart LE, Martin JL, Limpalaer M, Bruce TJA, Pickett JA. 2013. Responses of herbivore and predatory mites to tomato plants exposed to jasmonic acid seed treatment. Journal of Chemical Ecology 39: 1297-1300.
88. Thaler JS. 1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399: 686-688.
89. Ton J, D'Allesandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant Journal 49: 16-26.
90. Turlings TCJ, Loughrin JH, McCall PJ, Röse USR, Lewis WJ, Tumlinson JH. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proceedings of the National Academy of Sciences, USA 92: 4169-4174.
91. Turlings TCJ, Tumlinson JH, Lewis WJ. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253.
92. Uefune M, Choh Y, Abe J, Shiojiri K, Sano K, Takabayashi J. 2012. Application of synthetic herbivore-induced plant volatiles causes increased parasitism of herbivores in the field. Journal of Applied Entomology 136: 561-567.
93. Van Dam NM, Heil M. 2011. Multitrophic interactions below and above ground: en route to the next level. Journal of Ecology 99: 77-88.
94. Vieira CR, Blassioli Moraes MC, Borges M, Sujii ER, Laumann RA. 2013. cis-Jasmone indirect action on egg parasitoids (Hymenoptera: Scelionidae) and its application in biological control of soybean stink bugs (Hemiptera: Pentatomidae). Biological Control 64: 75-82.
95. Vivas M, Martin JA, Gil L, Solla A. 2012. Evaluating methyl jasmonate for induction of resistance to Fusarium oxysporum, F. circinatum and Ophiostoma novo-ulmi. Forest Systems 21: 289-299.
96. Wasternack C. 2007. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Annals of Botany 100: 681-697.
97. Wu JQ, Baldwin IT. 2010. New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics 44: 1-24.
98. Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L, Hu L, Li J, Han X, Zhang T, Lu J et al. 2012. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecology Letters 15: 1130-1139.
99. Yi H-S, Heil M, Adame-Álvarez R-M, Ballhorn D, Ryu C-M. 2009. Airborne induction and priming of plant resistance to a bacterial pathogen. Plant Physiology 151: 2152-2161.
100. Yuan ZL, Zhang CL, Lin FC. 2010. Role of diverse non-systemic fungal endophytes in plant performance and response to stress: progress and approaches. Journal of Plant Growth Regulation 29: 116-126.
101. Yue Q, Wang CL, Gianfagna TJ, Meyer WA. 2001. Volatile compounds of endophyte-free and infected tall fescue (Festuca arundinacea Schreb.). Phytochemistry 58: 935-941.
102. Zakir A, Bengtsson M, Sadek MM, Hansson BS, Witzgall P, Anderson P. 2013a. Specific response to herbivore-induced de novo synthesized plant volatiles provides reliable information for host plant selection in a moth. Journal of Experimental Biology 216: 3257-3263.
103. Zakir A, Sadek MM, Bengtsson M, Hansson BS, Witzgall P, Anderson P. 2013b. Herbivore-induced plant volatiles provide associational resistance against an ovipositing herbivore. Journal of Ecology 101: 410-417.
104. Zebelo SA, Matsui K, Ozawa R, Maffei ME. 2012. Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Science 196: 93-100.
105. Zhang ZZ, Li YB, Qi L, Wan XC. 2006. Antifungal activities of major tea leaf volatile constituents toward Colletorichum camelliae Massea. Journal of Agricultural and Food Chemistry 54: 3936-3940.