Volatile induction of infected and neighbouring uninfected plants potentially influence attraction/repellence of a cereal herbivore

Journal of Applied Entomology

Volumn 137, Issue 4, 2013, Pages 296-309

  Piesik, D ^a   Panka D ^a   Jeske, M ^a   Wenda Piesik, A ^a   Delaney, K J ^b   Weaver, D K ^c  

^a UNIVERSITY OF TECHNOLOGY AND LIFE SCIENCES   (Poland)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c MONTANA STATE UNIVERSITY   (United States)

Author keywords

Cereal; Fusarium; Herbivore; Odour; Pathogen; Volatile

Indexed keywords

ACETATE; BEETLE; CEREAL; CONCENTRATION (COMPOSITION); DOSE-RESPONSE RELATIONSHIP; FUNGAL DISEASE; HERBIVORY; HOST PLANT; HOST-PATHOGEN INTERACTION; INOCULATION; ODOR; PHYSIOLOGICAL RESPONSE; PLANT-HERBIVORE INTERACTION; TERPENE; VOLATILE ORGANIC COMPOUND;

CHRYSOMELIDAE; COLEOPTERA; CYANELLA; FUSARIUM; FUSARIUM CULMORUM; HORDEUM; OULEMA; OULEMA MELANOPUS; TRITICUM AESTIVUM; ZEA MAYS;

EID: 84876156643     PISSN: 09312048     EISSN: 14390418     Source Type: Journal    
DOI: 10.1111/j.1439-0418.2012.01742.x     Document Type: Article

References (76)

1. Alvarez-Castellanos PP, Bishop CD, Pascual-Villalobos MJ, 2001. Antifungal activity of the essential oil of flowerheads of garland chrysanthemum (Chrysanthemum coronarium) against agricultural pathogens. Phytochemistry 57, 99-102.
2. Arimura G, Kost C, Boland W, 2005. Herbivore-induced, indirect plant defences. Biochim. Biophys. Acta 1734, 91-111.
3. Arimura G, Matsui K, Takabayashi J, 2009. Chemical and molecular ecology of herbivore-induce plant volatiles: proximate factors and their ultimate functions. Plant Cell Phys. 50, 911-923.
4. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA, 2006. Volatile signaling plant-plant interactions: "talking trees" in the genomics era. Science 311, 812-815.
5. Beale MH, Birkett MA, Bruce TJA, Chamberlain K, Field LM, Huttly AK, Martin JL, Parker R, Phillips AL, Pickett JA, Prosser IM, Shewry PR, Smart LE, Wadhams LJ, Woodcock CM, Zhang Y, 2006. Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc. Natl. Acad. Sci. USA 103, 10509-10513.
6. Bonello P, McNee WR, Storer AJ, Wood DL, Gordon TR, 2001. The role of olfactory stimuli in the location of weakened hosts by twig-infesting Pityophthorus spp. Ecol. Entomol. 26, 8-15.
7. Booth C, 1971. The genus Fusarium. Commonwealth Mycological Institute, Kew, Surrey, UK, 1-237.
8. Buntin GD, Flanders KL, Slaughter RW, De Lamar ZD, 2004. Damage loss assessment and control of the cereal leaf beetle (Coleoptera: Chrysomelidae) in winter wheat. J. Econ. Entomol. 97, 374-382.
9. Burgess LW, 1981. General Ecology. In: Fusarium diseases, Biology and Taxonomy. Ed. by Nelson PE, Toussoun TA, Cook RJ, The Pennsylvania State University Press, University Park, 225-235.
10. Cardoza YJ, Albron HT, Tumlinson JH, 2002. In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J. Chem. Ecol. 28, 161-174.
11. Choh Y, Shimoda T, Ozawa R, Dicke M, Takabayashi J, 2004. Exposure of lima bean leaves to volatiles from herbivore-induced conspecific plants results in emission of carnivore attractants: active or passive process? J. Chem. Ecol. 30, 1305-1317.
12. Cook RJ, 1980. Fusarium foot rot of wheat and its control in the Pacific Northwest. Plant Dis. 64, 1061-1066.
13. D'Alessandro M, Turlings TCJ, 2005. In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatile organic compounds to parasitic wasps. Chem. Senses 30, 739-753.
14. De Lacy Costello BPJ, Evans P, Ewen RJ, Gunson HE, Jones PRH, Ratcliffe NM, Spencer-Phillips PTN, 2001. Gas chromatography-mass spectrometry analyses of volatile organic compounds from potato tubers inoculated with Phytophthora infestans or Fusarium coeruleum. Plant. Pathol. 50, 489-496.
15. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH, 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393, 570-573.
16. De Moraes CM, Mescher MC, Tumlinson JH, 2001. Caterpillar-induced nocturnal plant volatiles repel nonspecific females. Nature 410, 577-580.
17. De Vos M, Jander G, 2010. Volatile communication in plant-aphid interactions. Curr. Opin. Plant Biol. 13, 366-371.
18. Dicke M, Bruin J, 2001. Chemical information transfer between plants: back to the future. Biochem. Syst. Ecol. 29, 981-994.
19. Dicke M, van Loop JJA, Soler R, 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5, 317-324.
20. Dimitrijević B, Jelić M, Lomović S, 1999. The effect of mineral nutrition on the damage degree of spring wheat by Lema melanopus L. (Coleoptera: Chrysomelidae). Acta Entomol. Serbica 4, 49-55.
21. Dodman RL, Wildermuth GB, 1987. Inoculation methods for assessing resistance in wheat to crown rot caused by Fusarium graminearum Group 1. Aust. J. Agric. Res. 38, 473-486.
22. Dudareva N, Pichersky E, 2008. Metabolic engineering of plant volatiles. Curr. Opin. Biotechol. 19, 181-189.
23. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH, 2004. Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci., USA 101, 1781-1785.
24. 6 - green leaf volatiles trigger local and systemic VOC emission in tomato. Phytochemistry 61, 545-554.
25. Farag MA, Fokar M, Abd H, Zhang H, Allen RD, Paré PW, 2005. (Z)-3-hexenol induces defense genes and downstream metabolites in maize. Planta 220, 900-909.
26. Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC, 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10, 490-498.
27. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT, 2008. Shared signals - 'alarm calls' from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11, 24-34.
28. Heil M, Karban R, 2010. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25, 137-144.
29. Heil M, Silva Bueno JC, 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 104, 5467-5472.
30. Heil M, Lion U, Boland W, 2008. Defense-inducing volatiles: in search of the active motif. J. Chem. Ecol. 34, 601-604.
31. 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 Phytol. 186, 722-732.
32. Hoballah ME, Turlings TCJ, 2005. The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J. Chem. Ecol. 31, 2003-2018.
33. Holopainen JK, Gershenzon J, 2010. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 15, 176-184.
34. Ihrig RA, Herbert DA Jr, van Duyn JW, Bradley JR Jr, 2001. Relationship between cereal leaf beetle (Coleoptera: Chrysomelidae) egg and fourth-instar populations and impact of fourth-instar defoliation of winter wheat yields in North Carolina and Virginia. J. Econ. Entomol. 94, 634-639.
35. Karban R, Baldwin IT, 1997. Induced responses to herbivory. University of Chicago Press, Chicago, 319.
36. Kessler A, Baldwin IT, 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141-2144.
37. Kessler A, Baldwin IT, 2002. Plants responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53, 299-328.
38. Kessler A, Heil M, 2011. The multiple faces of indirect defences and their agents on natural selection. Funct. Ecol. 25, 348-357.
39. 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.
40. Kost C, Heil M, 2006. Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J. Ecol. 94, 619-628.
41. Kushalappa AC, Lui LH, Chen CR, Lee B, 2002. Volatile fingerprinting (SPME-GC-FID) to detect and discriminate diseases of potato tubers. Plant Dis. 86, 131-137.
42. Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor JE, Mullineaux PM, Hewitt CN, 2008. Isoprene emissions influence herbivore feeding decisions. Plant, Cell Environ. 31, 1410-1415.
43. Leitner M, Kaiser R, Rasmussen MO, Driguez H, Boland W, Mithöfer A, 2008. Microbial oligosaccharides differentially induce volatiles and signalling components in Medicago truncatula. Phytochemistry 69, 2029-2040.
44. Leslie JF, Summerell BA, 2006. The Fusarium laboratory manual. Blackwell Publishing, Ames, IA, USA, 388.
45. McCall PJ, Turlings TCJ, Lewis WJ, Tumlinson JH, 1993. Role of plant volatiles in host location by the specialist parasitoid Microplitis croceipes Cresson (Braconidae: Hymenoptera). J. Insect Behav. 6, 625-639.
46. Mumm R, Posthumus MA, Dicke M, 2008. Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant, Cell Environ. 31, 575-585.
47. Nelson PE, Toussoun TA, Marasas WFO, 1983. Fusarium species. An illustrated manual for identification. The Pennsylvania State University Press, University Park, PA, 1-193.
48. Peňuelas J, Llusià J, 2003. BVOCs: plant defense against climate warming? Trends Plant Sci. 8, 105-109.
49. Piesik D, Wenda-Piesik A, Weaver DK, Morrill WL, 2007. Influence of Fusarium crown rot disease on semiochemical production by wheat plants. J. Phytopathol. 155, 488-496.
50. Piesik D, Weaver DK, Runyon JB, Buteler ML, Peck GE, Morrill WL, 2008. Behavioral responses of wheat stem sawflies to wheat volatiles. Agric. Forest Entomol. 10, 245-253.
51. Piesik D, Łyszczarz A, Tabka P, Lamparski R, Bocianowski J, Delaney KJ, 2010. Volatile induction of three cereals: influence of mechanical injury and insect herbivory on injured plants and neighbouring uninjured plants. Ann. Appl. Biol. 157, 425-434.
52. Piesik D, Pańka D, Delaney KJ, Skoczek A, Lamparski R, Weaver DK, 2011a. Cereal crop volatile organic compound induction after mechanical injury, beetle herbivory (Oulema spp.), or fungal infection (Fusarium spp.). J. Plant Physiol. 168, 878-886.
53. Piesik D, Lemańczyk G, Skoczek A, Lamparski R, Bocianowski J, Kotwica K, Delaney KJ, 2011b. Fusarium infection in maize: Volatile induction of infected and neighboring uninfected plants has the potential to attract a pest cereal leaf beetle, Oulema melanopus. J. Plant Physiol. 168, 1534-1542.
54. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM, 2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308-316.
55. Rasmann S, Ko{double acute}llner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732-737.
56. Redman RS, Dunigan DD, Rodriguez RJ, 2001. Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytol. 151, 705-716.
57. Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ, 2009. Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J. Chem. Ecol. 35, 163-175.
58. Ruther J, Kleier S, 2005. Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J. Chem. Ecol. 31, 2217-2222.
59. SAS Institute, 2007. SAS user's guide: statistics, version 9.2. SAS Institute, Cary, NC.
60. Schnurer J, Olsson J, Borjesson T, 1999. Fungal volatiles as indicators of food and feeds spoilage. Fungal Genet. Biol. 27, 209-217.
61. Schoonhoven LM, Van Loon JJA, Dicke M, 2005. Insect-plant biology. Oxford University Press, Oxford, 421.
62. Shapiro SS, Wilk MB, 1965. An analysis of variance test for normality (complete samples). Biometrika 52, 591-611.
63. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J, 2006. Changing green leaf biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc. Natl. Acad. Sci. USA, 103, 16672-16676.
64. Shulaev V, Silverman P, Raskin I, 1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Science 385, 718-721.
65. Sokal RR, Rohlf FJ, 1995. Biometry: The principles and practice of statistics in biological research, 3rd edn. WH Freeman and Co., New York, 887.
66. Thaler JS, 1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399, 686-688.
67. Ton J, D'Alessandro 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 J. 49, 16-26.
68. Turlings TCJ, Ton J, 2006. Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr. Opin. Plant Biol. 9, 421-427.
69. Turlings TCJ, Tumlinson JH, Lewis WJ, 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251-1253.
70. Unsicker SB, Kunert G, Gershenzon J, 2009. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 2, 479-485.
71. Van Den Boom CEM, Van Beek TA, Posthumus MA, De Groot A, Dicke M, 2004. Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J. Chem. Ecol. 3, 69-89.
72. Vickers CE, Gershenzon J, Lerdau MT, Loreto F, 2009. A unified mechanism of action for isoprenoids in plant abiotic stress. Nat. Chem. Biol. 5, 283-291.
73. Vikram A, Hamzehzarghani H, Kushalappa AC, 2005. Volatile metabolites from the headspace of onion bulbs inoculated with postharvest pathogens as a tool for disease discrimination. Can. J. Plant Pathol. 27, 194-203.
74. Whittaker RH, Feeny PP, 1971. Allelochemics: chemical interactions between species. Science 171, 757-770.
75. Wildermuth GB, McNamara RB, 1994. Testing wheat seedlings for resistance to crown rot caused by Fusarium graminearum Group 1. Plant Dis. 78, 949-953.
76. Yi H-S, Heil M, Adame-Álvarez RM, Ballhorn DJ, Ryu C-M, 2009. Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151, 2152-2161.