Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore

Plant, Cell and Environment

Volumn 37, Issue 8, 2014, Pages 1924-1935

  Ponzio, Camille ^a   Gols, Rieta ^a   Weldegergis, Berhane T ^a   Dicke, Marcel ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Cotesia glomerata; HIPV; Indirect defence; Pieris brassicae; Tritrophic interactions

Indexed keywords

ANTIHERBIVORE DEFENSE; APHID; BACTERIUM; BIOGENIC EMISSION; BUTTERFLY; CATERPILLAR; HERB; HERBIVORY; HOST-PARASITOID INTERACTION; PLANT-HERBIVORE INTERACTION; SIGNAL; TRITROPHIC INTERACTION; VOLATILE SUBSTANCE; WASP;

APHIDIDAE; BACTERIA (MICROORGANISMS); BRASSICA NIGRA; BREVICORYNE BRASSICAE; COTESIA; COTESIA GLOMERATA; HEXAPODA; PIERIS BRASSICAE; XANTHOMONAS CAMPESTRIS; XANTHOMONAS CAMPESTRIS PV. CAMPESTRIS;

INSECT ATTRACTANTS; PHEROMONE; VOLATILE ORGANIC COMPOUND;

ANIMAL; ARTICLE; BUTTERFLY; CHEMISTRY; COTESIA GLOMERATA; HERBIVORY; HIPV; INDIRECT DEFENCE; LARVA; MUSTARD; PARASITOLOGY; PHYSIOLOGY; PIERIS BRASSICAE; PLANT DISEASE; TRITROPHIC INTERACTIONS; WASP; XANTHOMONAS CAMPESTRIS;

COTESIA GLOMERATA; HIPV; INDIRECT DEFENCE; PIERIS BRASSICAE; TRITROPHIC INTERACTIONS;

ANIMALS; BUTTERFLIES; HERBIVORY; LARVA; MUSTARD PLANT; PHEROMONES; PLANT DISEASES; VOLATILE ORGANIC COMPOUNDS; WASPS; XANTHOMONAS CAMPESTRIS;

EID: 84904341090     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12301     Document Type: Article

References (57)

1. Ballhorn D.J. (2011) Constraints of simultaneous resistance to a fungal pathogen and an insect herbivore in Lima Bean (Phaseolus lunatus L.). Journal of Chemical Ecology 37, 141-144.
2. de Boer J., Hordijk C., Posthumus M. & Dicke M. (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. Journal of Chemical Ecology 34, 281-290.
3. Bruessow F., Gouhier-Darimont C., Buchala A., Metraux J.-P. & Reymond P. (2010) Insect eggs suppress plant defence against chewing herbivores. The Plant Journal 62, 876-885.
4. Bukovinszky T., Poelman E.H., Kamp A., Hemerik L., Prekatsakis G. & Dicke M. (2012) Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency. Animal Behaviour 83, 501-509.
5. Cardoza Y. & Tumlinson J. (2006) Compatible and incompatible Xanthomonas infections differentially affect herbivore induced volatile emission by pepper plants. Journal of Chemical Ecology 32, 1755-1768.
6. Cardoza Y.J., Teal P.E.A. & Tumlinson J.H. (2003) Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environmental Entomology 32, 970-976.
7. Croft K., Juttner F. & Slusarenko A.J. (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiology 101, 13-24.
8. De Vos M., Van Oosten V., Van Poecke R., Van Pelt J., Pozo M., Mueller M., ... Pieterse C. (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923-937.
9. Denno R., McClure M. & Ott J. (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annual Review of Entomology 40, 297-331.
10. Dicke M. (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomologia Experimentalis et Applicata 91, 131-142.
11. Dicke M. & Baldwin I.T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. Trends in Plant Science 15, 167-175.
12. Dicke M., van Loon J.J.A. & Soler R. (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology 5, 317-324.
13. Doughty K.J., Blight M.M., Bock C.H., Fieldsend J.K. & Pickett J.A. (1996) Release of alkenyl isothiocyanates and other volatiles from Brassica rapa seedlings during infection by Alternaria brassicae. Phytochemistry 43, 371-374.
14. Erb M., Foresti N. & Turlings T. (2010) A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biology 10, 247.
15. Fatouros N.E., Lucas-Barbosa D., Weldegergis B.T., Pashalidou F.G., van Loon J.J.A., Dicke M., ... Huigens M.E. (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7, e43607.
16. Fei M., Gols R. & Harvey J.A. (2014) Seasonal phenology of interactions involving short-lived annual plants, a multivoltine herbivore and its endoparasitoid wasp. Journal of Animal Ecology 83, 234-244.
17. Geervliet J., Vet L. & Dicke M. (1994) Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoid Cotesia rubecula. Entomologia Experimentalis et Applicata 73, 289-297.
18. Geervliet J.B.F., Vet L.E.M. & Dicke M. (1996) Innate responses of the parasitoids Cotesia glomerata and C.rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes. Journal of Insect Behavior 9, 525-538.
19. Giordanengo P., Brunissen L., Rusterucci C., Vincent C., van Bel A., Dinant S., ... Bonnemain J.-L. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. Comptes Rendus Biologies 333, 516-523.
20. Glazebrook J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205-227.
21. Gols R., Witjes L.M.A., Van Loon J.J.A., Posthumus M.A., Dicke M. & Harvey J.A. (2008) The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid. Entomologia Experimentalis et Applicata 128, 99-108.
22. Gols R., Van Dam N.M., Raaijmakers C.E., Dicke M. & Harvey J.A. (2009) Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps? Oikos 118, 733-742.
23. Gols R., Bullock J., Dicke M., Bukovinszky T. & Harvey J. (2011) Smelling the wood from the trees: non-linear parasitoid responses to volatile attractants produced by wild and cultivated cabbage. Journal of Chemical Ecology 37, 795-807.
24. Gols R., Veenemans C., Potting R.P.J., Smid H.M., Dicke M., Harvey J.A. & Bukovinszky T. (2012) Variation in the specificity of plant volatiles and their use by a specialist and a generalist parasitoid. Animal Behaviour 83, 1231-1242.
25. Hare J. & Sun J. (2011) Production of induced volatiles by Datura wrightii in response to damage by insects: effect of herbivore species and time. Journal of Chemical Ecology 37, 751-764.
26. Huang J., Cardoza Y.J., Schmelz E.A., Raina R., Engelberth J. & Tumlinson J.H. (2003) Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae. Planta 217, 767-775.
27. Kaplan I. & Denno R.F. (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecology Letters 10, 977-994.
28. Koornneef A. & Pieterse C.M.J. (2008) Cross talk in defense signaling. Plant Physiology 146, 839-844.
29. Mattiacci L. & Dicke M. (1995) Host-age discrimination during host location by Cotesia glomerata, a larval parasitoid of Pieris brassicae. Entomologia Experimentalis et Applicata 76, 37-48.
30. Mattiacci L., Dicke M. & Posthumus M. (1994) Induction of parasitoid attracting synomone in brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damage and herbivore elicitor. Journal of Chemical Ecology 20, 2229-2247.
31. Moayeri H.R.S., Ashouri A., Poll L. & Enkegaard A. (2007) Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory versus single herbivory. Journal of Applied Entomology 131, 326-332.
32. Moran P.J. & Thompson G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology 125, 1074-1085.
33. Pieterse C.M.J. & Dicke M. (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends in Plant Science 12, 564-569.
34. Pieterse C.M.J., van der Does D., Zamioudis C., Leon-Reyes A. & van Wees S.C.M. (2012) Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28.
35. Poelman E.H., Bruinsma M., Zhu F., Weldegergis B.T., Boursault A.E., Jongema Y., ... Dicke M. (2012) Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biology 10, e1001435.
36. Ponzio C., Gols R., Pieterse C.M.J. & Dicke M. (2013) Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Functional Ecology 27, 587-598.
37. Rasmann S. & Turlings T. (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecology Letters 10, 926-936.
38. de Rijk M., Dicke M. & Poelman E.H. (2013) Foraging behaviour by parasitoids in multiherbivore communities. Animal Behaviour 85, 1517-1528.
39. Rodriguez-Saona C., Crafts-Brandner S.J. & Cañas L.A. (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. Journal of Chemical Ecology 29, 2539-2550.
40. Rostás M., Ton J., Mauch-Mani B. & Turlings T. (2006) Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naive parasitoids. Journal of Chemical Ecology 32, 1897-1909.
41. Schwartzberg E., Böröczky K. & Tumlinson J. (2011) Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba. Journal of Chemical Ecology 37, 1055-1062.
42. Shiojiri K., Takabayashi J., Yano S. & Takafuji A. (2000) Flight response of parasitoids toward plant-herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants. Applied Entomology and Zoology 35, 87-92.
43. Shiojiri K., Takabayashi J., Yano S. & Takafuji A. (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Population Ecology 43, 23-29.
44. Soler R., Harvey J.A., Kamp A.F.D., Vet L.E.M., Van der Putten W.H., Van Dam N.M., ... Martijn Bezemer T. (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116, 367-376.
45. Soler R., Pineda A., Li Y., Ponzio C., van Loon J.J.A., Weldegergis B.T. & Dicke M. (2012) Neonates know better than their mothers when selecting a host plant. Oikos 121, 1923-1934.
46. Spoel S.H. & Dong X. (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host & Microbe 3, 348-351.
47. Spoel S.H., Johnson J.S. & Dong X. (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences of the United States of America 104, 18842-18847.
48. Stam J.M., Kroes A., Li Y., Gols R., van Loon J.J.A., Poelman E.H. & Dicke M. (2014) Plant interactions with multiple insect herbivores: from community to genes. Annual Review of Plant Biology. doi: 10.1146/annurev-arplant-050213-035937.
49. Tack A.J.M. & Dicke M. (2013) Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Functional Ecology 27, 633-645.
50. Thaler J.S., Humphrey P.T. & Whiteman N.K. (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends in Plant Science 17, 260-270.
51. Ton J., Van Pelt J.A., Van Loon L.C. & Pieterse C.M.J. (2002) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Molecular Plant-Microbe Interactions 15, 27-34.
52. Turlings T. & Wäckers F. (2004) Recruitment of predators and parasitoids by herbivore-damaged plants. In Advances in Insect Chemical Ecology (eds R.T. Cardé & J. Millar ) pp. 21-75. Cambridge University Press, Cambridge.
53. Van Poecke R. & Dicke M. (2004) Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biology 6, 387-401.
54. Vet L.E.M. & Dicke M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141-172.
55. Vos M., Berrocal S.M., Karamaouna F., Hemerik L. & Vet L.E.M. (2001) Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecology Letters 4, 38-45.
56. Zhang P.-J., Zheng S.-J., van Loon J.J.A., Boland W., David A., Mumm R. & Dicke M. (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proceedings of the National Academy of Sciences of the United States of America 106, 21202-21207.
57. Zhang P.-J., Broekgaarden C., Zheng S.-J., Snoeren T.A.L., van Loon J.J.A., Gols R. & Dicke M. (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytologist 197, 1291-1299.