Reciprocal crosstalk between jasmonate and salicylate defence-signalling pathways modulates plant volatile emission and herbivore host-selection behaviour

Journal of Experimental Botany

Volumn 65, Issue 12, 2014, Pages 3289-3298

  Wei, Jianing ^a,b   Van Loon, Joop J A ^a   Rieta, Gols ^a   Menzel, Tila R ^a   Li, Na ^b   Kang, Le ^b   Dicke, Marcel ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b INSTITUTE OF ZOOLOGY   (China)

Author keywords

Dose effect; Herbivore behaviour; Induced plant defence; Phytohormonal signalling; Spider mite; Temporal effect

Indexed keywords

CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID; VOLATILE ORGANIC COMPOUND;

ANIMAL; DRUG EFFECTS; EGG LAYING; FEEDING BEHAVIOR; FOOD CHAIN; METABOLISM; PHASEOLUS; PHYSIOLOGY; SIGNAL TRANSDUCTION; TETRANYCHIDAE;

ANIMALS; CYCLOPENTANES; FEEDING BEHAVIOR; FOOD CHAIN; OVIPOSITION; OXYLIPINS; PHASEOLUS; SALICYLIC ACID; SIGNAL TRANSDUCTION; TETRANYCHIDAE; VOLATILE ORGANIC COMPOUNDS;

EID: 84904282763     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru181     Document Type: Article

References (55)

1. Atkinson NJ, Urwin PE. 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. Journal of Experimental Botany 63, 3523-3543.
2. Beckers GJM, Spoel SH. 2006. Fine-tuning plant defence signalling: Salicylate versus jasmonate. Plant Biology 8, 1-10.
3. Bostock RM. 1999. Signal conflicts and synergies in induced resistance to multiple attackers. Physiological and Molecular Plant Pathology 55, 99-109.
4. Bruce TJA, Pickett JA. 2011. Perception of plant volatile blends by herbivorous insects - Finding the right mix. Phytochemistry 72, 1605-1611.
5. Bruce TJA, Wadhams LJ, Woodcock CM. 2005. Insect host location: a volatile situation. Trends in Plant Science 10, 269-274.
6. Bruinsma M, Van Dam NM, Van Loon JJA, Dicke M. 2007. Jasmonic acid-induced changes in Brassica oleracea affect oviposition preference of two specialist herbivores. Journal of Chemical Ecology 33, 655-668.
7. Bukovinszky T, Poelman EH, 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.
8. Cui J, Bahrami AK, Pringle EG, Hernandez-Guzman G, Bender CL, Pierce NE, Ausubel FM. 2005. Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Sciences, USA 102, 1791-1796.
9. De Vos M, Van Oosten VR, Van Poecke RMP et al. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923-937.
10. Dicke M. 1986. Volatile spider-mite pheromone and host-plant kairomone, involved in spaced-out gregariousness in the spider-mite Tetranychus urticae. Physiological Entomology 11, 251-262.
11. Dicke M, Baldwin IT. 2010. The evolutionary context for herbivoreinduced plant volatiles: beyond the 'cry for help'. Trends in Plant Science 15, 167-175.
12. Dicke M, Gols R, Ludeking D, Posthumus MA. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. Journal of Chemical Ecology 25, 1907-1922.
13. Dicke M, van Loon JJA, Soler R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology 5, 317-324.
14. Dicke M, Vanbeek TA, Posthumus MA, Bendom N, Vanbokhoven H, Degroot AE. 1990. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions - involvement of host plant in its production. Journal of Chemical Ecology 16, 381-396.
15. Engelberth J, Koch T, Schuler G, Bachmann N, Rechtenbach J, Boland W. 2001. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiology 125, 369-377.
16. Erb M, Balmer D, De Lange ES, et al. 2011. Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots. Plant, Cell and Environment 34, 1088-1103.
17. Gols R, Roosjen M, Dijkman H, Dicke M. 2003. Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. Journal of Chemical Ecology 29, 2651-2666.
18. 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. Ecology Letters 11, 24-34.
19. Harrison S, Karban R. 1986. Behavioral-response of spider-mites (Tetranychus urticae) to induced resistance of cotton plants. Ecological Entomology 11, 181-188.
20. Heil M. 2008. Indirect defence via tritrophic interactions. New Phytologist 178, 41-61.
21. Heil M, Walters DR. 2009. Ecological consequences of plant defence signalling. Plant Innate Immunity 51, 667-716.
22. Kessler A, Baldwin IT. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141-2144.
23. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology 53, 299-328.
24. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiology 147, 1358-1368.
25. Kunkel BN, Brooks DM. 2002. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5, 325-331.
26. Leon-Reyes A, Du YJ, Koornneef A, Proietti S, Korbes AP, Memelink J, Pieterse CMJ, Ritsema T. 2010. Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Molecular Plant-Microbe Interactions 23, 187-197.
27. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RAM, Ritsema T, Pieterse CMJ. 2009. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESISRELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiology 149, 1797-1809.
28. Loivamaki M, Mumm R, Dicke M, Schnitzler JP. 2008. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proceedings of the National Academy of Sciences, USA 105, 17430-17435.
29. Lou YG, Du MH, Turlings TCJ, Cheng JA, Shan WF. 2005. Exogenous application of jasmonic acid induces volatile emissions in rice and enhances parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae. Journal of Chemical Ecology 31, 1985-2002.
30. Lu YB, Liu SS, Liu YQ, Furlong MJ, Zalucki MP. 2004. Contrary effects of jasmonate treatment of two closely related plant species on attraction of and oviposition by a specialist herbivore. Ecology Letters 7, 337-345.
31. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C. 2006. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology 140, 249-262.
32. Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T. 2000. Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant and Cell Physiology 41, 391-398.
33. Pallini A, Janssen A, Sabelis MW. 1997. Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors. Oecologia 110, 179-185.
34. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308-316.
35. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. 2012. Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28, 489-521.
36. 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. Functional Ecology 27, 587-598.
37. Rodriguez-Saona C, Crafts-Brandner SJ, Canas LA. 2003. Volatile emissions triggered by multiple herbivore damage: Beet armyworm and whitefly feeding on cotton plants. Journal of Chemical Ecology 29, 2539-2550.
38. 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. Journal of Chemical Ecology 36, 1043-1057.
39. Schmelz EA, Alborn HT, Tumlinson JH. 2003. Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiologia Plantarum 117, 403-412.
40. Spoel SH, Johnson JS, Dong X. 2007. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences, USA 104, 18842-18847.
41. Stam JM, Kroes A, Li Y, Gols R, van Loon JJA, Poelman EH, 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 (in press).
42. Stout MJ, Thaler JS, Thomma BPHJ. 2006. Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annual Review of Entomology 51, 663-689.
43. Thaler JS, Agrawal AA, Halitschke R. 2010. Salicylate-mediated interactions between pathogens and herbivores. Ecology 91, 1075-1082.
44. 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. Journal of Chemical Ecology 28, 1131-1159.
45. Thaler JS, Humphrey PT, Whiteman NK. 2012. Evolution of jasmonate and salicylate signal crosstalk. Trends in Plant Science 17, 260-270.
46. Thaler JS, Stout MJ, Karban R, Duffey SS. 2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecological Entomology 26, 312-324.
47. Turlings TCJ, Loughrin JH, Mccall PJ, Rose 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.
48. van Dam NM, Hadwich K, Baldwin IT. 2000. Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta. Oecologia 122, 371-379.
49. 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 Journal 38, 650-663.
50. von Dahl CC, Baldwin IT. 2007. Deciphering the role of ethylene in plant- herbivore interactions. Journal of Plant Growth Regulation 26, 201-209.
51. Wei JN, Wang LH, Zhao JH, Li CY, Ge F, Kang L. 2011. Ecological trade-offs between jasmonic acid-dependent direct and indirect plant defences in tritrophic interactions. New Phytologist 189, 557-567.
52. Wei JN, Wang LZ, Zhu JW, Zhang SF, Nandi OI, Kang L. 2007. Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. PLoS ONE 2, e852.
53. Zarate SI, Kempema LA, Walling LL. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology 143, 866-875.
54. Zhang PJ, Zheng SJ, van Loon JJA, 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, USA 106, 21202-21207.
55. Zheng SJ, van Dijk JP, Bruinsma M, Dicke M. 2007. Sensitivity and speed of induced defense of cabbage (Brassica oleracea L.): Dynamics of BoLOX expression patterns during insect and pathogen attack. Molecular Plant-Microbe Interactions 20, 1332-1345.