Indirect defence of Arabidopsis against herbivorous insects : combining parasitoid behaviour and chemical analyses with a molecular genetic approach

Many plant species are known to defend themselves against herbivorous insects indirectly, by producing volatiles in response to herbivory. These volatiles attract carnivorous enemies of the herbivores, such as parasitoids. Research on the model plant Arabidopsis thaliana (L.) Heynh. (Brassicaceae) has contributed considerably to the unravelling of signal transduction pathways involved in direct plant defence mechanisms against pathogens. In this thesis I demonstrate that Arabidopsis is also a good model plant for studying signal transduction pathways involved in indirect defence mechanisms, by showing that: (a) Arabidopsis plants infested by Pieris rapae caterpillars (Lepidoptera: Pieridae) emit volatiles from several major biosynthetic pathways, including terpenoids, methyl-salicylate (MeSA), nitriles and green leaf volatiles; (b) Adult females of Cotesia rubecula (Hymenoptera: Braconidae), a specialist parasitoid wasp of P. rapae , were attracted to P. rapae- infested Arabidopsis plants; and (c) Genes from major biosynthetic pathways involved in volatile production were induced by caterpillar feeding.Moreover, I show that the octadecanoid and the salicylic acid pathways are involved in the induced attraction of C. rubecula by P. rapae -infested Arabidopsis . Besides exogenous application of jasmonic acid (JA) or salicylic acid (SA), I used transgenic Arabidopsis that do not show induced JA levels after wounding (S-12) and transgenic Arabidopsis that do not accumulate SA (NahG). Treatment of Arabidopsis with JA resulted in an increased attraction of parasitoid wasps compared to untreated plants, whereas treatment with SA did not. Transgenic plants impaired in the octadecanoid or the salicylic acid pathway were less attractive than wild-type plants. Chemical analysis of the volatile blends emitted by JA-treated wild-type and P. rapae -infested wild-type, S-12 and NahG plants, demonstrate that JA and SA are indeed involved in the herbivory-induced production of volatiles. Moreover, these data suggest important roles for MeSA and the terpenoid (3 E,7E )-4,8,12-trimethyl-1,3,7,11-tridecate traene as parasitoid attractants . Additionally, these data suggest a signalling role of the plant hormone 12-oxo-phytodienoic acid in induced volatile emissions.Although direct defence mechanisms against pathogens and herbivores are often also regulated through JA and SA, these signal transduction pathways differ from those involved in indirect defence of Arabidopsis against P. rapae , as I demonstrated by using the signal transduction mutants npr1-1 and jar1-1 .In this thesis it is also shown that herbivore species with a different way of feeding compared to P. rapae caterpillars - aphids and spider mites - induced no or less attraction of C. rubecula when infesting Arabidopsis. This difference in parasitoid attraction may be the result of different induction of JA and SA signalling pathways by different herbivore species.In conclusion, this thesis demonstrates that combing parasitoid behaviour and chemical analysis with a molecular genetic approach can be highly valuable in unravelling signal-transduction pathways involved in indirect defence of plants, a method that so far has been under-exploited.

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Bibliographic Details
Main Author: van Poecke, R.M.P.
Other Authors: Dicke, M.
Format: Doctoral thesis biblioteca
Language:English
Subjects:animal behaviour, arabidopsis thaliana, defence mechanisms, host parasite relationships, insect attractants, insect pests, molecular genetics, parasitoids, volatile compounds, diergedrag, gastheer parasiet relaties, insectenlokstoffen, insectenplagen, moleculaire genetica, parasitoïden, verdedigingsmechanismen, vluchtige verbindingen,
Online Access:https://research.wur.nl/en/publications/indirect-defence-of-arabidopsis-against-herbivorous-insects-combi
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Summary:Many plant species are known to defend themselves against herbivorous insects indirectly, by producing volatiles in response to herbivory. These volatiles attract carnivorous enemies of the herbivores, such as parasitoids. Research on the model plant Arabidopsis thaliana (L.) Heynh. (Brassicaceae) has contributed considerably to the unravelling of signal transduction pathways involved in direct plant defence mechanisms against pathogens. In this thesis I demonstrate that Arabidopsis is also a good model plant for studying signal transduction pathways involved in indirect defence mechanisms, by showing that: (a) Arabidopsis plants infested by Pieris rapae caterpillars (Lepidoptera: Pieridae) emit volatiles from several major biosynthetic pathways, including terpenoids, methyl-salicylate (MeSA), nitriles and green leaf volatiles; (b) Adult females of Cotesia rubecula (Hymenoptera: Braconidae), a specialist parasitoid wasp of P. rapae , were attracted to P. rapae- infested Arabidopsis plants; and (c) Genes from major biosynthetic pathways involved in volatile production were induced by caterpillar feeding.Moreover, I show that the octadecanoid and the salicylic acid pathways are involved in the induced attraction of C. rubecula by P. rapae -infested Arabidopsis . Besides exogenous application of jasmonic acid (JA) or salicylic acid (SA), I used transgenic Arabidopsis that do not show induced JA levels after wounding (S-12) and transgenic Arabidopsis that do not accumulate SA (NahG). Treatment of Arabidopsis with JA resulted in an increased attraction of parasitoid wasps compared to untreated plants, whereas treatment with SA did not. Transgenic plants impaired in the octadecanoid or the salicylic acid pathway were less attractive than wild-type plants. Chemical analysis of the volatile blends emitted by JA-treated wild-type and P. rapae -infested wild-type, S-12 and NahG plants, demonstrate that JA and SA are indeed involved in the herbivory-induced production of volatiles. Moreover, these data suggest important roles for MeSA and the terpenoid (3 E,7E )-4,8,12-trimethyl-1,3,7,11-tridecate traene as parasitoid attractants . Additionally, these data suggest a signalling role of the plant hormone 12-oxo-phytodienoic acid in induced volatile emissions.Although direct defence mechanisms against pathogens and herbivores are often also regulated through JA and SA, these signal transduction pathways differ from those involved in indirect defence of Arabidopsis against P. rapae , as I demonstrated by using the signal transduction mutants npr1-1 and jar1-1 .In this thesis it is also shown that herbivore species with a different way of feeding compared to P. rapae caterpillars - aphids and spider mites - induced no or less attraction of C. rubecula when infesting Arabidopsis. This difference in parasitoid attraction may be the result of different induction of JA and SA signalling pathways by different herbivore species.In conclusion, this thesis demonstrates that combing parasitoid behaviour and chemical analysis with a molecular genetic approach can be highly valuable in unravelling signal-transduction pathways involved in indirect defence of plants, a method that so far has been under-exploited.