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The plastidial metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate modulates defence responses against aphids.
Plant Cell Environ. 2019 07; 42(7):2309-2323.PC

Abstract

Feeding by insect herbivores such as caterpillars and aphids induces plant resistance mechanisms that are mediated by the phytohormones jasmonic acid (JA) and salicylic acid (SA). These phytohormonal pathways often crosstalk. Besides phytohormones, methyl-D-erythriol-2,4-cyclodiphosphate (MEcPP), the penultimate metabolite in the methyl-D-erythritol-4-phosphate pathway, has been speculated to regulate transcription of nuclear genes in response to biotic stressors such as aphids. Here, we show that MEcPP uniquely enhances the SA pathway without attenuating the JA pathway. Arabidopsis mutant plants that accumulate high levels of MEcPP (hds3) are highly resistant to the cabbage aphid (Brevicoryne brassicae), whereas resistance to the large cabbage white caterpillar (Pieris brassicae) remains unaltered. Thus, MEcPP is a distinct signalling molecule that acts beyond phytohormonal crosstalk to induce resistance against the cabbage aphid in Arabidopsis. We dissect the molecular mechanisms of MEcPP mediating plant resistance against the aphid B. brassicae. This shows that MEcPP induces the expression of genes encoding enzymes involved in the biosynthesis of several primary and secondary metabolic pathways contributing to enhanced resistance against this aphid species. A unique ability to regulate multifaceted molecular mechanisms makes MEcPP an attractive target for metabolic engineering in Brassica crop plants to increase resistance to cabbage aphids.

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Authors+Show Affiliations

Onkokesung N
Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands.
Reichelt M
Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
Wright LP
Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
Phillips MA
Department of Biology and Graduate Program in Cellular and Systems Biology, University of Toronto-Mississauga, Mississauga, Ontario, Canada.
Gershenzon J
Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany.
Dicke M
Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands.

MeSH

AnimalsAphidsArabidopsisArabidopsis ProteinsBrassicaCyclopentanesCytochrome P-450 Enzyme SystemDisease ResistanceErythritolGene Expression Regulation, PlantGlucosinolatesMetabolic Networks and PathwaysMetabolomeOxylipinsPlant Growth RegulatorsSalicylic AcidSecondary MetabolismSignal TransductionSugar PhosphatesTranscription Factors

Pub Type(s)

Journal Article

Language

eng

PubMed ID

30786032

Citation

Onkokesung, Nawaporn, et al. "The Plastidial Metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate Modulates Defence Responses Against Aphids." Plant, Cell & Environment, vol. 42, no. 7, 2019, pp. 2309-2323.
Onkokesung N, Reichelt M, Wright LP, et al. The plastidial metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate modulates defence responses against aphids. Plant Cell Environ. 2019;42(7):2309-2323.
Onkokesung, N., Reichelt, M., Wright, L. P., Phillips, M. A., Gershenzon, J., & Dicke, M. (2019). The plastidial metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate modulates defence responses against aphids. Plant, Cell & Environment, 42(7), 2309-2323. https://doi.org/10.1111/pce.13538
Onkokesung N, et al. The Plastidial Metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate Modulates Defence Responses Against Aphids. Plant Cell Environ. 2019;42(7):2309-2323. PubMed PMID: 30786032.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The plastidial metabolite 2-C-methyl-D-erythritol-2,4-cyclodiphosphate modulates defence responses against aphids. AU - Onkokesung,Nawaporn, AU - Reichelt,Michael, AU - Wright,Louwrance P, AU - Phillips,Michael A, AU - Gershenzon,Jonathan, AU - Dicke,Marcel, Y1 - 2019/03/08/ PY - 2018/10/31/received PY - 2019/02/09/revised PY - 2019/02/17/accepted PY - 2019/2/21/pubmed PY - 2020/5/6/medline PY - 2019/2/21/entrez KW - Arabidopsis KW - aphid resistance KW - indole glucosinolates KW - phloem-sucking herbivores KW - phytohormone signalling KW - retrograde signalling KW - secondary metabolites SP - 2309 EP - 2323 JF - Plant, cell & environment JO - Plant Cell Environ VL - 42 IS - 7 N2 - Feeding by insect herbivores such as caterpillars and aphids induces plant resistance mechanisms that are mediated by the phytohormones jasmonic acid (JA) and salicylic acid (SA). These phytohormonal pathways often crosstalk. Besides phytohormones, methyl-D-erythriol-2,4-cyclodiphosphate (MEcPP), the penultimate metabolite in the methyl-D-erythritol-4-phosphate pathway, has been speculated to regulate transcription of nuclear genes in response to biotic stressors such as aphids. Here, we show that MEcPP uniquely enhances the SA pathway without attenuating the JA pathway. Arabidopsis mutant plants that accumulate high levels of MEcPP (hds3) are highly resistant to the cabbage aphid (Brevicoryne brassicae), whereas resistance to the large cabbage white caterpillar (Pieris brassicae) remains unaltered. Thus, MEcPP is a distinct signalling molecule that acts beyond phytohormonal crosstalk to induce resistance against the cabbage aphid in Arabidopsis. We dissect the molecular mechanisms of MEcPP mediating plant resistance against the aphid B. brassicae. This shows that MEcPP induces the expression of genes encoding enzymes involved in the biosynthesis of several primary and secondary metabolic pathways contributing to enhanced resistance against this aphid species. A unique ability to regulate multifaceted molecular mechanisms makes MEcPP an attractive target for metabolic engineering in Brassica crop plants to increase resistance to cabbage aphids. SN - 1365-3040 UR - https://www.unboundmedicine.com/medline/citation/30786032/The_plastidial_metabolite_2_C_methyl_D_erythritol_24_cyclodiphosphate_modulates_defence_responses_against_aphids_ DB - PRIME DP - Unbound Medicine ER -