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Caterpillar Herbivory and Salivary Enzymes Decrease Transcript Levels of Medicago truncatula genes Encoding Early Enzymes in Terpenoid Biosynthesis

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Abstract

In response to caterpillar herbivory, alfalfa and related plant species defend themselves through the induction of saponin and volatile terpenoid biosynthesis. Both these types of defensive compounds are derived from the metabolic intermediate, isopentenyl diphosphate (IPP). In plants, two distinct biosynthetic pathways can generate IPP; the cytosolic mevalonate pathway and the plastid-associated 2C-methyl erythritol 4-phosphate (MEP) pathway. In Medicago truncatula, transcript levels of key regulatory genes active in the early steps of these biosynthetic pathways were measured in response to larval herbivory by the beet armyworm, Spodoptera exigua. Transcripts encoding enzymes at early steps of both terpenoid pathways were lower in caterpillar-damaged leaves. Higher degrees of herbivore damage accentuated the decrease in transcript levels; however, transcript amounts were not affected by insect larval stage. Insect larvae, manipulated to reduce labial gland salivary secretions, were used to examine the role of the salivary elicitors in modulating gene expression. Results suggest that an insect salivary factor, possibly glucose oxidase (GOX), may be involved in reduction of transcript levels following herbivory. Addition of GOX or hydrogen peroxide to mechanically wounded leaves confirm these findings. In comparison, transcript levels of a gene encoding a putative terpene synthase are induced in mechanically- or insect-damaged leaves. These data show that insect salivary factors can act to suppress transcript levels of genes involved in plant defense pathways. Findings also suggest that in response to stress such as insect herbivory, regulation occurs at the early steps of the MEP pathway.

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Abbreviations

DMNT:

(3E)-4,8-dimethyl-1,3,7-nonatriene

dxs1 :

d-1-deoxyxylulose 5-phosphate synthase

dxr1 :

d-1-deoxyxylulose 5-phosphate reductoisomerase

GOX:

glucose oxidase

hmg1 :

3-hydroxy- 3-methylglutaryl CoA reductase

H2O2:

hydrogen peroxide

IPP:

isopentenyl diphosphate

MVA:

mevalonate

MEP:

2C-methyl erythritol 4-phosphate

TMTT:

(E,E)-4,8–12-trimethyl-1,3,7-tridecatetraene

tps1 :

terpene synthase

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Author notes

  1. Jacqueline C. Bede

    Present address: Department of Plant Science, McGill University, Quebec, H9X 3V9, Canada

  2. Richard O. Musser

    Present address: Department of Biological Sciences, Western Illinois University, Macomb, IL, USA

Authors and Affiliations

  1. Department of Plant Pathology, University of Arkansas, Fayetteville, AR, 72701, USA

    Jacqueline C. Bede & Kenneth L. Korth

  2. Department of Entomology, University of Arkansas, Fayetteville, AR, 72701, USA

    Richard O. Musser

  3. Department of Entomology, Penn State University, University Park, PA, 16802, USA

    Gary W. Felton

Authors
  1. Jacqueline C. Bede
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  2. Richard O. Musser
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  3. Gary W. Felton
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  4. Kenneth L. Korth
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Corresponding author

Correspondence to Kenneth L. Korth.

Additional information

Data Deposition: M. truncatula gene accession numbers: dxs1: AW689301; dxr1: BG456710; hmg1: AW687494; tps1: BF640252; pgk: BE322172. GenBank Accession Numbers for orthologous genes: dxs: Lycopersicon esculentum AF143812; dxr: Arabidopsis thaliana AX081292; hmg: Solanum tuberosum L01401; tps: Gossypium hirsutum AF270425; pgk: A. thaliana AC069159; rDNA: Oryza sativa X54194.

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Bede, J.C., Musser, R.O., Felton, G.W. et al. Caterpillar Herbivory and Salivary Enzymes Decrease Transcript Levels of Medicago truncatula genes Encoding Early Enzymes in Terpenoid Biosynthesis. Plant Mol Biol 60, 519–531 (2006). https://doi.org/10.1007/s11103-005-4923-y

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  • DOI: https://doi.org/10.1007/s11103-005-4923-y

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