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Effects of Feeding Spodoptera littoralis on Lima Bean Leaves: IV. Diurnal and Nocturnal Damage Differentially Initiate Plant Volatile Emission^1,[W],[OA]

Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, D–07745 Jena, Germany (G.-i.A., S.K., M.K., V.V., A.D., P.B., P.D., W.B.); and Department of Plant Biology and Centre of Excellence for Plant and Microbial Biosensing, University of Turin, I–10125 Turin, Italy (V.V., M.E.M.)

Continuous mechanical damage initiates the rhythmic emission of volatiles in lima bean (Phaseolus lunatus) leaves; the emission resembles that induced by herbivore damage. The effect of diurnal versus nocturnal damage on the initiation of plant defense responses was investigated using MecWorm, a robotic device designed to reproduce tissue damage caused by herbivore attack. Lima bean leaves that were damaged by MecWorm during the photophase emitted maximal levels of β-ocimene and (Z)-3-hexenyl acetate in the late photophase. Leaves damaged during the dark phase responded with the nocturnal emission of (Z)-3-hexenyl acetate, but with only low amounts of β-ocimene; this emission was followed by an emission burst directly after the onset of light. In the presence of ¹³CO₂, this light-dependent synthesis of β-ocimene resulted in incorporation of 75% to 85% of ¹³C, demonstrating that biosynthesis of β-ocimene is almost exclusively fueled by the photosynthetic fixation of CO₂ along the plastidial 2-C-methyl-D-erythritol 4-P pathway. Jasmonic acid (JA) accumulated locally in direct response to the damage and led to immediate up-regulation of the P. lunatus β-ocimene synthase gene (PlOS) independent of the phase, that is, light or dark. Nocturnal damage caused significantly higher concentrations of JA (approximately 2–3 times) along with enhanced expression levels of PlOS. Transgenic Arabidopsis thaliana transformed with PlOS promoter::β-glucuronidase fusion constructs confirmed expression of the enzyme at the wounded sites. In summary, damage-dependent JA levels directly control the expression level of PlOS, regardless of light or dark conditions, and photosynthesis is the major source for the early precursors of the 2-C-methyl-D-erythritol 4-P pathway.

² These authors contributed equally to the article.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Wilhelm Boland (boland{at}ice.mpg.de).

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www.plantphysiol.org/cgi/doi/10.1104/pp.107.111088

^* Corresponding author; e-mail boland{at}ice.mpg.de.

Received October 16, 2007; accepted December 10, 2007; published December 28, 2007.

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