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Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission - PubMed

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Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission

Gen-ichiro Arimura et al. Plant Physiol. 2008 Mar.

Abstract

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 beta-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 beta-ocimene; this emission was followed by an emission burst directly after the onset of light. In the presence of (13)CO(2), this light-dependent synthesis of beta-ocimene resulted in incorporation of 75% to 85% of (13)C, demonstrating that biosynthesis of beta-ocimene is almost exclusively fueled by the photosynthetic fixation of CO(2) 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 beta-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 :: beta-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.

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Figures

Figure 1.
Figure 1.

Gas chromatographic separation of the β-ocimene isomers formed by the recombinant PlOS enzyme with GDP as substrate.

Figure 2.
Figure 2.

Emission of the volatiles β-ocimene and Hex-Ac and transcript levels of PlOS in damaged lima bean leaves. Damage conditions: larvae of S. littoralis under a 14:10 LD cycle (A) and under a LD cycle set with 4 h of additional darkness (AD) during the second (25–29 h) and third (49–53 h) photoperiods (B). Time of day is shown across the top x axis, and total elapsed time is shown on the bottom x axis. Headspace analyses were performed in triplicate. Emission is expressed as ng min−1 g−1 FW. Data regarding to the transcript levels represent the mean ±

se

(n = 4–5).

Figure 3.
Figure 3.

Emissions of β-ocimene and Hex-Ac (A and B) and levels of JA and PlOS transcripts (C and D) in MecWorm-treated leaves. Damage program: 6 h during either the photophase (A and C) or the dark phase (B and D) according to a 14:10 LD cycle. Damage periods started 2 h after the onset of the light or dark phase with punching every 5 s for 6 h (9

am

–3

pm

during the photophase and from 11

pm

–5

am

during the night). Headspace analyses were performed in triplicate. Emission is expressed as ng min−1 g−1 FW. JA and transcript levels represent the mean ±

se

(n = 3–4).

Figure 4.
Figure 4.

Pulse labeling of (E)-β-ocimene after administration of 13CO2. Ambient air in the cabinet was exchanged by synthetic air containing 13CO2 gas (380 μg mL−1) 0.5 h before the onset of the light phase. Headspace analysis was started at its onset. The shaded box corresponds to the presence of 13CO2. One hour after the onset of the photophase, the cabinet was purged with ambient air to remove 13CO2. Collection periods for volatiles are indicated. Mass spectra of β-ocimene from leaves in ambient air or 13CO2-containing air are shown on top. Data represent the mean ±

se

(n = 4).

Figure 5.
Figure 5.

Effect of herbivory, wounding, and chemical treatment on the expression level of PlOS in lima bean leaves. Chemical treatments: JA (0.5 m

m

), salicylic acid (SA; 0.5 m

m

), and alamethicin (ALA; 1 m

m

). Means with small letters are significantly different according to ANOVA followed by Scheffe's test (P < 0.05). Data represent the mean ±

se

(n = 4).

Figure 6.
Figure 6.

Localization of PlOS transcript and accumulation of JA in mechanically damaged lima bean leaves. A, Leaf damaged for 6 h by MecWorm during the first and second dark phases. See Figure 3D for details. Leaf segments were harvested 32 h after initiation of the first MecWorm damage. Sections 2 and 3 correspond to the first and the second nocturnal damage. Undamaged sections 1 and 4 served as control. Data represent the mean ±

se

(n = 3–4). Scale bar = 10 mm. Means followed with small letters are significantly different according to ANOVA followed by Scheffe's test (P < 0.05). B and C, Wound-induced expression of PlOS promoter∷GUS reporter gene constructs in leaves of 6-week-old Arabidopsis plants. Wounding by a needle (B) or MecWorm treatment (C) induced GUS activity after 2 h in areas in close proximity to wounding sites. Histochemical GUS assays were performed with two independent lines. Scale bar = 2 mm.

Figure 7.
Figure 7.

Schematic representation of the signaling and metabolic pathways required for herbivore-induced β-ocimene and Hex-Ac emissions in lima bean leaves in a daily cycle. LOX, Lipoxygenase.

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References

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