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Pectin methylesterase NaPME1 contributes to the emission of methanol during insect herbivory and to the elicitation of defence responses in Nicotiana attenuata.

Körner E, von Dahl CC, Bonaventure G, Baldwin IT - J. Exp. Bot. (2009)

Bottom Line: Silenced lines (ir-pme) showed 50% reduced PME activity in leaves and 70% reduced MeOH emissions after OS elicitation compared with the wild type (WT), demonstrating that the herbivore-induced MeOH emissions originate from the demethylation of pectin by PME.This genotype also presented reduced levels of OS-induced trypsin proteinase inhibitor activity in leaves and consistently increased M. sexta larvae performance compared with WT plants.Together, these results indicated that PME contributes, probably indirectly by affecting cell wall properties, to the induction of anti-herbivore responses.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Chemical Ecology, Department of Molecular Ecology, Hans-Knöll-Str. 8, D-07745 Jena, Germany.

ABSTRACT
Pectin methylesterases (PMEs) catalyse the demethylation of pectin within plant cell walls, releasing methanol (MeOH) in the process. Thus far, PMEs have been found to be involved in diverse processes such as plant growth and development and defence responses against pathogens. Herbivore attack increases PME expression and activity and MeOH emissions in several plant species. To gain further insights into the role of PMEs in defence responses against herbivores, the expression of a Manduca sexta oral secretion (OS)-inducible PME in Nicotiana attenuata (NaPME1) was silenced by RNA interference (RNAi)-mediated gene silencing. Silenced lines (ir-pme) showed 50% reduced PME activity in leaves and 70% reduced MeOH emissions after OS elicitation compared with the wild type (WT), demonstrating that the herbivore-induced MeOH emissions originate from the demethylation of pectin by PME. In the initial phase of the OS-induced jasmonic acid (JA) burst (first 30 min), ir-pme lines produced WT levels of this hormone and of jasmonyl-isoleucine (JA-Ile); however, these levels were significantly reduced in the later phase (60-120 min) of the burst. Similarly, suppressed levels of the salicylic acid (SA) burst induced by OS elicitation were observed in ir-pme lines even though wounded ir-pme leaves contained slightly increased amounts of SA. This genotype also presented reduced levels of OS-induced trypsin proteinase inhibitor activity in leaves and consistently increased M. sexta larvae performance compared with WT plants. These latter responses could not be recovered by application of exogenous MeOH. Together, these results indicated that PME contributes, probably indirectly by affecting cell wall properties, to the induction of anti-herbivore responses.

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Silencing NaPME1 affects phytohormone dynamics after OS elicitation. Mean (±SE) JA (A) and JA-Ile (B) levels in N. attenuata leaves of WT plants (squares) and ir-pme lines 434-7 (circles) and 457-8 (triangles) 30, 60, 90, and 120 min after elicitation. Leaves were wounded and the wounds treated with either water (w+w, dashed lines) or 1:1 diluted M. sexta oral secretions (w+OS, solid lines). Control plants remained untreated (t=0 min) (n=4–5). (C) Mean (±SE) SA levels of WT plants and ir-pme lines 120 min after elicitation (n=5). (D) Mean (±SE) ethylene emissions of single leaves after wounding and application of OS (n=5). Asterisks represent significant differences from the WT (ANOVA).
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fig2: Silencing NaPME1 affects phytohormone dynamics after OS elicitation. Mean (±SE) JA (A) and JA-Ile (B) levels in N. attenuata leaves of WT plants (squares) and ir-pme lines 434-7 (circles) and 457-8 (triangles) 30, 60, 90, and 120 min after elicitation. Leaves were wounded and the wounds treated with either water (w+w, dashed lines) or 1:1 diluted M. sexta oral secretions (w+OS, solid lines). Control plants remained untreated (t=0 min) (n=4–5). (C) Mean (±SE) SA levels of WT plants and ir-pme lines 120 min after elicitation (n=5). (D) Mean (±SE) ethylene emissions of single leaves after wounding and application of OS (n=5). Asterisks represent significant differences from the WT (ANOVA).

Mentions: Manduca sexta larvae attack or OS elicitation causes a transient increase in JA and the amino acid conjugate JA-Ile which is larger than the increase caused by wounding alone (Schittko et al., 2000; Kang et al., 2006). The levels of these phytohormones were quantified in control and treated leaves (30, 60, 90, and 120 min after wounding or OS elicitation). In line 457-8, JA accumulated at significantly reduced levels (Fig. 2A, ANOVA, F2,11=5.49, P=0.02) after 30 min of induction, and in line 434-7 JA accumulated at significantly reduced levels after 60 min compared with the WT. At 90 min after OS treatment, leaves of both ir-pme lines contained 40% less JA than WT leaves (Fig. 2A, ANOVA, F2,11=8.31, P <0.01). A similar profile was observed for JA-Ile accumulation, with lower levels at 90 min in both ir-pme lines compared with WT (Fig. 2B, ANOVA, F2,11=8.27, P <0.01). In contrast, the accumulation of both JA and JA-Ile did not differ between WT and ir-pme lines after wounding alone (Fig. 2A, B, two-way ANOVA: JA, F2,59=0.29, P=0.75; JA-Ile, F2,59=0.34, P=0.72).


Pectin methylesterase NaPME1 contributes to the emission of methanol during insect herbivory and to the elicitation of defence responses in Nicotiana attenuata.

Körner E, von Dahl CC, Bonaventure G, Baldwin IT - J. Exp. Bot. (2009)

Silencing NaPME1 affects phytohormone dynamics after OS elicitation. Mean (±SE) JA (A) and JA-Ile (B) levels in N. attenuata leaves of WT plants (squares) and ir-pme lines 434-7 (circles) and 457-8 (triangles) 30, 60, 90, and 120 min after elicitation. Leaves were wounded and the wounds treated with either water (w+w, dashed lines) or 1:1 diluted M. sexta oral secretions (w+OS, solid lines). Control plants remained untreated (t=0 min) (n=4–5). (C) Mean (±SE) SA levels of WT plants and ir-pme lines 120 min after elicitation (n=5). (D) Mean (±SE) ethylene emissions of single leaves after wounding and application of OS (n=5). Asterisks represent significant differences from the WT (ANOVA).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2692009&req=5

fig2: Silencing NaPME1 affects phytohormone dynamics after OS elicitation. Mean (±SE) JA (A) and JA-Ile (B) levels in N. attenuata leaves of WT plants (squares) and ir-pme lines 434-7 (circles) and 457-8 (triangles) 30, 60, 90, and 120 min after elicitation. Leaves were wounded and the wounds treated with either water (w+w, dashed lines) or 1:1 diluted M. sexta oral secretions (w+OS, solid lines). Control plants remained untreated (t=0 min) (n=4–5). (C) Mean (±SE) SA levels of WT plants and ir-pme lines 120 min after elicitation (n=5). (D) Mean (±SE) ethylene emissions of single leaves after wounding and application of OS (n=5). Asterisks represent significant differences from the WT (ANOVA).
Mentions: Manduca sexta larvae attack or OS elicitation causes a transient increase in JA and the amino acid conjugate JA-Ile which is larger than the increase caused by wounding alone (Schittko et al., 2000; Kang et al., 2006). The levels of these phytohormones were quantified in control and treated leaves (30, 60, 90, and 120 min after wounding or OS elicitation). In line 457-8, JA accumulated at significantly reduced levels (Fig. 2A, ANOVA, F2,11=5.49, P=0.02) after 30 min of induction, and in line 434-7 JA accumulated at significantly reduced levels after 60 min compared with the WT. At 90 min after OS treatment, leaves of both ir-pme lines contained 40% less JA than WT leaves (Fig. 2A, ANOVA, F2,11=8.31, P <0.01). A similar profile was observed for JA-Ile accumulation, with lower levels at 90 min in both ir-pme lines compared with WT (Fig. 2B, ANOVA, F2,11=8.27, P <0.01). In contrast, the accumulation of both JA and JA-Ile did not differ between WT and ir-pme lines after wounding alone (Fig. 2A, B, two-way ANOVA: JA, F2,59=0.29, P=0.75; JA-Ile, F2,59=0.34, P=0.72).

Bottom Line: Silenced lines (ir-pme) showed 50% reduced PME activity in leaves and 70% reduced MeOH emissions after OS elicitation compared with the wild type (WT), demonstrating that the herbivore-induced MeOH emissions originate from the demethylation of pectin by PME.This genotype also presented reduced levels of OS-induced trypsin proteinase inhibitor activity in leaves and consistently increased M. sexta larvae performance compared with WT plants.Together, these results indicated that PME contributes, probably indirectly by affecting cell wall properties, to the induction of anti-herbivore responses.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Chemical Ecology, Department of Molecular Ecology, Hans-Knöll-Str. 8, D-07745 Jena, Germany.

ABSTRACT
Pectin methylesterases (PMEs) catalyse the demethylation of pectin within plant cell walls, releasing methanol (MeOH) in the process. Thus far, PMEs have been found to be involved in diverse processes such as plant growth and development and defence responses against pathogens. Herbivore attack increases PME expression and activity and MeOH emissions in several plant species. To gain further insights into the role of PMEs in defence responses against herbivores, the expression of a Manduca sexta oral secretion (OS)-inducible PME in Nicotiana attenuata (NaPME1) was silenced by RNA interference (RNAi)-mediated gene silencing. Silenced lines (ir-pme) showed 50% reduced PME activity in leaves and 70% reduced MeOH emissions after OS elicitation compared with the wild type (WT), demonstrating that the herbivore-induced MeOH emissions originate from the demethylation of pectin by PME. In the initial phase of the OS-induced jasmonic acid (JA) burst (first 30 min), ir-pme lines produced WT levels of this hormone and of jasmonyl-isoleucine (JA-Ile); however, these levels were significantly reduced in the later phase (60-120 min) of the burst. Similarly, suppressed levels of the salicylic acid (SA) burst induced by OS elicitation were observed in ir-pme lines even though wounded ir-pme leaves contained slightly increased amounts of SA. This genotype also presented reduced levels of OS-induced trypsin proteinase inhibitor activity in leaves and consistently increased M. sexta larvae performance compared with WT plants. These latter responses could not be recovered by application of exogenous MeOH. Together, these results indicated that PME contributes, probably indirectly by affecting cell wall properties, to the induction of anti-herbivore responses.

Show MeSH
Related in: MedlinePlus