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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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PME1 transcript levels, PME activity, and MeOH emissions are reduced in ir-pme lines. (A) Northern blot analysis of NaPME1 mRNA in WT plants and ir-pme lines (434-7, 457-8) 6 h after wounding+OS treatment (OS) and in control leaves (Ctrl). (B) Mean (±SE) PME activity in N. attenuata leaves of WT plants and ir-pme lines 4 h after elicitation. Leaves were wounded and the wounds treated with either water (w+w) or 1:1 diluted M. sexta oral secretions (w+OS). Control plants remained untreated (n=4–5). (C) Mean (±SE) methanol emissions of single N. attenuata leaves of WT plants and ir-pme lines after wounding alone (wound) or subsequent application of 1:1 diluted M. sexta OS (w+OS) (n=3–5). Asterisks represent significant differences from the WT (ANOVA).
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fig1: PME1 transcript levels, PME activity, and MeOH emissions are reduced in ir-pme lines. (A) Northern blot analysis of NaPME1 mRNA in WT plants and ir-pme lines (434-7, 457-8) 6 h after wounding+OS treatment (OS) and in control leaves (Ctrl). (B) Mean (±SE) PME activity in N. attenuata leaves of WT plants and ir-pme lines 4 h after elicitation. Leaves were wounded and the wounds treated with either water (w+w) or 1:1 diluted M. sexta oral secretions (w+OS). Control plants remained untreated (n=4–5). (C) Mean (±SE) methanol emissions of single N. attenuata leaves of WT plants and ir-pme lines after wounding alone (wound) or subsequent application of 1:1 diluted M. sexta OS (w+OS) (n=3–5). Asterisks represent significant differences from the WT (ANOVA).

Mentions: It has been previously shown that N. attenuata plants emit large amounts of MeOH when attacked by M. sexta larvae and it has been proposed that the source of this MeOH is the result of PME activation (von Dahl et al., 2006). Thus, the PME1 transcript levels, PME activity, and the release of MeOH in ir-pme lines were determined after they had been elicited with M. sexta OS. Control plants were left untreated. Transcript levels were measured in leaves of WT and ir-pme lines using northern blot analysis (Fig. 1A). In WT plants, NaPME1 transcripts were detectable in both control and treated leaves. As expected, OS treatment increased PME1 transcript levels several fold after 6 h. In contrast, in leaves of ir-pme lines, no NaPME1 transcripts were detectable in either control or treated plants (Fig. 1A).


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)

PME1 transcript levels, PME activity, and MeOH emissions are reduced in ir-pme lines. (A) Northern blot analysis of NaPME1 mRNA in WT plants and ir-pme lines (434-7, 457-8) 6 h after wounding+OS treatment (OS) and in control leaves (Ctrl). (B) Mean (±SE) PME activity in N. attenuata leaves of WT plants and ir-pme lines 4 h after elicitation. Leaves were wounded and the wounds treated with either water (w+w) or 1:1 diluted M. sexta oral secretions (w+OS). Control plants remained untreated (n=4–5). (C) Mean (±SE) methanol emissions of single N. attenuata leaves of WT plants and ir-pme lines after wounding alone (wound) or subsequent application of 1:1 diluted M. sexta OS (w+OS) (n=3–5). 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

fig1: PME1 transcript levels, PME activity, and MeOH emissions are reduced in ir-pme lines. (A) Northern blot analysis of NaPME1 mRNA in WT plants and ir-pme lines (434-7, 457-8) 6 h after wounding+OS treatment (OS) and in control leaves (Ctrl). (B) Mean (±SE) PME activity in N. attenuata leaves of WT plants and ir-pme lines 4 h after elicitation. Leaves were wounded and the wounds treated with either water (w+w) or 1:1 diluted M. sexta oral secretions (w+OS). Control plants remained untreated (n=4–5). (C) Mean (±SE) methanol emissions of single N. attenuata leaves of WT plants and ir-pme lines after wounding alone (wound) or subsequent application of 1:1 diluted M. sexta OS (w+OS) (n=3–5). Asterisks represent significant differences from the WT (ANOVA).
Mentions: It has been previously shown that N. attenuata plants emit large amounts of MeOH when attacked by M. sexta larvae and it has been proposed that the source of this MeOH is the result of PME activation (von Dahl et al., 2006). Thus, the PME1 transcript levels, PME activity, and the release of MeOH in ir-pme lines were determined after they had been elicited with M. sexta OS. Control plants were left untreated. Transcript levels were measured in leaves of WT and ir-pme lines using northern blot analysis (Fig. 1A). In WT plants, NaPME1 transcripts were detectable in both control and treated leaves. As expected, OS treatment increased PME1 transcript levels several fold after 6 h. In contrast, in leaves of ir-pme lines, no NaPME1 transcripts were detectable in either control or treated plants (Fig. 1A).

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