Abstract
How plants perceive herbivory is not yet well understood. We investigated early responses of the model plant Arabidopsis (Arabidopsis thaliana) to attack from the generalist grasshopper herbivore, Schistocerca gregaria (Caelifera). When compared with wounding alone, S. gregaria attack and the application of grasshopper oral secretions (GS) to puncture wounds elicited a rapid accumulation of various oxylipins, including 13-hydroperoxy octadecatrienoic acid, 12-oxo-phytodienoic acid (OPDA), jasmonic acid, and jasmonic acid-isoleucine. Additionally, GS increased cytosolic calcium levels, mitogen-activated protein kinase (MPK3 and MPK6) activity, and ethylene emission but not the accumulation of hydrogen peroxide. Although GS contain caeliferin A16:0, a putative elicitor of caeliferan herbivores, treatment with pure, synthetic caeliferin A16:0 did not induce any of the observed responses. With mutant plants, we demonstrate that the observed changes in oxylipin levels are independent of MPK3 and MPK6 activity but that MPK6 is important for the GS-induced ethylene release. Biochemical and pharmacological analyses revealed that the lipase activity of GS plays a central role in the GS-induced accumulation of oxylipins, especially OPDA, which could be fully mimicked by treating puncture wounds only with a lipase from Rhizopus arrhizus. GS elicitation increased the levels of OPDA-responsive transcripts. Because the oral secretions of most insects used to study herbivory-induced responses in Arabidopsis rapidly elicit similar accumulations of OPDA, we suggest that lipids containing OPDA (arabidopsides) play an important role in the activation of herbivory-induced responses.
Highlights
How plants perceive herbivory is not yet well understood
JA biosynthesis starts in the chloroplast with the release of a-linolenic acid, which is converted to 13hydroperoxy octadecatrienoic acid (13-HPOT) by 13lipoxygenases and subsequently into cyclopentenone 12-oxo-phytodienoic acid (OPDA) by the activity of allene oxide synthase and allene oxide cyclase
We found that feeding of the locust Schistocerca gregaria induced JA accumulation and ET release in Arabidopsis (Supplemental Fig. S1)
Summary
How plants perceive herbivory is not yet well understood. We investigated early responses of the model plant Arabidopsis (Arabidopsis thaliana) to attack from the generalist grasshopper herbivore, Schistocerca gregaria (Caelifera). Herbivore attack is transduced into specific defense responses by a sophisticated signaling system (for review, see Wu and Baldwin, 2010) This complex system, which consists of evolutionarily conserved defense pathways, is activated in various plant species by the perception of herbivory and HAMPS. JA-Ile is bound by the CORONATINEINSENSITIVE (COI1)-JA-zim domain protein complex, leading to the degradation of negative transcriptional regulators and the activation of signal transduction (Thines et al, 2007; Chini et al, 2009; Sheard et al, 2010) Until now, it was not completely elucidated in Arabidopsis (Arabidopsis thaliana) which lipases are involved in the supply of the precursors for JA biosynthesis. In Arabidopsis, OPDA is esterified in galactolipids, called arabidopsides (Stelmach et al, 2001; Hisamatsu et al, 2003, 2005; Andersson et al, 2006; Buseman et al, 2006; Nakajyo et al, 2006; Bottcher and Weiler, 2007; Kourtchenko et al, 2007)
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