Lipase Activity in Insect Oral Secretions Mediates Defense Responses in Arabidopsis      

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.

Nicotiana attenuata LECTIN RECEPTOR KINASE1 Suppresses the Insect-Mediated Inhibition of Induced Defense Responses during Manduca sexta Herbivory

“…result consistent with undetectable levels of FACs in the S. gregaria OS (Schmelz et al, 2009;Schä fer et al, 2011).…”

CML42-Mediated Calcium Signaling Coordinates Responses to Spodoptera Herbivory and Abiotic Stresses in Arabidopsis

“…Our data here show that S. littoralis OS induces cytosolic Ca 2+ and phytohormone elevation in Arabidopsis and thus activates defense. It is interesting that both JA and cis-OPDA show prolonged elevation upon OS treatment, indicating a sustained defense by plants, as reported for grasshopper OS in Arabidopsis (Schäfer et al, 2011).…”

“…This cascade was reported to directly impact transcription factors for defense responses independent of phytohormone-related signaling pathways (Kanchiswamy et al, 2010). In the case of interaction between Arabidopsis with the generalist grasshopper herbivore Schistocerca gregaria, application of grasshopper OS to puncture wounds elicited increased cytosolic Ca 2+ and phytohormone levels (Schäfer et al, 2011). Ca 2+ has also been implicated in downstream parts of herbivoretriggered signaling cascades, because jasmonates and synthetic analogs induce Ca 2+ elevations in tobacco (Nicotiana benthamiana) BY-2 cell culture (Walter et al, 2007).…”

Mechanisms of plant defense against insect herbivores

“…123 The lipase activity of grasshopper oral secretions evoked an immediate and quick accumulation of various oxylipins, such as, 13-hydroperoxy octadecatrienoic acid, 12-oxo-phytodienoic acid (OPDA), JA, and jasmonic acid-isoleucine in Arabidopsis. 124 Furthermore, there was increase in cytosolic calcium, ethylene emission and activity of MAPKs on treatment with grasshopper oral secretions.…”