Herbivory Rapidly Activates MAPK Signaling in Attacked and Unattacked Leaf Regions but Not between Leaves ofNicotiana attenuata

Abstract

Mitogen-activated protein kinase (MAPK) signaling plays a central role in transducing extracellular stimuli into intracellular responses, but its role in mediating plant responses to herbivore attack remains largely unexplored. When Manduca sexta larvae attack their host plant, Nicotiana attenuata, the plant's wound response is reconfigured at transcriptional, phytohormonal, and defensive levels due to the introduction of oral secretions (OS) into wounds during feeding. We show that OS dramatically amplify wound-induced MAPK activity and that fatty acid-amino acid conjugates in M. sexta OS are the elicitors. Virus-induced gene silencing of salicylic acid-induced protein kinase (SIPK) and wound-induced protein kinase revealed their importance in mediating wound and OS-elicited hormonal responses and transcriptional regulation of defense-related genes. We found that after applying OS to wounds created in one portion of a leaf, SIPK is activated in both wounded and specific unwounded regions of the leaf but not in phylotactically connected adjacent leaves. We propose that M. sexta attack elicits a mobile signal that travels to nonwounded regions of the attacked leaf where it activates MAPK signaling and, thus, downstream responses; subsequently, a different signal is transported by the vascular system to systemic leaves to initiate defense responses without activating MAPKs in systemic leaves.

A Comparison of Two Nicotiana attenuata Accessions Reveals Large Differences in Signaling Induced by Oral Secretions of the Specialist Herbivore Manduca sexta

“…Similar results were obtained in an independently repeated experiment (Supplemental Fig. S1), as well as in another experiment in which synthetic FACs, the components of M. sexta OS that elicit MAPKs (Wu et al, 2007a), were used (Supplemental Fig. S2).…”

“…S2). Activity levels of WIPK were much lower than those of SIPK (Wu et al, 2007a) and show a weak band in the in-gel kinase assay (Fig. 2); no difference between UT and AZ was detected.…”

“…Activation of SIPK and WIPK, upstream signal transduction components that modulate downstream phytohormonal and transcriptional changes in plants, is crucial for plants' ability to initiate herbivore resistance (Zhang and Klessig, 2001;Liu and Zhang, 2004;Wu et al, 2007a).…”

“…The moment M. sexta begins to feed, a cascade of signaling events leads to increased defense levels (Fig. 1); N. attenuata plants recognize herbivory-specific elicitors derived from M. sexta oral secretions (OS), namely, fatty acidamino acid conjugates (FACs), and quickly activate mitogen-activated protein kinase (MAPK) signaling and, subsequently, JA-and ethylene (ET)-mediated defense responses Halitschke and Baldwin, 2003;Wu et al, 2007a). These include: (1) a highly reconfigured transcriptome that encompasses changes in transcript levels of defense-and growthrelated genes; (2) the release of volatile organic compounds (VOCs) that function as an indirect defense; and (3) the accumulation of herbivore-deterrent or -damaging secondary metabolites, for example, nicotine and trypsin proteinase inhibitors (TPIs; Reymond and Farmer, 1998;Hermsmeier et al, 2001;Kessler and Baldwin, 2001;Zavala et al, 2004b).…”

Comparative analyses of transcriptome and proteome in response to cotton bollworm between a resistant wild soybean and a susceptible soybean cultivar

“…Previous studies found that SA could inhibit the expression of some antiherbivore related genes in potato (Sivasankar et al 2000), and the decrease of SA content in response to Manduca sexta in Nicotiana attenuata was correlated to the induction of defense responses (Gilardoni et al 2011). Interestingly, a minor increase of endogenous SA content in response to M. sexta in N. attenuata was also reported, suggesting a complicated role of SA in herbivory defense responses (Wu et al 2007). In our studies, the SA responsive gene, GmPR1 (Glyma15g06780.…”