An Ecological Analysis of the Herbivory-Elicited JA Burst and Its Metabolism: Plant Memory Processes and Predictions of the Moving Target Model

Abstract

BackgroundRapid herbivore-induced jasmonic acid (JA) accumulation is known to mediate many induced defense responses in vascular plants, but little is known about how JA bursts are metabolized and modified in response to repeated elicitations, are propagated throughout elicited leaves, or how they directly influence herbivores.Methodology/Principal FindingsWe found the JA burst in a native population of Nicotiana attenuata to be highly robust despite environmental variation and we examined the JA bursts produced by repeated elicitations with Manduca sexta oral secretions (OS) at whole- and within-leaf spatial scales. Surprisingly, a 2nd OS-elicitation suppressed an expected JA burst at both spatial scales, but subsequent elicitations caused more rapid JA accumulation in elicited tissue. The baseline of induced JA/JA-Ile increased with number of elicitations in discrete intervals. Large veins constrained the spatial spread of JA bursts, leading to heterogeneity within elicited leaves. 1st-instar M. sexta larvae were repelled by elicitations and changed feeding sites. JA conjugated with isoleucine (JA-Ile) translates elicitations into defense production (e.g., TPIs), but conjugation efficiency varied among sectors and depended on NaWRKY3/6 transcription factors. Elicited TPI activity correlated strongly with the heterogeneity of JA/JA-Ile accumulations after a single elicitation, but not repeated elicitations.Conclusions/SignificanceEcologically informed scaling of leaf elicitation reveals the contribution of repeated herbivory events to the formation of plant memory of herbivory and the causes and importance of heterogeneity in induced defense responses. Leaf vasculature, in addition to transmitting long-distance damage cues, creates heterogeneity in JA bursts within attacked leaves that may be difficult for an attacking herbivore to predict. Such unpredictability is a central tenet of the Moving Target Model of defense, which posits that variability in itself is defensive.

R2R3-NaMYB8 Regulates the Accumulation of Phenylpropanoid-Polyamine Conjugates, Which Are Essential for Local and Systemic Defense against Insect Herbivores inNicotiana attenuata

“…This experimental setup was specifically designed to mimic the initial feeding of the rosette leaves by neonates just hatched from oviposited eggs, before they increased size and mobility of first instar larvae migrating to other plant parts (Stork et al, 2009). Both generalist and specialist herbivores were allowed to feed only on systemically induced young stem leaves (Fig.…”

Transcriptional regulation of plant inducible defenses against herbivores: a mini-review

“…In many plant species, JA/JA-Ile burst start immediately after herbivore attack, with the accumulation attaining maximum levels in a few hours. For example, in N. attenuata maximum JA accumulations are attained in leaves one hour after simulated herbivore attack (Stork et al 2009). Similar trends were reported in plants belonging to Solanaceae, Brassicaceae, Poaceae, and Salicaceae families (Pauwels et al 2009;Wasternack and Kombrink 2010).…”

Effects of mechanostimulation on gravitropism and signal persistence in flax roots

“…Memory effects have been linked to temperature [10][11][12] drought stress, 13,14 ozone stress, 15 and herbivory. 16,17 As diverse as the remembered stimuli are the underlying mechanisms of memory function. Cold memory depends on methylation of cold-responsive genes 18,19 that integrates week-long temperature shifts for robust flower induction 20 and extends over generations.…”