Abstract
BackgroundHerbivory induces the activation of mitogen-activated protein kinases (MAPKs), the accumulation of jasmonates and defensive metabolites in damaged leaves and in distal undamaged leaves. Previous studies mainly focused on individual responses and a limited number of systemic leaves, and more research is needed for a better understanding of how different plant parts respond to herbivory. In the wild tobacco Nicotiana attenuata, FACs (fatty acid-amino acid conjugates) in Manduca sexta oral secretions (OS) are the major elicitors that induce herbivory-specific signaling but their role in systemic signaling is largely unknown.ResultsHere, we show that simulated herbivory (adding M. sexta OS to fresh wounds) dramatically increased SIPK (salicylic acid-induced protein kinase) activity and jasmonic acid (JA) levels in damaged leaves and in certain (but not all) undamaged systemic leaves, whereas wounding alone had no detectable systemic effects; importantly, FACs and wounding are both required for activating these systemic responses. In contrast to the activation of SIPK and elevation of JA in specific systemic leaves, increases in the activity of an important anti-herbivore defense, trypsin proteinase inhibitor (TPI), were observed in all systemic leaves after simulated herbivory, suggesting that systemic TPI induction does not require SIPK activation and JA increases. Leaf ablation experiments demonstrated that within 10 minutes after simulated herbivory, a signal (or signals) was produced and transported out of the treated leaves, and subsequently activated systemic responses.ConclusionsOur results reveal that N. attenuata specifically recognizes herbivore-derived FACs in damaged leaves and rapidly send out a long-distance signal to phylotactically connected leaves to activate MAPK and JA signaling, and we propose that FACs that penetrated into wounds rapidly induce the production of another long-distance signal(s) which travels to all systemic leaves and activates TPI defense.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0326-z) contains supplementary material, which is available to authorized users.
Highlights
Herbivory induces the activation of mitogen-activated protein kinases (MAPKs), the accumulation of jasmonates and defensive metabolites in damaged leaves and in distal undamaged leaves
We found that a rapid mobile signal induces salicylic acid-induced protein kinase (SIPK) activation and jasmonic acid (JA)/JA-isoleucine conjugate (JA-Ile) accumulation in certain, but not all, systemic leaves in N. attenuata, and the production of this signal is highly dependent on fatty acid-amino acid conjugates (FACs) in M. sexta oral secretions (OS) that are introduced into wounds during feeding; neither wounding nor FACs alone can induce elevated SIPK activity and JA/JA-Ile levels in systemic leaves
Using trypsin proteinase inhibitor (TPI) activity assay and leaf ablation approach, we demonstrate that the pattern of TPI induction is different from that of systemically induced SIPK and JA/JA-Ile, and we propose that another signal travels at a similar speed to almost all systemic leaves to activate TPI biosynthesis
Summary
Herbivory induces the activation of mitogen-activated protein kinases (MAPKs), the accumulation of jasmonates and defensive metabolites in damaged leaves and in distal undamaged leaves. In the wild tobacco Nicotiana attenuata, FACs (fatty acid-amino acid conjugates) in Manduca sexta oral secretions (OS) are the major elicitors that induce herbivory-specific signaling but their role in systemic signaling is largely unknown. Herbivores pose a major threat to plants To cope with this challenge, plants have evolved sophisticated defense systems to perceive damage and herbivore-derived elicitors (the so-called herbivore-associated molecular patterns, HAMPs) [1] and activate a chain reaction of downstream. Nicotiana attenuata, in addition to PIs, transcriptional and metabolomic analyses indicated that various genes and metabolites are up-regulated in systemic undamaged leaves and roots [7,8,9]. Wounding or herbivory activates MAPKs within a few minutes [3,4,14,15] and rapidly induces the biosynthesis of JA, with levels peaking within 1–2 h [16,17]
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
