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Turnabout Is Fair Play: Herbivory-Induced Plant Chitinases Excreted in Fall Armyworm Frass Suppress Herbivore Defenses in Maize

The perception of herbivory by plants is known to be triggered by the deposition of insect-derived factors such as saliva and oral secretions, oviposition materials, and even feces. Such insect-derived materials harbor chemical cues that may elicit herbivore and/or pathogen-induced defenses in plant...

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Published in:Plant physiology (Bethesda) 2016-05, Vol.171 (1), p.694-706
Main Authors: Ray, Swayamjit, Alves, Patrick C.M.S., Ahmad, Imtiaz, Gaffoor, Iffa, Acevedo, Flor E., Peiffer, Michelle, Jin, Shan, Han, Yang, Shakeel, Samina, Felton, Gary W., Luthe, Dawn S.
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container_title Plant physiology (Bethesda)
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creator Ray, Swayamjit
Alves, Patrick C.M.S.
Ahmad, Imtiaz
Gaffoor, Iffa
Acevedo, Flor E.
Peiffer, Michelle
Jin, Shan
Han, Yang
Shakeel, Samina
Felton, Gary W.
Luthe, Dawn S.
description The perception of herbivory by plants is known to be triggered by the deposition of insect-derived factors such as saliva and oral secretions, oviposition materials, and even feces. Such insect-derived materials harbor chemical cues that may elicit herbivore and/or pathogen-induced defenses in plants. Several insect-derived molecules that trigger herbivore-induced defenses in plants are known; however, insect-derived molecules suppressing them are largely unknown. In this study, we identified two plant chitinases from fall armyworm (Spodoptera frugiperda) larval frass that suppress herbivore defenses while simultaneously inducing pathogen defenses in maize (Zea mays). Fall armyworm larvae feed in enclosed whorls of maize plants, where frass accumulates over extended periods of time in close proximity to damaged leaf tissue. Our study shows that maize chitinases, Pr4 and Endochitinase A, are induced during herbivory and subsequently deposited on the host with the feces. These plant chitinases mediate the suppression of herbivore-induced defenses, thereby increasing the performance of the insect on the host. Pr4 and Endochitinase A also trigger the antagonistic pathogen defense pathway in maize and suppress fungal pathogen growth on maize leaves. Frass-induced suppression of herbivore defenses by deposition of the plant-derived chitinases Pr4 and Endochitinase A is a unique way an insect can co-opt the plant's defense proteins for its own benefit. It is also a phenomenon unlike the induction of herbivore defenses by insect oral secretions in most host-herbivore systems.
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Such insect-derived materials harbor chemical cues that may elicit herbivore and/or pathogen-induced defenses in plants. Several insect-derived molecules that trigger herbivore-induced defenses in plants are known; however, insect-derived molecules suppressing them are largely unknown. In this study, we identified two plant chitinases from fall armyworm (Spodoptera frugiperda) larval frass that suppress herbivore defenses while simultaneously inducing pathogen defenses in maize (Zea mays). Fall armyworm larvae feed in enclosed whorls of maize plants, where frass accumulates over extended periods of time in close proximity to damaged leaf tissue. Our study shows that maize chitinases, Pr4 and Endochitinase A, are induced during herbivory and subsequently deposited on the host with the feces. These plant chitinases mediate the suppression of herbivore-induced defenses, thereby increasing the performance of the insect on the host. 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ispartof Plant physiology (Bethesda), 2016-05, Vol.171 (1), p.694-706
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source Oxford Journals Online; JSTOR Archival Journals
subjects Animals
Ascomycota - pathogenicity
Chitin - metabolism
Chitinases - genetics
Chitinases - metabolism
Feces - chemistry
Female
Herbivory
Host-Pathogen Interactions
Insect Proteins - metabolism
Larva
Plant Leaves
Plant Proteins - metabolism
Proteomics - methods
SIGNALING AND RESPONSE
Spodoptera - chemistry
Spodoptera - growth & development
Zea mays - enzymology
Zea mays - microbiology
title Turnabout Is Fair Play: Herbivory-Induced Plant Chitinases Excreted in Fall Armyworm Frass Suppress Herbivore Defenses in Maize
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