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Fragments of ATP synthase mediate plant perception of insect attack.

ABSTRACT: Plants can perceive a wide range of biotic attackers and respond with targeted induced defenses. Specificity in plant non-self-recognition occurs either directly by perception of pest-derived elicitors or indirectly through resistance protein recognition of host targets that are inappropriately proteolyzed. Indirect plant perception can occur during interactions with pathogens, yet evidence for analogous events mediating the detection of insect herbivores remains elusive. Here we report indirect perception of herbivory in cowpea (Vigna unguiculata) plants attacked by fall armyworm (Spodoptera frugiperda) larvae. We isolated and identified a disulfide-bridged peptide (+ICDINGVCVDA-), termed inceptin, from S. frugiperda larval oral secretions that promotes cowpea ethylene production at 1 fmol leaf(-1) and triggers increases in the defense-related phytohormones salicylic acid and jasmonic acid. Inceptins are proteolytic fragments of chloroplastic ATP synthase gamma-subunit regulatory regions that mediate plant perception of herbivory through the induction of volatile, phenylpropanoid, and protease inhibitor defenses. Only S. frugiperda larvae that previously ingested chloroplastic ATP synthase gamma-subunit proteins and produced inceptins significantly induced cowpea defenses after herbivory. Digestive fragments of an ancient and essential plant enzyme, inceptin functions as a potent indirect signal initiating specific plant responses to insect attack.

SUBMITTER: Schmelz EA

PROVIDER: S-EPMC1482674 | biostudies-literature | 2006 Jun

REPOSITORIES: biostudies-literature

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Fragments of ATP synthase mediate plant perception of insect attack.

Schmelz Eric A EA Carroll Mark J MJ LeClere Sherry S Phipps Stephen M SM Meredith Julia J Chourey Prem S PS Alborn Hans T HT Teal Peter E A PE

Proceedings of the National Academy of Sciences of the United States of America 20060523 23

Plants can perceive a wide range of biotic attackers and respond with targeted induced defenses. Specificity in plant non-self-recognition occurs either directly by perception of pest-derived elicitors or indirectly through resistance protein recognition of host targets that are inappropriately proteolyzed. Indirect plant perception can occur during interactions with pathogens, yet evidence for analogous events mediating the detection of insect herbivores remains elusive. Here we report indirect ...[more]

PMID: 16720701

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Project description:Plant defenses against pathogens and insects are regulated differentially by cross-communicating signaling pathways in which salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) play key roles. To understand how plants integrate pathogen- and insect-induced signals into specific defense responses, we monitored the dynamics of SA, JA, and ET signaling in Arabidopsis after attack by a set of microbial pathogens and herbivorous insects with different modes of attack. Arabidopsis plants were exposed to a pathogenic leaf bacterium (Pseudomonas syringae pv. tomato), a pathogenic leaf fungus (Alternaria brassicicola), tissue-chewing caterpillars (Pieris rapae), cell-content-feeding thrips (Frankliniella occidentalis), or phloem-feeding aphids (Myzus persicae). Monitoring the signal signature in each plant-attacker combination showed that the kinetics of SA, JA, and ET production varies greatly in both quantity and timing. Analysis of global gene expression profiles demonstrated that the signal signature characteristic of each Arabidopsis-attacker combination is orchestrated into a surprisingly complex set of transcriptional alterations in which, in all cases, stress-related genes are overrepresented. Comparison of the transcript profiles revealed that consistent changes induced by pathogens and insects with very different modes of attack can show considerable overlap. Of all consistent changes induced by A. brassicicola, P. rapae, and F. occidentalis, more than 50% were also induced consistently by P. syringae. Notably, although these four attackers all stimulated JA biosynthesis, the majority of the changes in JA-responsive gene expression were attacker-specific. All together our study shows that SA, JA, and ET play a primary role in the orchestration of the plant's defense response, but other regulatory mechanisms, such as pathway cross-talk or additional attacker-induced signals, eventually shape the highly complex attacker-specific defense response. In the experimental set up we intended to select for genes that showed a more than 2-fold change in the same direction(up or down)at two time points after pathogen or insect attack. The results are described in the following paper: De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., Van Pelt, J.A., Pozo, M.J., Mueller, M.J., Buchala, A.J., Metraux, J.-P., Van Loon, L.C., Dicke, M. and Pieterse, C.M.J. (2005). Signal signature and transcriptome changes in Arabidopsis upon pathogen and insect attack. Molecular Plant-Microbe Interactions. Experimenter name = Corne Pieterse Experimenter phone = +31 30 253 3013 Experimenter fax = +31 30 251 8366 Experimenter department = Section Phytopathology Experimenter institute = Utrecht University Experimenter address = Department of Biology Experimenter address = Utrecht University Experimenter address = Sorbonnelaan 16 Experimenter address = Utrecht Experimenter zip/postal_code = 3584CA Experimenter country = The Netherlands Keywords: time_series_design; pathogenicity_design

Project description:Plant defenses against pathogens and insects are regulated differentially by cross-communicating signaling pathways in which salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) play key roles. To understand how plants integrate pathogen- and insect-induced signals into specific defense responses, we monitored the dynamics of SA, JA, and ET signaling in Arabidopsis after attack by a set of microbial pathogens and herbivorous insects with different modes of attack. Arabidopsis plants were exposed to a pathogenic leaf bacterium (Pseudomonas syringae pv. tomato), a pathogenic leaf fungus (Alternaria brassicicola), tissue-chewing caterpillars (Pieris rapae), cell-content-feeding thrips (Frankliniella occidentalis), or phloem-feeding aphids (Myzus persicae). Monitoring the signal signature in each plant-attacker combination showed that the kinetics of SA, JA, and ET production varies greatly in both quantity and timing. Analysis of global gene expression profiles demonstrated that the signal signature characteristic of each Arabidopsis-attacker combination is orchestrated into a surprisingly complex set of transcriptional alterations in which, in all cases, stress-related genes are overrepresented. Comparison of the transcript profiles revealed that consistent changes induced by pathogens and insects with very different modes of attack can show considerable overlap. Of all consistent changes induced by A. brassicicola, P. rapae, and F. occidentalis, more than 50% were also induced consistently by P. syringae. Notably, although these four attackers all stimulated JA biosynthesis, the majority of the changes in JA-responsive gene expression were attacker-specific. All together our study shows that SA, JA, and ET play a primary role in the orchestration of the plant's defense response, but other regulatory mechanisms, such as pathway cross-talk or additional attacker-induced signals, eventually shape the highly complex attacker-specific defense response. In the experimental set up we intended to select for genes that showed a more than 2-fold change in the same direction(up or down)at two time points after pathogen or insect attack. The results are described in the following paper:; De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., Van Pelt, J.A., Pozo, M.J., Mueller, M.J., Buchala, A.J., Metraux, J.-P., Van Loon, L.C., Dicke, M. and Pieterse, C.M.J. (2005). Signal signature and transcriptome changes in Arabidopsis upon pathogen and insect attack. Molecular Plant-Microbe Interactions. Experimenter name = Corne Pieterse; Experimenter phone = +31 30 253 3013; Experimenter fax = +31 30 251 8366; Experimenter department = Section Phytopathology; Experimenter institute = Utrecht University; Experimenter address = Department of Biology; Experimenter address = Utrecht University; Experimenter address = Sorbonnelaan 16; Experimenter address = Utrecht; Experimenter zip/postal_code = 3584CA; Experimenter country = The Netherlands Experiment Overall Design: 14 samples were used in this experiment

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Fragments of ATP synthase mediate plant perception of insect attack.

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Fragments of ATP synthase mediate plant perception of insect attack.

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