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Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase

Biotic stresses induced by herbivores result in diverse physiological changes in plants. In the interaction between the Lima bean (Phaseolus lunatus) and the herbivore Spodoptera littoralis, the earliest event induced by feeding on leaves is the depolarization of the plasma membrane potential (Vm),...

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Autores principales: Camoni, Lorenzo, Barbero, Francesca, Aducci, Patrizia, Maffei, Massimo E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6086434/
https://www.ncbi.nlm.nih.gov/pubmed/30096181
http://dx.doi.org/10.1371/journal.pone.0202142
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author Camoni, Lorenzo
Barbero, Francesca
Aducci, Patrizia
Maffei, Massimo E.
author_facet Camoni, Lorenzo
Barbero, Francesca
Aducci, Patrizia
Maffei, Massimo E.
author_sort Camoni, Lorenzo
collection PubMed
description Biotic stresses induced by herbivores result in diverse physiological changes in plants. In the interaction between the Lima bean (Phaseolus lunatus) and the herbivore Spodoptera littoralis, the earliest event induced by feeding on leaves is the depolarization of the plasma membrane potential (Vm), which is the results of both mechanical damage and insect oral secretions (OS). Although this herbivore-induced Vm depolarization depends on a calcium-dependent opening of potassium channels, the attacked leaf remains depolarized for an extended period, which cannot be explained by the sole action of potassium channels. Here we show that the plasma membrane H(+)-ATPase of P. lunatus leaves is strongly inhibited by S. littoralis OS. Inhibition of the H(+)-ATPase was also found in plasma membranes purified from leaf sections located distally from the application zone of OS, thus suggesting a long-distance transport of a signaling molecule(s). S. littoralis’ OS did not influence the amount of the plasma membrane H(+)-ATPase, whereas the levels of membrane-bound 14-3-3 proteins were significantly decreased in membranes purified from treated leaves. Furthermore, OS strongly reduced the in vitro interaction between P. lunatus H(+)-ATPase and 14-3-3 proteins. The results of this work demonstrate that inhibition of the plasma membrane H(+)-ATPase is a key component of the S. littoralis OS mechanism leading to an enduring Vm depolarization in P. lunatus wounded leaves.
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spelling pubmed-60864342018-08-28 Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase Camoni, Lorenzo Barbero, Francesca Aducci, Patrizia Maffei, Massimo E. PLoS One Research Article Biotic stresses induced by herbivores result in diverse physiological changes in plants. In the interaction between the Lima bean (Phaseolus lunatus) and the herbivore Spodoptera littoralis, the earliest event induced by feeding on leaves is the depolarization of the plasma membrane potential (Vm), which is the results of both mechanical damage and insect oral secretions (OS). Although this herbivore-induced Vm depolarization depends on a calcium-dependent opening of potassium channels, the attacked leaf remains depolarized for an extended period, which cannot be explained by the sole action of potassium channels. Here we show that the plasma membrane H(+)-ATPase of P. lunatus leaves is strongly inhibited by S. littoralis OS. Inhibition of the H(+)-ATPase was also found in plasma membranes purified from leaf sections located distally from the application zone of OS, thus suggesting a long-distance transport of a signaling molecule(s). S. littoralis’ OS did not influence the amount of the plasma membrane H(+)-ATPase, whereas the levels of membrane-bound 14-3-3 proteins were significantly decreased in membranes purified from treated leaves. Furthermore, OS strongly reduced the in vitro interaction between P. lunatus H(+)-ATPase and 14-3-3 proteins. The results of this work demonstrate that inhibition of the plasma membrane H(+)-ATPase is a key component of the S. littoralis OS mechanism leading to an enduring Vm depolarization in P. lunatus wounded leaves. Public Library of Science 2018-08-10 /pmc/articles/PMC6086434/ /pubmed/30096181 http://dx.doi.org/10.1371/journal.pone.0202142 Text en © 2018 Camoni et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Camoni, Lorenzo
Barbero, Francesca
Aducci, Patrizia
Maffei, Massimo E.
Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase
title Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase
title_full Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase
title_fullStr Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase
title_full_unstemmed Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase
title_short Spodoptera littoralis oral secretions inhibit the activity of Phaseolus lunatus plasma membrane H(+)-ATPase
title_sort spodoptera littoralis oral secretions inhibit the activity of phaseolus lunatus plasma membrane h(+)-atpase
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6086434/
https://www.ncbi.nlm.nih.gov/pubmed/30096181
http://dx.doi.org/10.1371/journal.pone.0202142
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