Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids

The effects of microorganisms on plant-insect interactions have usually been underestimated. While plant growth-promoting rhizobacteria (PGPR) are known to induce plant defenses, endosymbiotic bacteria hosted by herbivorous insects are often beneficial to the host. Here, we aimed to assess whether P...

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Main Authors: Laurent Serteyn, Céleste Quaghebeur, Marc Ongena, Nuri Cabrera, Andrea Barrera, Marco A. Molina-Montenegro, Frédéric Francis, Claudio C. Ramírez
Format: Article
Language:English
Published: MDPI AG 2020-04-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/11/4/234
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author Laurent Serteyn
Céleste Quaghebeur
Marc Ongena
Nuri Cabrera
Andrea Barrera
Marco A. Molina-Montenegro
Frédéric Francis
Claudio C. Ramírez
author_facet Laurent Serteyn
Céleste Quaghebeur
Marc Ongena
Nuri Cabrera
Andrea Barrera
Marco A. Molina-Montenegro
Frédéric Francis
Claudio C. Ramírez
author_sort Laurent Serteyn
collection DOAJ
description The effects of microorganisms on plant-insect interactions have usually been underestimated. While plant growth-promoting rhizobacteria (PGPR) are known to induce plant defenses, endosymbiotic bacteria hosted by herbivorous insects are often beneficial to the host. Here, we aimed to assess whether PGPR-induced defenses in broad bean plants impact the pea aphid, depending on its genotype and the presence of endosymbionts. We estimated aphid reproduction, quantified defense- and growth-related phytohormones by GC-MS, and measured different plant growth and physiology parameters, after PGPR treatment. In addition, we recorded the feeding behavior of aphids by electropenetrography. We found that the PGPR treatment of broad bean plants reduced the reproduction of one of the pea aphid clones. We highlighted a phenomenon of PGPR-induced plant defense priming, but no noticeable plant growth promotion. The main changes in aphid probing behavior were related to salivation events into phloem sieve elements. We suggest that the endosymbiont <i>Hamiltonella defensa</i> played a key role in plant-insect interactions, possibly helping aphids to counteract plant-induced resistance and allowing them to develop normally on PGPR-treated plants. Our results imply that plant- and aphid-associated microorganisms add greater complexity to the outcomes of aphid-plant interactions.
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spelling doaj.art-29f73bc24c2344ea90fc0489da52fbbf2023-11-19T20:58:44ZengMDPI AGInsects2075-44502020-04-0111423410.3390/insects11040234Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of AphidsLaurent Serteyn0Céleste Quaghebeur1Marc Ongena2Nuri Cabrera3Andrea Barrera4Marco A. Molina-Montenegro5Frédéric Francis6Claudio C. Ramírez7Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege, Passage des Déportés 2, B-5030 Gembloux, BelgiumFunctional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege, Passage des Déportés 2, B-5030 Gembloux, BelgiumMicrobial Processes and Interactions Research Unit, Gembloux Agro-Bio Tech, University of Liege, B-5030 Gembloux, BelgiumLaboratorio Interacciones Insecto-Planta, Instituto de Ciencias Biológicas, Universidad de Talca, 1141 Talca, ChileLaboratorio de Ecología Vegetal, Instituto de Ciencias Biológicas, Universidad de Talca, 1141 Talca, ChileLaboratorio de Ecología Vegetal, Instituto de Ciencias Biológicas, Universidad de Talca, 1141 Talca, ChileFunctional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege, Passage des Déportés 2, B-5030 Gembloux, BelgiumLaboratorio Interacciones Insecto-Planta, Instituto de Ciencias Biológicas, Universidad de Talca, 1141 Talca, ChileThe effects of microorganisms on plant-insect interactions have usually been underestimated. While plant growth-promoting rhizobacteria (PGPR) are known to induce plant defenses, endosymbiotic bacteria hosted by herbivorous insects are often beneficial to the host. Here, we aimed to assess whether PGPR-induced defenses in broad bean plants impact the pea aphid, depending on its genotype and the presence of endosymbionts. We estimated aphid reproduction, quantified defense- and growth-related phytohormones by GC-MS, and measured different plant growth and physiology parameters, after PGPR treatment. In addition, we recorded the feeding behavior of aphids by electropenetrography. We found that the PGPR treatment of broad bean plants reduced the reproduction of one of the pea aphid clones. We highlighted a phenomenon of PGPR-induced plant defense priming, but no noticeable plant growth promotion. The main changes in aphid probing behavior were related to salivation events into phloem sieve elements. We suggest that the endosymbiont <i>Hamiltonella defensa</i> played a key role in plant-insect interactions, possibly helping aphids to counteract plant-induced resistance and allowing them to develop normally on PGPR-treated plants. Our results imply that plant- and aphid-associated microorganisms add greater complexity to the outcomes of aphid-plant interactions.https://www.mdpi.com/2075-4450/11/4/234<i>Acyrthosiphon pisum</i><i>Bacillus amyloliquefaciens</i>electropenetrography<i>Hamiltonella defensa</i>interactionsplant growth-promoting rhizobacteria (PGPR)
spellingShingle Laurent Serteyn
Céleste Quaghebeur
Marc Ongena
Nuri Cabrera
Andrea Barrera
Marco A. Molina-Montenegro
Frédéric Francis
Claudio C. Ramírez
Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids
Insects
<i>Acyrthosiphon pisum</i>
<i>Bacillus amyloliquefaciens</i>
electropenetrography
<i>Hamiltonella defensa</i>
interactions
plant growth-promoting rhizobacteria (PGPR)
title Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids
title_full Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids
title_fullStr Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids
title_full_unstemmed Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids
title_short Induced Systemic Resistance by a Plant Growth-Promoting Rhizobacterium Impacts Development and Feeding Behavior of Aphids
title_sort induced systemic resistance by a plant growth promoting rhizobacterium impacts development and feeding behavior of aphids
topic <i>Acyrthosiphon pisum</i>
<i>Bacillus amyloliquefaciens</i>
electropenetrography
<i>Hamiltonella defensa</i>
interactions
plant growth-promoting rhizobacteria (PGPR)
url https://www.mdpi.com/2075-4450/11/4/234
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