Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly

Entomopathogenic fungi infect insects via spores but also live inside plant tissues as endophytes. Frequently, colonization by entomopathogens provides plants with increased resistance against insects, but the mechanisms are little understood. This study investigated direct, local, and systemic root...

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Main Authors: Catalina Posada-Vergara, Katharina Lohaus, Mohammad Alhussein, Stefan Vidal, Michael Rostás
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/8/9/969
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author Catalina Posada-Vergara
Katharina Lohaus
Mohammad Alhussein
Stefan Vidal
Michael Rostás
author_facet Catalina Posada-Vergara
Katharina Lohaus
Mohammad Alhussein
Stefan Vidal
Michael Rostás
author_sort Catalina Posada-Vergara
collection DOAJ
description Entomopathogenic fungi infect insects via spores but also live inside plant tissues as endophytes. Frequently, colonization by entomopathogens provides plants with increased resistance against insects, but the mechanisms are little understood. This study investigated direct, local, and systemic root-mediated interactions between isolates of the fungus <i>Metarhizium brunneum</i> and larvae of the cabbage root fly (CRF) <i>Delia radicum</i> attacking <i>Brassica napus</i> plants. All fungal isolates infected CRF when conidia were present in the soil, leading to 43–93% mortality. Locally, root-associated <i>M. brunneum</i> isolates reduced herbivore damage by 10–20% and in three out of five isolates caused significant insect mortality due to plant-mediated and/or direct effects. A split-root experiment with isolate Gd12 also demonstrated systemic plant resistance with significantly reduced root collar damage by CRF. LC-MS analyses showed that fungal root colonization did not induce changes in phytohormones, while herbivory increased jasmonic acid (JA) and glucosinolate concentrations. Proteinase inhibitor gene expression was also increased. Fungal colonization, however, primed herbivore-induced JA and the expression of the JA-responsive plant defensin 1.2 (PDF1.2) gene. We conclude that root-associated <i>M. brunneum</i> benefits plant health through multiple mechanisms, such as the direct infection of insects, as well as the local and systemic priming of the JA pathway.
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spelling doaj.art-d5ab55219f7241d4957bba14c988bd292023-11-23T17:10:05ZengMDPI AGJournal of Fungi2309-608X2022-09-018996910.3390/jof8090969Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root FlyCatalina Posada-Vergara0Katharina Lohaus1Mohammad Alhussein2Stefan Vidal3Michael Rostás4Agricultural Entomology, Department of Crop Sciences, University of Göttingen, Grisebachstr 6, 37077 Göttingen, GermanyAgricultural Entomology, Department of Crop Sciences, University of Göttingen, Grisebachstr 6, 37077 Göttingen, GermanyMolecular Phytopathology and Mycotoxin Research, Department of Crop Sciences, University of Göttingen, Grisebachstr 6, 37077 Göttingen, GermanyAgricultural Entomology, Department of Crop Sciences, University of Göttingen, Grisebachstr 6, 37077 Göttingen, GermanyAgricultural Entomology, Department of Crop Sciences, University of Göttingen, Grisebachstr 6, 37077 Göttingen, GermanyEntomopathogenic fungi infect insects via spores but also live inside plant tissues as endophytes. Frequently, colonization by entomopathogens provides plants with increased resistance against insects, but the mechanisms are little understood. This study investigated direct, local, and systemic root-mediated interactions between isolates of the fungus <i>Metarhizium brunneum</i> and larvae of the cabbage root fly (CRF) <i>Delia radicum</i> attacking <i>Brassica napus</i> plants. All fungal isolates infected CRF when conidia were present in the soil, leading to 43–93% mortality. Locally, root-associated <i>M. brunneum</i> isolates reduced herbivore damage by 10–20% and in three out of five isolates caused significant insect mortality due to plant-mediated and/or direct effects. A split-root experiment with isolate Gd12 also demonstrated systemic plant resistance with significantly reduced root collar damage by CRF. LC-MS analyses showed that fungal root colonization did not induce changes in phytohormones, while herbivory increased jasmonic acid (JA) and glucosinolate concentrations. Proteinase inhibitor gene expression was also increased. Fungal colonization, however, primed herbivore-induced JA and the expression of the JA-responsive plant defensin 1.2 (PDF1.2) gene. We conclude that root-associated <i>M. brunneum</i> benefits plant health through multiple mechanisms, such as the direct infection of insects, as well as the local and systemic priming of the JA pathway.https://www.mdpi.com/2309-608X/8/9/969endophytic entomopathogenic fungi<i>Delia radicum</i><i>Metarhizium brunneum</i><i>Brassica napus</i>plant-fungal-insect interactionssplit-root
spellingShingle Catalina Posada-Vergara
Katharina Lohaus
Mohammad Alhussein
Stefan Vidal
Michael Rostás
Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly
Journal of Fungi
endophytic entomopathogenic fungi
<i>Delia radicum</i>
<i>Metarhizium brunneum</i>
<i>Brassica napus</i>
plant-fungal-insect interactions
split-root
title Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly
title_full Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly
title_fullStr Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly
title_full_unstemmed Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly
title_short Root Colonization by Fungal Entomopathogen Systemically Primes Belowground Plant Defense against Cabbage Root Fly
title_sort root colonization by fungal entomopathogen systemically primes belowground plant defense against cabbage root fly
topic endophytic entomopathogenic fungi
<i>Delia radicum</i>
<i>Metarhizium brunneum</i>
<i>Brassica napus</i>
plant-fungal-insect interactions
split-root
url https://www.mdpi.com/2309-608X/8/9/969
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AT katharinalohaus rootcolonizationbyfungalentomopathogensystemicallyprimesbelowgroundplantdefenseagainstcabbagerootfly
AT mohammadalhussein rootcolonizationbyfungalentomopathogensystemicallyprimesbelowgroundplantdefenseagainstcabbagerootfly
AT stefanvidal rootcolonizationbyfungalentomopathogensystemicallyprimesbelowgroundplantdefenseagainstcabbagerootfly
AT michaelrostas rootcolonizationbyfungalentomopathogensystemicallyprimesbelowgroundplantdefenseagainstcabbagerootfly