The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes

The fungal endophyte <i>Penicillium olsonii</i> ML37 is a biocontrol agent of Fusarium head blight in wheat (caused by <i>Fusarium graminearum</i>), which has shown a limited direct inhibition of fungal growth in vitro. We used RNA-seq and LC-MS/MS analyses to elucidate metab...

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Main Authors: Edward C. Rojas, Birgit Jensen, Hans J. L. Jørgensen, Meike A. C. Latz, Pilar Esteban, David B. Collinge
Format: Article
Language:English
Published: MDPI AG 2022-03-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/8/4/345
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author Edward C. Rojas
Birgit Jensen
Hans J. L. Jørgensen
Meike A. C. Latz
Pilar Esteban
David B. Collinge
author_facet Edward C. Rojas
Birgit Jensen
Hans J. L. Jørgensen
Meike A. C. Latz
Pilar Esteban
David B. Collinge
author_sort Edward C. Rojas
collection DOAJ
description The fungal endophyte <i>Penicillium olsonii</i> ML37 is a biocontrol agent of Fusarium head blight in wheat (caused by <i>Fusarium graminearum</i>), which has shown a limited direct inhibition of fungal growth in vitro. We used RNA-seq and LC-MS/MS analyses to elucidate metabolic interactions of the three-way system Penicillium–wheat–Fusarium in greenhouse experiments. We demonstrated that <i>P. olsonii</i> ML37 colonises wheat spikes and transiently activates plant defence mechanisms, as pretreated spikes show a faster and stronger expression of the defence metabolism during the first 24 h after pathogen inoculation. This effect was transient and the expression of the same genes was lower in the pathogen-infected spikes than in those infected by <i>P. olsonii</i> alone. This response to the endophyte includes the transcriptional activation of several WRKY transcription factors. This early activation is associated with a reduction in FHB symptoms and significantly lower levels of the <i>F. graminearum</i> metabolites 15-acetyl-DON and culmorin. An increase in the Penicillium-associated metabolite asperphanamate confirms colonisation by the endophyte. Our results suggest that the mode of action used by <i>P. olsonii</i> ML37 is via a local defence activation in wheat spikes, and that this fungus has potential as a novel biological alternative in wheat disease control.
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spelling doaj.art-5149b8b6aa7e42ec804e4695c10625492023-12-03T13:34:27ZengMDPI AGJournal of Fungi2309-608X2022-03-018434510.3390/jof8040345The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat SpikesEdward C. Rojas0Birgit Jensen1Hans J. L. Jørgensen2Meike A. C. Latz3Pilar Esteban4David B. Collinge5Section for Microbial Ecology and Biotechnology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Copenhagen, DenmarkSection for Microbial Ecology and Biotechnology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Copenhagen, DenmarkCopenhagen Plant Science Centre, University of Copenhagen, Thorvaldsensvej 40, 1871 Copenhagen, DenmarkCopenhagen Plant Science Centre, University of Copenhagen, Thorvaldsensvej 40, 1871 Copenhagen, DenmarkSection for Microbial Ecology and Biotechnology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Copenhagen, DenmarkSection for Microbial Ecology and Biotechnology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Copenhagen, DenmarkThe fungal endophyte <i>Penicillium olsonii</i> ML37 is a biocontrol agent of Fusarium head blight in wheat (caused by <i>Fusarium graminearum</i>), which has shown a limited direct inhibition of fungal growth in vitro. We used RNA-seq and LC-MS/MS analyses to elucidate metabolic interactions of the three-way system Penicillium–wheat–Fusarium in greenhouse experiments. We demonstrated that <i>P. olsonii</i> ML37 colonises wheat spikes and transiently activates plant defence mechanisms, as pretreated spikes show a faster and stronger expression of the defence metabolism during the first 24 h after pathogen inoculation. This effect was transient and the expression of the same genes was lower in the pathogen-infected spikes than in those infected by <i>P. olsonii</i> alone. This response to the endophyte includes the transcriptional activation of several WRKY transcription factors. This early activation is associated with a reduction in FHB symptoms and significantly lower levels of the <i>F. graminearum</i> metabolites 15-acetyl-DON and culmorin. An increase in the Penicillium-associated metabolite asperphanamate confirms colonisation by the endophyte. Our results suggest that the mode of action used by <i>P. olsonii</i> ML37 is via a local defence activation in wheat spikes, and that this fungus has potential as a novel biological alternative in wheat disease control.https://www.mdpi.com/2309-608X/8/4/345asperphenamatebiological controlculmorinendophyteFusarium head blightinduced resistance
spellingShingle Edward C. Rojas
Birgit Jensen
Hans J. L. Jørgensen
Meike A. C. Latz
Pilar Esteban
David B. Collinge
The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes
Journal of Fungi
asperphenamate
biological control
culmorin
endophyte
Fusarium head blight
induced resistance
title The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes
title_full The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes
title_fullStr The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes
title_full_unstemmed The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes
title_short The Fungal Endophyte <i>Penicillium olsonii</i> ML37 Reduces Fusarium Head Blight by Local Induced Resistance in Wheat Spikes
title_sort fungal endophyte i penicillium olsonii i ml37 reduces fusarium head blight by local induced resistance in wheat spikes
topic asperphenamate
biological control
culmorin
endophyte
Fusarium head blight
induced resistance
url https://www.mdpi.com/2309-608X/8/4/345
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