Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis

Abstract Phoma stem canker disease of oilseed rape (Brassica napus) is caused by the extracellular fungal pathogen Leptosphaeria maculans. Although this pathogen resides exclusively in apoplastic spaces surrounding plant cells, the significance of extracellular vesicles (EVs) has not been assessed....

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Main Authors: Nathaniel Hearfield, Dominik Brotherton, Zedi Gao, Jameel Inal, Henrik U. Stotz
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Journal of Extracellular Biology
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Online Access:https://doi.org/10.1002/jex2.70029
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author Nathaniel Hearfield
Dominik Brotherton
Zedi Gao
Jameel Inal
Henrik U. Stotz
author_facet Nathaniel Hearfield
Dominik Brotherton
Zedi Gao
Jameel Inal
Henrik U. Stotz
author_sort Nathaniel Hearfield
collection DOAJ
description Abstract Phoma stem canker disease of oilseed rape (Brassica napus) is caused by the extracellular fungal pathogen Leptosphaeria maculans. Although this pathogen resides exclusively in apoplastic spaces surrounding plant cells, the significance of extracellular vesicles (EVs) has not been assessed. Here, we show a method to collect apoplastic fluids (AFs) from infected leaves or cotyledons for collection of EVs during the process of host colonisation. The 15,000 × g supernatants of AFs were shown to contain ribulose‐bisphosphate carboxylase (RuBisCO) at 7 days post‐inoculation with L. maculans, a protein that was absent from unchallenged cotyledons. RuBisCO release coincided with the switch from biotrophy to necrotrophy, suggesting the involvement of host cell death. However, RuBisCO release did not differ between compatible and incompatible interactions, suggesting necrotrophic host cell death might not be the only process involved. EVs were also collected from axenic fungal cultures and characterised for their particle size distribution using nanoparticle tracking analysis and transmission electron microscopy. The protein composition of EV‐enriched fractions was analysed using SDS‐PAGE and proteomics. Enrichment analysis of gene ontology terms provided evidence for involvement of glucan and chitin metabolism as well as catalase and peptidase activities. Most of the proteins identified have previously been found in EV studies and/or EV databases, and for most of the proteins evidence was found for an involvement in pathogenicity/virulence.
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spelling doaj-art-e5ea58d74ac74609987488dd5ee346de2025-08-20T02:45:04ZengWileyJournal of Extracellular Biology2768-28112025-02-0142n/an/a10.1002/jex2.70029Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesisNathaniel Hearfield0Dominik Brotherton1Zedi Gao2Jameel Inal3Henrik U. Stotz4Centre for Agriculture, Food and Environmental Management University of Hertfordshire Hatfield UKSchool of Life & Medical Sciences University of Hertfordshire Hatfield UKSchool of Life & Medical Sciences University of Hertfordshire Hatfield UKSchool of Life & Medical Sciences University of Hertfordshire Hatfield UKCentre for Agriculture, Food and Environmental Management University of Hertfordshire Hatfield UKAbstract Phoma stem canker disease of oilseed rape (Brassica napus) is caused by the extracellular fungal pathogen Leptosphaeria maculans. Although this pathogen resides exclusively in apoplastic spaces surrounding plant cells, the significance of extracellular vesicles (EVs) has not been assessed. Here, we show a method to collect apoplastic fluids (AFs) from infected leaves or cotyledons for collection of EVs during the process of host colonisation. The 15,000 × g supernatants of AFs were shown to contain ribulose‐bisphosphate carboxylase (RuBisCO) at 7 days post‐inoculation with L. maculans, a protein that was absent from unchallenged cotyledons. RuBisCO release coincided with the switch from biotrophy to necrotrophy, suggesting the involvement of host cell death. However, RuBisCO release did not differ between compatible and incompatible interactions, suggesting necrotrophic host cell death might not be the only process involved. EVs were also collected from axenic fungal cultures and characterised for their particle size distribution using nanoparticle tracking analysis and transmission electron microscopy. The protein composition of EV‐enriched fractions was analysed using SDS‐PAGE and proteomics. Enrichment analysis of gene ontology terms provided evidence for involvement of glucan and chitin metabolism as well as catalase and peptidase activities. Most of the proteins identified have previously been found in EV studies and/or EV databases, and for most of the proteins evidence was found for an involvement in pathogenicity/virulence.https://doi.org/10.1002/jex2.70029apoplastextracellular vesiclesnanoscalepectinphytopathogenprotein network
spellingShingle Nathaniel Hearfield
Dominik Brotherton
Zedi Gao
Jameel Inal
Henrik U. Stotz
Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
Journal of Extracellular Biology
apoplast
extracellular vesicles
nanoscale
pectin
phytopathogen
protein network
title Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
title_full Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
title_fullStr Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
title_full_unstemmed Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
title_short Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
title_sort establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis
topic apoplast
extracellular vesicles
nanoscale
pectin
phytopathogen
protein network
url https://doi.org/10.1002/jex2.70029
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AT dominikbrotherton establishmentofanexperimentalsystemtoanalyseextracellularvesiclesduringapoplasticfungalpathogenesis
AT zedigao establishmentofanexperimentalsystemtoanalyseextracellularvesiclesduringapoplasticfungalpathogenesis
AT jameelinal establishmentofanexperimentalsystemtoanalyseextracellularvesiclesduringapoplasticfungalpathogenesis
AT henrikustotz establishmentofanexperimentalsystemtoanalyseextracellularvesiclesduringapoplasticfungalpathogenesis