A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen

Abstract Secreted laccases are important enzymes on a broad ecological scale for their role in mediating plant-microbe interactions, but within ascomycete fungi these enzymes have been primarily associated with melanin biosynthesis. In this study, a putatively secreted laccase, Sslac2, was character...

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Main Authors: Nathaniel M. Westrick, Eddie G. Dominguez, Madeline Bondy, Christina M. Hull, Damon L. Smith, Mehdi Kabbage
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-06034-7
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author Nathaniel M. Westrick
Eddie G. Dominguez
Madeline Bondy
Christina M. Hull
Damon L. Smith
Mehdi Kabbage
author_facet Nathaniel M. Westrick
Eddie G. Dominguez
Madeline Bondy
Christina M. Hull
Damon L. Smith
Mehdi Kabbage
author_sort Nathaniel M. Westrick
collection DOAJ
description Abstract Secreted laccases are important enzymes on a broad ecological scale for their role in mediating plant-microbe interactions, but within ascomycete fungi these enzymes have been primarily associated with melanin biosynthesis. In this study, a putatively secreted laccase, Sslac2, was characterized from the broad-host-range plant pathogen Sclerotinia sclerotiorum, which is largely unpigmented and is not dependent on melanogenesis for plant infection. Gene knockouts of Sslac2 demonstrate wide ranging developmental phenotypes and are functionally non-pathogenic. These mutants also displayed indiscriminate growth behaviors and enhanced biomass formation, seemingly as a result of their inability to respond to canonical environmental growth cues, a phenomenon further confirmed through chemical stress, physiological, and transcriptomic analyses. Transmission and scanning electron microscopy demonstrate apparent differences in extracellular matrix structure between WT and mutant strains that likely explain the inability of the mutants to respond to their environment. Targeting Sslac2 using host-induced gene silencing significantly improved resistance to S. sclerotiorum, suggesting that fungal laccases could be a valuable target of disease control. Collectively, we identified a laccase critical to the development and virulence of the broad-host-range pathogen S. sclerotiorum and propose a potentially novel role for fungal laccases in modulating environmental sensing.
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spelling doaj.art-addf0b3200a1415892c62ffbc8553dee2024-03-24T12:29:25ZengNature PortfolioCommunications Biology2399-36422024-03-017111110.1038/s42003-024-06034-7A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogenNathaniel M. Westrick0Eddie G. Dominguez1Madeline Bondy2Christina M. Hull3Damon L. Smith4Mehdi Kabbage5Valley Laboratory, Connecticut Agricultural Experiment StationDepartment of Biomolecular Chemistry, University of Wisconsin-Madison, School of Medicine and Public HealthDepartment of Plant Pathology, University of Wisconsin-MadisonDepartment of Biomolecular Chemistry, University of Wisconsin-Madison, School of Medicine and Public HealthDepartment of Plant Pathology, University of Wisconsin-MadisonDepartment of Plant Pathology, University of Wisconsin-MadisonAbstract Secreted laccases are important enzymes on a broad ecological scale for their role in mediating plant-microbe interactions, but within ascomycete fungi these enzymes have been primarily associated with melanin biosynthesis. In this study, a putatively secreted laccase, Sslac2, was characterized from the broad-host-range plant pathogen Sclerotinia sclerotiorum, which is largely unpigmented and is not dependent on melanogenesis for plant infection. Gene knockouts of Sslac2 demonstrate wide ranging developmental phenotypes and are functionally non-pathogenic. These mutants also displayed indiscriminate growth behaviors and enhanced biomass formation, seemingly as a result of their inability to respond to canonical environmental growth cues, a phenomenon further confirmed through chemical stress, physiological, and transcriptomic analyses. Transmission and scanning electron microscopy demonstrate apparent differences in extracellular matrix structure between WT and mutant strains that likely explain the inability of the mutants to respond to their environment. Targeting Sslac2 using host-induced gene silencing significantly improved resistance to S. sclerotiorum, suggesting that fungal laccases could be a valuable target of disease control. Collectively, we identified a laccase critical to the development and virulence of the broad-host-range pathogen S. sclerotiorum and propose a potentially novel role for fungal laccases in modulating environmental sensing.https://doi.org/10.1038/s42003-024-06034-7
spellingShingle Nathaniel M. Westrick
Eddie G. Dominguez
Madeline Bondy
Christina M. Hull
Damon L. Smith
Mehdi Kabbage
A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
Communications Biology
title A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
title_full A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
title_fullStr A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
title_full_unstemmed A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
title_short A single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
title_sort single laccase acts as a key component of environmental sensing in a broad host range fungal pathogen
url https://doi.org/10.1038/s42003-024-06034-7
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