Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions

Pseudomonas fuscovaginae is the most prominent bacterial sheath rot pathogen, causing sheath brown rot disease in rice. This disease occurs worldwide and it is characterized by typical necrotic lesions on the sheath, as well as a reduction in the number of emitted panicles and filled grains. P. fusc...

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Main Authors: Enrico Ferrarini, Mihael Špacapan, Van Bach Lam, Andrea McCann, Catherine Cesa-Luna, Bishnu Prasad Marahatta, Edwin De Pauw, René De Mot, Vittorio Venturi, Monica Höfte
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1008980/full
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author Enrico Ferrarini
Mihael Špacapan
Van Bach Lam
Andrea McCann
Catherine Cesa-Luna
Bishnu Prasad Marahatta
Edwin De Pauw
René De Mot
Vittorio Venturi
Monica Höfte
author_facet Enrico Ferrarini
Mihael Špacapan
Van Bach Lam
Andrea McCann
Catherine Cesa-Luna
Bishnu Prasad Marahatta
Edwin De Pauw
René De Mot
Vittorio Venturi
Monica Höfte
author_sort Enrico Ferrarini
collection DOAJ
description Pseudomonas fuscovaginae is the most prominent bacterial sheath rot pathogen, causing sheath brown rot disease in rice. This disease occurs worldwide and it is characterized by typical necrotic lesions on the sheath, as well as a reduction in the number of emitted panicles and filled grains. P. fuscovaginae has been shown to produce syringotoxin and fuscopeptin cyclic lipopeptides (CLPs), which have been linked to pathogenicity. In this study, we investigated the role of P. fuscovaginae UPB0736 CLPs in plant pathogenicity, antifungal activity and swarming motility. To do so, we sequenced the strain to obtain a single-contig genome and we constructed deletion mutants in the biosynthetic gene clusters responsible for the synthesis of CLPs. We show that UPB0736 produces a third CLP of 13 amino acids, now named asplenin, and we link this CLP with the swarming activity of the strain. We could then show that syringotoxin is particularly active against Rhizoctonia solani in vitro. By testing the mutants in planta we investigated the role of both fuscopeptin and syringotoxin in causing sheath rot lesions. We proved that the presence of these two CLPs considerably affected the number of emitted panicles, although their number was still significantly affected in the mutants deficient in both fuscopeptin and syringotoxin. These results reveal the importance of CLPs in P. fuscovaginae pathogenicity, but also suggest that other pathogenicity factors may be involved.
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spelling doaj.art-a3a8ec3b2a074dcaa98bb7c212d200122022-12-22T02:29:02ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.10089801008980Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactionsEnrico Ferrarini0Mihael Špacapan1Van Bach Lam2Andrea McCann3Catherine Cesa-Luna4Bishnu Prasad Marahatta5Edwin De Pauw6René De Mot7Vittorio Venturi8Monica Höfte9Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, BelgiumInternational Centre for Genetic Engineering and Biotechnology (ICGEB), Trieste, ItalyDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, BelgiumDepartment of Chemistry, Faculty of Sciences, University of Liège, Liège, BelgiumCentre of Microbial and Plant Genetics, Faculty of Bioscience Engineering, KU Leuven, Leuven, BelgiumDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, BelgiumDepartment of Chemistry, Faculty of Sciences, University of Liège, Liège, BelgiumCentre of Microbial and Plant Genetics, Faculty of Bioscience Engineering, KU Leuven, Leuven, BelgiumInternational Centre for Genetic Engineering and Biotechnology (ICGEB), Trieste, ItalyDepartment of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, BelgiumPseudomonas fuscovaginae is the most prominent bacterial sheath rot pathogen, causing sheath brown rot disease in rice. This disease occurs worldwide and it is characterized by typical necrotic lesions on the sheath, as well as a reduction in the number of emitted panicles and filled grains. P. fuscovaginae has been shown to produce syringotoxin and fuscopeptin cyclic lipopeptides (CLPs), which have been linked to pathogenicity. In this study, we investigated the role of P. fuscovaginae UPB0736 CLPs in plant pathogenicity, antifungal activity and swarming motility. To do so, we sequenced the strain to obtain a single-contig genome and we constructed deletion mutants in the biosynthetic gene clusters responsible for the synthesis of CLPs. We show that UPB0736 produces a third CLP of 13 amino acids, now named asplenin, and we link this CLP with the swarming activity of the strain. We could then show that syringotoxin is particularly active against Rhizoctonia solani in vitro. By testing the mutants in planta we investigated the role of both fuscopeptin and syringotoxin in causing sheath rot lesions. We proved that the presence of these two CLPs considerably affected the number of emitted panicles, although their number was still significantly affected in the mutants deficient in both fuscopeptin and syringotoxin. These results reveal the importance of CLPs in P. fuscovaginae pathogenicity, but also suggest that other pathogenicity factors may be involved.https://www.frontiersin.org/articles/10.3389/fpls.2022.1008980/fullbacterial sheath brown rotfuscopeptinsyringotoxinasplenincyclic lipopeptidesrice
spellingShingle Enrico Ferrarini
Mihael Špacapan
Van Bach Lam
Andrea McCann
Catherine Cesa-Luna
Bishnu Prasad Marahatta
Edwin De Pauw
René De Mot
Vittorio Venturi
Monica Höfte
Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
Frontiers in Plant Science
bacterial sheath brown rot
fuscopeptin
syringotoxin
asplenin
cyclic lipopeptides
rice
title Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
title_full Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
title_fullStr Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
title_full_unstemmed Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
title_short Versatile role of Pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
title_sort versatile role of pseudomonas fuscovaginae cyclic lipopeptides in plant and microbial interactions
topic bacterial sheath brown rot
fuscopeptin
syringotoxin
asplenin
cyclic lipopeptides
rice
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1008980/full
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