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...
Main Authors: | , , , , , , , , , |
---|---|
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 |
_version_ | 1818470195554942976 |
---|---|
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. |
first_indexed | 2024-04-13T21:34:28Z |
format | Article |
id | doaj.art-a3a8ec3b2a074dcaa98bb7c212d20012 |
institution | Directory Open Access Journal |
issn | 1664-462X |
language | English |
last_indexed | 2024-04-13T21:34:28Z |
publishDate | 2022-11-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Plant Science |
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 |
work_keys_str_mv | AT enricoferrarini versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT mihaelspacapan versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT vanbachlam versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT andreamccann versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT catherinecesaluna versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT bishnuprasadmarahatta versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT edwindepauw versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT renedemot versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT vittorioventuri versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions AT monicahofte versatileroleofpseudomonasfuscovaginaecycliclipopeptidesinplantandmicrobialinteractions |