An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.

We have identified from the mutualistic grass endophyte Epichloë festucae a non-ribosomal peptide synthetase gene (sidN) encoding a siderophore synthetase. The enzymatic product of SidN is shown to be a novel extracellular siderophore designated as epichloënin A, related to ferrirubin from the ferri...

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Published in:PLoS Pathogens
Main Authors: Linda J Johnson, Albert Koulman, Michael Christensen, Geoffrey A Lane, Karl Fraser, Natasha Forester, Richard D Johnson, Gregory T Bryan, Susanne Rasmussen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1003332&type=printable
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author Linda J Johnson
Albert Koulman
Michael Christensen
Geoffrey A Lane
Karl Fraser
Natasha Forester
Richard D Johnson
Gregory T Bryan
Susanne Rasmussen
author_facet Linda J Johnson
Albert Koulman
Michael Christensen
Geoffrey A Lane
Karl Fraser
Natasha Forester
Richard D Johnson
Gregory T Bryan
Susanne Rasmussen
author_sort Linda J Johnson
collection DOAJ
container_title PLoS Pathogens
description We have identified from the mutualistic grass endophyte Epichloë festucae a non-ribosomal peptide synthetase gene (sidN) encoding a siderophore synthetase. The enzymatic product of SidN is shown to be a novel extracellular siderophore designated as epichloënin A, related to ferrirubin from the ferrichrome family. Targeted gene disruption of sidN eliminated biosynthesis of epichloënin A in vitro and in planta. During iron-depleted axenic growth, ΔsidN mutants accumulated the pathway intermediate N(5)-trans-anhydromevalonyl-N(5)-hydroxyornithine (trans-AMHO), displayed sensitivity to oxidative stress and showed deficiencies in both polarized hyphal growth and sporulation. Infection of Lolium perenne (perennial ryegrass) with ΔsidN mutants resulted in perturbations of the endophyte-grass symbioses. Deviations from the characteristic tightly regulated synchronous growth of the fungus with its plant partner were observed and infected plants were stunted. Analysis of these plants by light and transmission electron microscopy revealed abnormalities in the distribution and localization of ΔsidN mutant hyphae as well as deformities in hyphal ultrastructure. We hypothesize that lack of epichloënin A alters iron homeostasis of the symbiotum, changing it from mutually beneficial to antagonistic. Iron itself or epichloënin A may serve as an important molecular/cellular signal for controlling fungal growth and hence the symbiotic interaction.
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spelling doaj-art-e4f613d9a0644aff808f01bdf1a5abc62025-08-20T03:25:03ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742013-01-0195e100333210.1371/journal.ppat.1003332An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.Linda J JohnsonAlbert KoulmanMichael ChristensenGeoffrey A LaneKarl FraserNatasha ForesterRichard D JohnsonGregory T BryanSusanne RasmussenWe have identified from the mutualistic grass endophyte Epichloë festucae a non-ribosomal peptide synthetase gene (sidN) encoding a siderophore synthetase. The enzymatic product of SidN is shown to be a novel extracellular siderophore designated as epichloënin A, related to ferrirubin from the ferrichrome family. Targeted gene disruption of sidN eliminated biosynthesis of epichloënin A in vitro and in planta. During iron-depleted axenic growth, ΔsidN mutants accumulated the pathway intermediate N(5)-trans-anhydromevalonyl-N(5)-hydroxyornithine (trans-AMHO), displayed sensitivity to oxidative stress and showed deficiencies in both polarized hyphal growth and sporulation. Infection of Lolium perenne (perennial ryegrass) with ΔsidN mutants resulted in perturbations of the endophyte-grass symbioses. Deviations from the characteristic tightly regulated synchronous growth of the fungus with its plant partner were observed and infected plants were stunted. Analysis of these plants by light and transmission electron microscopy revealed abnormalities in the distribution and localization of ΔsidN mutant hyphae as well as deformities in hyphal ultrastructure. We hypothesize that lack of epichloënin A alters iron homeostasis of the symbiotum, changing it from mutually beneficial to antagonistic. Iron itself or epichloënin A may serve as an important molecular/cellular signal for controlling fungal growth and hence the symbiotic interaction.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1003332&type=printable
spellingShingle Linda J Johnson
Albert Koulman
Michael Christensen
Geoffrey A Lane
Karl Fraser
Natasha Forester
Richard D Johnson
Gregory T Bryan
Susanne Rasmussen
An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.
title An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.
title_full An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.
title_fullStr An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.
title_full_unstemmed An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.
title_short An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne.
title_sort extracellular siderophore is required to maintain the mutualistic interaction of epichloe festucae with lolium perenne
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1003332&type=printable
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