A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.

In the plant pathogenic ascomycete Fusarium fujikuroi the synthesis of several economically important secondary metabolites (SM) depends on the nitrogen status of the cells. Of these SMs, gibberellin and bikaverin synthesis is subject to nitrogen catabolite repression (NCR) and is therefore only exe...

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Main Authors: Dominik Wagner, Philipp Wiemann, Kathleen Huß, Ulrike Brandt, André Fleißner, Bettina Tudzynski
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3829961?pdf=render
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spelling doaj-c7485e20927b4918adcb283201e98dcf2020-11-25T01:34:56ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-01811e8074010.1371/journal.pone.0080740A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.Dominik WagnerPhilipp WiemannKathleen HußUlrike BrandtAndré FleißnerBettina TudzynskiIn the plant pathogenic ascomycete Fusarium fujikuroi the synthesis of several economically important secondary metabolites (SM) depends on the nitrogen status of the cells. Of these SMs, gibberellin and bikaverin synthesis is subject to nitrogen catabolite repression (NCR) and is therefore only executed under nitrogen starvation conditions. How the signal of available nitrogen quantity and quality is sensed and transmitted to transcription factors is largely unknown. Earlier work revealed an essential regulatory role of the glutamine synthetase (GS) in the nitrogen regulation network and secondary metabolism as its deletion resulted in total loss of SM gene expression. Here we present extensive gene regulation studies of the wild type, the Δgln1 mutant and complementation strains of the gln1 deletion mutant expressing heterologous GS-encoding genes of prokaryotic and eukaryotic origin or 14 different F. fujikuroi gln1 copies with site-directed mutations. All strains were grown under different nitrogen conditions and characterized regarding growth, expression of NCR-responsive genes and biosynthesis of SM. We provide evidence for distinct roles of the GS in sensing and transducing the signals to NCR-responsive genes. Three site directed mutations partially restored secondary metabolism and GS-dependent gene expression, but not glutamine formation, demonstrating for the first time that the catalytic and regulatory roles of GS can be separated. The distinct mutant phenotypes show that the GS (1) participates in NH4 (+)-sensing and transducing the signal towards NCR-responsive transcription factors and their subsequent target genes; (2) affects carbon catabolism and (3) activates the expression of a distinct set of non-NCR GS-dependent genes. These novel insights into the regulatory role of the GS provide fascinating perspectives for elucidating regulatory roles of GS proteins of different organism in general.http://europepmc.org/articles/PMC3829961?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Dominik Wagner
Philipp Wiemann
Kathleen Huß
Ulrike Brandt
André Fleißner
Bettina Tudzynski
spellingShingle Dominik Wagner
Philipp Wiemann
Kathleen Huß
Ulrike Brandt
André Fleißner
Bettina Tudzynski
A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.
PLoS ONE
author_facet Dominik Wagner
Philipp Wiemann
Kathleen Huß
Ulrike Brandt
André Fleißner
Bettina Tudzynski
author_sort Dominik Wagner
title A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.
title_short A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.
title_full A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.
title_fullStr A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.
title_full_unstemmed A sensing role of the glutamine synthetase in the nitrogen regulation network in Fusarium fujikuroi.
title_sort sensing role of the glutamine synthetase in the nitrogen regulation network in fusarium fujikuroi.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description In the plant pathogenic ascomycete Fusarium fujikuroi the synthesis of several economically important secondary metabolites (SM) depends on the nitrogen status of the cells. Of these SMs, gibberellin and bikaverin synthesis is subject to nitrogen catabolite repression (NCR) and is therefore only executed under nitrogen starvation conditions. How the signal of available nitrogen quantity and quality is sensed and transmitted to transcription factors is largely unknown. Earlier work revealed an essential regulatory role of the glutamine synthetase (GS) in the nitrogen regulation network and secondary metabolism as its deletion resulted in total loss of SM gene expression. Here we present extensive gene regulation studies of the wild type, the Δgln1 mutant and complementation strains of the gln1 deletion mutant expressing heterologous GS-encoding genes of prokaryotic and eukaryotic origin or 14 different F. fujikuroi gln1 copies with site-directed mutations. All strains were grown under different nitrogen conditions and characterized regarding growth, expression of NCR-responsive genes and biosynthesis of SM. We provide evidence for distinct roles of the GS in sensing and transducing the signals to NCR-responsive genes. Three site directed mutations partially restored secondary metabolism and GS-dependent gene expression, but not glutamine formation, demonstrating for the first time that the catalytic and regulatory roles of GS can be separated. The distinct mutant phenotypes show that the GS (1) participates in NH4 (+)-sensing and transducing the signal towards NCR-responsive transcription factors and their subsequent target genes; (2) affects carbon catabolism and (3) activates the expression of a distinct set of non-NCR GS-dependent genes. These novel insights into the regulatory role of the GS provide fascinating perspectives for elucidating regulatory roles of GS proteins of different organism in general.
url http://europepmc.org/articles/PMC3829961?pdf=render
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