A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger

Understanding the genetic, molecular and evolutionary basis of cysteine-stabilized antifungal proteins (AFPs) from fungi is important for understanding whether their function is mainly defensive or associated with fungal growth and development. In the current study, a transcriptome meta-analysis of...

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Main Authors: Paege, Norman, Jung, Sascha, Schäpe, Paul, Müller-Hagen, Dirk, Ouedraogo, Jean-Paul, Heiderich, Caroline, Jedamzick, Johanna, Nitsche, Benjamin M., van den Hondel, Cees A., Ram, Arthur F., Meyer, Vera
Format: Online
Language:English
Published: Public Library of Science 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5106034/
id pubmed-5106034
recordtype oai_dc
spelling pubmed-51060342016-12-08 A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger Paege, Norman Jung, Sascha Schäpe, Paul Müller-Hagen, Dirk Ouedraogo, Jean-Paul Heiderich, Caroline Jedamzick, Johanna Nitsche, Benjamin M. van den Hondel, Cees A. Ram, Arthur F. Meyer, Vera Research Article Understanding the genetic, molecular and evolutionary basis of cysteine-stabilized antifungal proteins (AFPs) from fungi is important for understanding whether their function is mainly defensive or associated with fungal growth and development. In the current study, a transcriptome meta-analysis of the Aspergillus niger γ-core protein AnAFP was performed to explore co-expressed genes and pathways, based on independent expression profiling microarrays covering 155 distinct cultivation conditions. This analysis uncovered that anafp displays a highly coordinated temporal and spatial transcriptional profile which is concomitant with key nutritional and developmental processes. Its expression profile coincides with early starvation response and parallels with genes involved in nutrient mobilization and autophagy. Using fluorescence- and luciferase reporter strains we demonstrated that the anafp promoter is active in highly vacuolated compartments and foraging hyphal cells during carbon starvation with CreA and FlbA, but not BrlA, as most likely regulators of anafp. A co-expression network analysis supported by luciferase-based reporter assays uncovered that anafp expression is embedded in several cellular processes including allorecognition, osmotic and oxidative stress survival, development, secondary metabolism and autophagy, and predicted StuA and VelC as additional regulators. The transcriptomic resources available for A. niger provide unparalleled resources to investigate the function of proteins. Our work illustrates how transcriptomic meta-analyses can lead to hypotheses regarding protein function and predict a role for AnAFP during slow growth, allorecognition, asexual development and nutrient recycling of A. niger and propose that it interacts with the autophagic machinery to enable these processes. Public Library of Science 2016-11-11 /pmc/articles/PMC5106034/ /pubmed/27835655 http://dx.doi.org/10.1371/journal.pone.0165755 Text en © 2016 Paege et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Paege, Norman
Jung, Sascha
Schäpe, Paul
Müller-Hagen, Dirk
Ouedraogo, Jean-Paul
Heiderich, Caroline
Jedamzick, Johanna
Nitsche, Benjamin M.
van den Hondel, Cees A.
Ram, Arthur F.
Meyer, Vera
spellingShingle Paege, Norman
Jung, Sascha
Schäpe, Paul
Müller-Hagen, Dirk
Ouedraogo, Jean-Paul
Heiderich, Caroline
Jedamzick, Johanna
Nitsche, Benjamin M.
van den Hondel, Cees A.
Ram, Arthur F.
Meyer, Vera
A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger
author_facet Paege, Norman
Jung, Sascha
Schäpe, Paul
Müller-Hagen, Dirk
Ouedraogo, Jean-Paul
Heiderich, Caroline
Jedamzick, Johanna
Nitsche, Benjamin M.
van den Hondel, Cees A.
Ram, Arthur F.
Meyer, Vera
author_sort Paege, Norman
title A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger
title_short A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger
title_full A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger
title_fullStr A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger
title_full_unstemmed A Transcriptome Meta-Analysis Proposes Novel Biological Roles for the Antifungal Protein AnAFP in Aspergillus niger
title_sort transcriptome meta-analysis proposes novel biological roles for the antifungal protein anafp in aspergillus niger
description Understanding the genetic, molecular and evolutionary basis of cysteine-stabilized antifungal proteins (AFPs) from fungi is important for understanding whether their function is mainly defensive or associated with fungal growth and development. In the current study, a transcriptome meta-analysis of the Aspergillus niger γ-core protein AnAFP was performed to explore co-expressed genes and pathways, based on independent expression profiling microarrays covering 155 distinct cultivation conditions. This analysis uncovered that anafp displays a highly coordinated temporal and spatial transcriptional profile which is concomitant with key nutritional and developmental processes. Its expression profile coincides with early starvation response and parallels with genes involved in nutrient mobilization and autophagy. Using fluorescence- and luciferase reporter strains we demonstrated that the anafp promoter is active in highly vacuolated compartments and foraging hyphal cells during carbon starvation with CreA and FlbA, but not BrlA, as most likely regulators of anafp. A co-expression network analysis supported by luciferase-based reporter assays uncovered that anafp expression is embedded in several cellular processes including allorecognition, osmotic and oxidative stress survival, development, secondary metabolism and autophagy, and predicted StuA and VelC as additional regulators. The transcriptomic resources available for A. niger provide unparalleled resources to investigate the function of proteins. Our work illustrates how transcriptomic meta-analyses can lead to hypotheses regarding protein function and predict a role for AnAFP during slow growth, allorecognition, asexual development and nutrient recycling of A. niger and propose that it interacts with the autophagic machinery to enable these processes.
publisher Public Library of Science
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5106034/
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