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Title: Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network

Abstract

BACKGROUND: Enzymatic plant biomass degradation by fungi is a highly complex process and one of the leading challenges in developing a biobased economy. Some industrial fungi (e.g. Aspergillus niger) have a long history of use with respect to plant biomass degradation and for that reason have become 'model' species for this topic. A. niger is a major industrial enzyme producer that has a broad ability to degrade plant based polysaccharides. A. niger wild-type, the (hemi-)cellulolytic regulator (xlnR) and xylulokinase (xkiA1) mutant strains were grown on a monocot (corn stover, CS) and dicot (soybean hulls, SBH) substrate. The xkiA1 mutant is unable to utilize the pentoses D-xylose and L-arabinose and the polysaccharide xylan, and was previously shown to accumulate inducers for the (hemi-)cellulolytic transcriptional activator XlnR and the arabinanolytic transcriptional activator AraR in the presence of pentoses, resulting in overexpression of their target genes. The xlnR mutant has reduced growth on xylan and down-regulation of its target genes. The mutants therefore have a similar phenotype on xylan, but an opposite transcriptional effect. D-xylose and L-arabinose are the most abundant monosaccharides after D-glucose in nearly all plant-derived biomass materials. In this study we evaluated the effect of the xlnR and xkiA1 mutationmore » during growth on two pentose-rich substrates by transcriptome analysis. RESULTS: Particular attention was given to CAZymes, metabolic pathways and transcription factors related to the plant biomass degradation. Genes coding for the main enzymes involved in plant biomass degradation were down-regulated at the beginning of the growth on CS and SBH. However, at a later time point, significant differences were found in the expression profiles of both mutants on CS compared to SBH. CONCLUSION: This study demonstrates the high complexity of the plant biomass degradation process by fungi, by showing that mutant strains with fairly straightforward phenotypes on pure mono- and polysaccharides, have much less clear-cut phenotypes and transcriptomes on crude plant biomass.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [2];  [2];  [2];  [3]; ORCiD logo [1]
  1. Utrecht Univ. (The Netherlands)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1591830
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; transcriptomics; Aspergillus Niger; XlnR; XkiA; gene expression

Citation Formats

Khosravi, Claire, Kowalczyk, Joanna E., Chroumpi, Tania, Battaglia, Evy, Aguilar Pontes, Maria-Victoria, Peng, Mao, Wiebenga, Ad, Ng, Vivian, Lipzen, Anna, He, Guifen, Bauer, Diane, Grigoriev, Igor V., and de Vries, Ronald P. Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network. United States: N. p., 2019. Web. doi:10.1186/s12864-019-6235-7.
Khosravi, Claire, Kowalczyk, Joanna E., Chroumpi, Tania, Battaglia, Evy, Aguilar Pontes, Maria-Victoria, Peng, Mao, Wiebenga, Ad, Ng, Vivian, Lipzen, Anna, He, Guifen, Bauer, Diane, Grigoriev, Igor V., & de Vries, Ronald P. Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network. United States. https://doi.org/10.1186/s12864-019-6235-7
Khosravi, Claire, Kowalczyk, Joanna E., Chroumpi, Tania, Battaglia, Evy, Aguilar Pontes, Maria-Victoria, Peng, Mao, Wiebenga, Ad, Ng, Vivian, Lipzen, Anna, He, Guifen, Bauer, Diane, Grigoriev, Igor V., and de Vries, Ronald P. Thu . "Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network". United States. https://doi.org/10.1186/s12864-019-6235-7. https://www.osti.gov/servlets/purl/1591830.
@article{osti_1591830,
title = {Transcriptome analysis of Aspergillus niger xlnR and xkiA mutants grown on corn Stover and soybean hulls reveals a highly complex regulatory network},
author = {Khosravi, Claire and Kowalczyk, Joanna E. and Chroumpi, Tania and Battaglia, Evy and Aguilar Pontes, Maria-Victoria and Peng, Mao and Wiebenga, Ad and Ng, Vivian and Lipzen, Anna and He, Guifen and Bauer, Diane and Grigoriev, Igor V. and de Vries, Ronald P.},
abstractNote = {BACKGROUND: Enzymatic plant biomass degradation by fungi is a highly complex process and one of the leading challenges in developing a biobased economy. Some industrial fungi (e.g. Aspergillus niger) have a long history of use with respect to plant biomass degradation and for that reason have become 'model' species for this topic. A. niger is a major industrial enzyme producer that has a broad ability to degrade plant based polysaccharides. A. niger wild-type, the (hemi-)cellulolytic regulator (xlnR) and xylulokinase (xkiA1) mutant strains were grown on a monocot (corn stover, CS) and dicot (soybean hulls, SBH) substrate. The xkiA1 mutant is unable to utilize the pentoses D-xylose and L-arabinose and the polysaccharide xylan, and was previously shown to accumulate inducers for the (hemi-)cellulolytic transcriptional activator XlnR and the arabinanolytic transcriptional activator AraR in the presence of pentoses, resulting in overexpression of their target genes. The xlnR mutant has reduced growth on xylan and down-regulation of its target genes. The mutants therefore have a similar phenotype on xylan, but an opposite transcriptional effect. D-xylose and L-arabinose are the most abundant monosaccharides after D-glucose in nearly all plant-derived biomass materials. In this study we evaluated the effect of the xlnR and xkiA1 mutation during growth on two pentose-rich substrates by transcriptome analysis. RESULTS: Particular attention was given to CAZymes, metabolic pathways and transcription factors related to the plant biomass degradation. Genes coding for the main enzymes involved in plant biomass degradation were down-regulated at the beginning of the growth on CS and SBH. However, at a later time point, significant differences were found in the expression profiles of both mutants on CS compared to SBH. CONCLUSION: This study demonstrates the high complexity of the plant biomass degradation process by fungi, by showing that mutant strains with fairly straightforward phenotypes on pure mono- and polysaccharides, have much less clear-cut phenotypes and transcriptomes on crude plant biomass.},
doi = {10.1186/s12864-019-6235-7},
journal = {BMC Genomics},
number = 1,
volume = 20,
place = {United States},
year = {Thu Nov 14 00:00:00 EST 2019},
month = {Thu Nov 14 00:00:00 EST 2019}
}

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Works referenced in this record:

Genetic Interaction of Aspergillus nidulans galR, xlnR and araR in Regulating D-Galactose and L-Arabinose Release and Catabolism Gene Expression
journal, November 2015


ggplot2
book, January 2009


CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation
journal, May 1999


Deletion of either the regulatory gene ara1 or metabolic gene xki1 in Trichoderma reesei leads to increased CAZyme gene expression on crude plant biomass
journal, April 2019

  • Benocci, Tiziano; Aguilar-Pontes, Maria Victoria; Kun, Roland Sándor
  • Biotechnology for Biofuels, Vol. 12, Issue 1
  • DOI: 10.1186/s13068-019-1422-y

Corn Stover Fractions and Bioenergy
journal, January 2006

  • Akin, Danny E.; Morrison, W. Herbert; Rigsby, Luanne L.
  • Applied Biochemistry and Biotechnology, Vol. 129, Issue 1-3
  • DOI: 10.1385/ABAB:129:1:104

Pectin, a versatile polysaccharide present in plant cell walls
journal, March 2009

  • Voragen, Alphons G. J.; Coenen, Gerd-Jan; Verhoef, René P.
  • Structural Chemistry, Vol. 20, Issue 2
  • DOI: 10.1007/s11224-009-9442-z

Molecular Cloning and Characterization of a Transcriptional Activator Gene, amyR , Involved in the Amylolytic Gene Expression in Aspergillus oryzae
journal, January 2000

  • Gomi, Katsuya; Akeno, Terumi; Minetoki, Toshitaka
  • Bioscience, Biotechnology, and Biochemistry, Vol. 64, Issue 4
  • DOI: 10.1271/bbb.64.816

Isolation and characterization of two xylitol dehydrogenases from Aspergillus niger
journal, July 1994


Regulation of the α-glucuronidase-encoding gene ( aguA ) from Aspergillus niger
journal, September 2002

  • Vries, R. de; Vondervoort, P. van de; L., Hendriks
  • Molecular Genetics and Genomics, Vol. 268, Issue 1
  • DOI: 10.1007/s00438-002-0729-7

Thermo-mechanical extrusion pretreatment for conversion of soybean hulls to fermentable sugars
journal, August 2011


Improved Hemicellulase Production by Genetic Modification of Carbon Catabolite Repression and Xylanolitic Activation in Aspergillus niger
journal, March 2018


FactoMineR : An R Package for Multivariate Analysis
journal, January 2008

  • Lê, Sébastien; Josse, Julie; Husson, François
  • Journal of Statistical Software, Vol. 25, Issue 1
  • DOI: 10.18637/jss.v025.i01

featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013


Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
journal, January 2002


Regulation of pentose utilisation by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger
journal, April 2011

  • Battaglia, Evy; Hansen, Sara Fasmer; Leendertse, Anne
  • Applied Microbiology and Biotechnology, Vol. 91, Issue 2
  • DOI: 10.1007/s00253-011-3242-2

The transcriptional activator GaaR of Aspergillus niger is required for release and utilization of d- galacturonic acid from pectin
journal, May 2016


In vivo functional analysis of L-rhamnose metabolic pathway in Aspergillus niger: a tool to identify the potential inducer of RhaR
journal, November 2017


EglC, a New Endoglucanase from Aspergillus niger with Major Activity towards Xyloglucan
journal, April 2002


Hydrolysis Characteristics of Tissue Fractions Resulting From Mechanical Separation of Corn Stover
journal, January 2005

  • Bootsma, Jason A.; Shanks, Brent H.
  • Applied Biochemistry and Biotechnology, Vol. 125, Issue 1
  • DOI: 10.1385/ABAB:125:1:027

Uncovering the Genome-Wide Transcriptional Responses of the Filamentous Fungus Aspergillus niger to Lignocellulose Using RNA Sequencing
journal, August 2012


Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse
journal, January 2011

  • de Souza, Wagner R.; de Gouvea, Paula F.; Savoldi, Marcela
  • Biotechnology for Biofuels, Vol. 4, Issue 1
  • DOI: 10.1186/1754-6834-4-40

Identification of a Novel L-rhamnose Uptake Transporter in the Filamentous Fungus Aspergillus niger
journal, December 2016


Isolation and characterization of two specific regulatory Aspergillus niger mutants shows antagonistic regulation of arabinan and xylan metabolism
journal, May 2003

  • de Groot, Marco J. L.; van de Vondervoort, Peter J. I.; de Vries, Ronald P.
  • Microbiology, Vol. 149, Issue 5
  • DOI: 10.1099/mic.0.25993-0

Analysis of regulation of pentose utilisation in Aspergillus niger reveals evolutionary adaptations in Eurotiales
journal, June 2011


The roles of the zinc finger transcription factors XlnR, ClrA and ClrB in the breakdown of lignocellulose by Aspergillus niger
journal, January 2016


Aspergillus Enzymes Involved in Degradation of Plant Cell Wall Polysaccharides
journal, December 2001


A new transcriptional activator for amylase genes in Aspergillus
journal, December 1999

  • Petersen, K. L.; Lehmbeck, J.; Christensen, T.
  • Molecular and General Genetics MGG, Vol. 262, Issue 4-5
  • DOI: 10.1007/s004380051129

Effect of anatomical fractionation on the enzymatic hydrolysis of acid and alkaline pretreated corn stover
journal, November 2009


Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi
journal, April 2012

  • Coradetti, S. T.; Craig, J. P.; Xiong, Y.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
  • DOI: 10.1073/pnas.1200785109

Widespread adenine N6-methylation of active genes in fungi
journal, May 2017

  • Mondo, Stephen J.; Dannebaum, Richard O.; Kuo, Rita C.
  • Nature Genetics, Vol. 49, Issue 6
  • DOI: 10.1038/ng.3859

The influence of Aspergillus niger transcription factors AraR and XlnR in the gene expression during growth in d-xylose, l-arabinose and steam-exploded sugarcane bagasse
journal, November 2013

  • de Souza, Wagner Rodrigo; Maitan-Alfenas, Gabriela Piccolo; de Gouvêa, Paula Fagundes
  • Fungal Genetics and Biology, Vol. 60
  • DOI: 10.1016/j.fgb.2013.07.007

A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production
journal, July 2004


Isolation and analysis of xln R, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger
journal, January 1998


HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


The transcriptional activators AraR and XlnR from Aspergillus niger regulate expression of pentose catabolic and pentose phosphate pathway genes
journal, September 2014


Differential Expression of Three α-Galactosidase Genes and a Single β-Galactosidase Gene from Aspergillus niger
journal, June 1999

  • de Vries, Ronald P.; van den Broeck, Hetty C.; Dekkers, Ester
  • Applied and Environmental Microbiology, Vol. 65, Issue 6
  • DOI: 10.1128/AEM.65.6.2453-2460.1999

Regulation of the Feruloyl Esterase ( faeA ) Gene from Aspergillus niger
journal, December 1999


The Transcriptional Activator XlnR Regulates Both Xylanolytic and Endoglucanase Gene Expression inAspergillus niger
journal, October 1998

  • van Peij, Noël N. M. E.; Gielkens, Marco M. C.; de Vries, Ronald P.
  • Applied and Environmental Microbiology, Vol. 64, Issue 10
  • DOI: 10.1128/AEM.64.10.3615-3619.1998

Two Cellobiohydrolase-Encoding Genes from Aspergillus niger Require d-Xylose and the Xylanolytic Transcriptional Activator XlnR for Their Expression
journal, January 1999


ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages
journal, June 2020


Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021


Investigation of the role of typhoid toxin in acute typhoid fever in a human challenge model
text, January 2019

  • Gibani, Malick M.; Jones, Elizabeth; Barton, Amber
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.54588

The transcriptional activator GaaR of Aspergillus niger is required for release and utilization of d- galacturonic acid from pectin
journal, May 2016


Regulation of pentose utilisation by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger
journal, April 2011

  • Battaglia, Evy; Hansen, Sara Fasmer; Leendertse, Anne
  • Applied Microbiology and Biotechnology, Vol. 91, Issue 2
  • DOI: 10.1007/s00253-011-3242-2

Aspergillus niger RhaR, a regulator involved in l-rhamnose release and catabolism
journal, February 2014


Regulation of the α-glucuronidase-encoding gene ( aguA ) from Aspergillus niger
journal, September 2002

  • Vries, R. de; Vondervoort, P. van de; L., Hendriks
  • Molecular Genetics and Genomics, Vol. 268, Issue 1
  • DOI: 10.1007/s00438-002-0729-7

A new transcriptional activator for amylase genes in Aspergillus
journal, December 1999

  • Petersen, K. L.; Lehmbeck, J.; Christensen, T.
  • Molecular and General Genetics MGG, Vol. 262, Issue 4-5
  • DOI: 10.1007/s004380051129

Pectin, a versatile polysaccharide present in plant cell walls
journal, March 2009

  • Voragen, Alphons G. J.; Coenen, Gerd-Jan; Verhoef, René P.
  • Structural Chemistry, Vol. 20, Issue 2
  • DOI: 10.1007/s11224-009-9442-z

Thermo-mechanical extrusion pretreatment for conversion of soybean hulls to fermentable sugars
journal, August 2011


The transcriptional activators AraR and XlnR from Aspergillus niger regulate expression of pentose catabolic and pentose phosphate pathway genes
journal, September 2014


Synergy between enzymes from Aspergillus involved in the degradation of plant cell wall polysaccharides
journal, August 2000


Widespread adenine N6-methylation of active genes in fungi
journal, May 2017

  • Mondo, Stephen J.; Dannebaum, Richard O.; Kuo, Rita C.
  • Nature Genetics, Vol. 49, Issue 6
  • DOI: 10.1038/ng.3859

HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

Synergism between IL7R and CXCR4 drives BCR-ABL induced transformation in Philadelphia chromosome-positive acute lymphoblastic leukemia
journal, June 2020


IL-1-dependent enteric gliosis guides intestinal inflammation and dysmotility and modulates macrophage function
journal, August 2022


Isolation and analysis of xln R, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger
journal, January 1998


L-Arabinose and D-Xylose Catabolism in Aspergillus niger
journal, August 1989


Isolation and characterization of two xylitol dehydrogenases from Aspergillus niger
journal, July 1994


d-Xylose Concentration-Dependent Hydrolase Expression Profiles and the Function of CreA and XlnR in Aspergillus niger
journal, February 2012

  • Mach-Aigner, Astrid R.; Omony, Jimmy; Jovanovic, Birgit
  • Applied and Environmental Microbiology, Vol. 78, Issue 9
  • DOI: 10.1128/aem.07772-11

Transcriptome analysis of Aspergillus niger grown on sugarcane bagasse
journal, January 2011

  • de Souza, Wagner R.; de Gouvea, Paula F.; Savoldi, Marcela
  • Biotechnology for Biofuels, Vol. 4, Issue 1
  • DOI: 10.1186/1754-6834-4-40

In vivo functional analysis of L-rhamnose metabolic pathway in Aspergillus niger: a tool to identify the potential inducer of RhaR
journal, November 2017


Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Deletion of either the regulatory gene ara1 or metabolic gene xki1 in Trichoderma reesei leads to increased CAZyme gene expression on crude plant biomass
journal, April 2019

  • Benocci, Tiziano; Aguilar-Pontes, Maria Victoria; Kun, Roland Sándor
  • Biotechnology for Biofuels, Vol. 12, Issue 1
  • DOI: 10.1186/s13068-019-1422-y

Molecular Cloning and Characterization of a Transcriptional Activator Gene, amyR , Involved in the Amylolytic Gene Expression in Aspergillus oryzae
journal, January 2000

  • Gomi, Katsuya; Akeno, Terumi; Minetoki, Toshitaka
  • Bioscience, Biotechnology, and Biochemistry, Vol. 64, Issue 4
  • DOI: 10.1271/bbb.64.816

Uncovering the Genome-Wide Transcriptional Responses of the Filamentous Fungus Aspergillus niger to Lignocellulose Using RNA Sequencing
journal, August 2012


Identification of a Novel L-rhamnose Uptake Transporter in the Filamentous Fungus Aspergillus niger
journal, December 2016


Genetic Interaction of Aspergillus nidulans galR, xlnR and araR in Regulating D-Galactose and L-Arabinose Release and Catabolism Gene Expression
journal, November 2015


Improved Hemicellulase Production by Genetic Modification of Carbon Catabolite Repression and Xylanolitic Activation in Aspergillus niger
journal, March 2018


Analysis of regulation of pentose utilisation in Aspergillus niger reveals evolutionary adaptations in Eurotiales
journal, June 2011