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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 Lab. (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. 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., 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. doi: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 = {2019},
month = {11}
}

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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


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


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


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

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


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


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

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


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

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


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


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

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

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


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

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


Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger
journal, November 1988

  • Bos, C. J.; Debets, A. J. M.; Swart, K.
  • Current Genetics, Vol. 14, Issue 5
  • DOI: 10.1007/BF00521266

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


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

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


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


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


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

    Works referencing / citing this record:

    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

    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

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


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


    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

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


    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

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


    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

    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


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


    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

    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

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


    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


    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

    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