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

Kowalczyk, Joanna E.; Gruben, Birgit S.; Battaglia, Evy; Wiebenga, Ad; Majoor, Eline; de Vries, Ronald P.

doi:10.1371/journal.pone.0143200

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

Journal Article · Wed Nov 18 00:00:00 EST 2015 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0143200· OSTI ID:1627773

Kowalczyk, Joanna E. ^[1]; Gruben, Birgit S. ^[2]; Battaglia, Evy ^[2]; Wiebenga, Ad ^[3]; Majoor, Eline ^[3]; de Vries, Ronald P. ^[3]

Univ. of Utrecht (Netherlands). CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology. Fungal Physiology; DOE/OSTI
Univ. of Utrecht (Netherlands). CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology. Fungal Physiology; Univ. of Utrecht (Netherlands). Microbiology
Univ. of Utrecht (Netherlands). CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology. Fungal Physiology

In Aspergillus nidulans, the xylanolytic regulator XlnR and the arabinanolytic regulator AraR co-regulate pentose catabolism. In nature, the pentose sugars D-xylose and L-arabinose are both main building blocks of the polysaccharide arabinoxylan. In pectin and arabinogalactan, these two monosaccharides are found in combination with D-galactose. GalR, the regulator that responds to the presence of D-galactose, regulates the D-galactose catabolic pathway. In this study we investigated the possible interaction between XlnR, AraR and GalR in pentose and/or D-galactose catabolism in A. nidulans. Growth phenotypes and metabolic gene expression profiles were studied in single, double and triple disruptant A. nidulans strains of the genes encoding these paralogous transcription factors. Our results demonstrate that AraR and XlnR not only control pentose catabolic pathway genes, but also genes of the oxido-reductive D-galactose catabolic pathway. This suggests an interaction between three transcriptional regulators in D-galactose catabolism. Conversely, GalR is not involved in regulation of pentose catabolism, but controls only genes of the oxidoreductive D-galactose catabolic pathway.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627773

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 11 Vol. 10; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (34)

Sybil: Methods and Software for Multiple Genome Comparison and Visualization Crabtree, Jonathan; Angiuoli, Samuel V.; Wortman, Jennifer R. Gene Function Analysis https://doi.org/10.1007/978-1-59745-547-3_6	book	January 2007
Regulation of formation of the intracellular β-gaiactosidase activity ofAspergillus nidulans Fekete, Erzsébet; Karaffa, Levente; Sándor, Erzsébet Archives of Microbiology, Vol. 179, Issue 1 https://doi.org/10.1007/s00203-002-0491-6	journal	January 2002
The alternative d-galactose degrading pathway of Aspergillus nidulans proceeds via l-sorbose Fekete, Erzs�bet; Karaffa, Levente; S�ndor, Erzs�bet Archives of Microbiology, Vol. 181, Issue 1 https://doi.org/10.1007/s00203-003-0622-8	journal	January 2004
The ‘true’ l -xylulose reductase of filamentous fungi identified in Aspergillus niger Mojzita, Dominik; Vuoristo, Kiira; Koivistoinen, Outi M. FEBS Letters, Vol. 584, Issue 16 https://doi.org/10.1016/j.febslet.2010.06.037	journal	July 2010
Sorbitol dehydrogenase of Aspergillus niger , SdhA, is part of the oxido-reductive d -galactose pathway and essential for d -sorbitol catabolism Koivistoinen, Outi M.; Richard, Peter; Penttilä, Merja FEBS Letters, Vol. 586, Issue 4 https://doi.org/10.1016/j.febslet.2012.01.004	journal	January 2012
GalX regulates the d -galactose oxido-reductive pathway in Aspergillus niger Gruben, Birgit S.; Zhou, Miaomiao; de Vries, Ronald P. FEBS Letters, Vol. 586, Issue 22 https://doi.org/10.1016/j.febslet.2012.09.029	journal	October 2012
Identification of the galactitol dehydrogenase, LadB, that is part of the oxido-reductive d-galactose catabolic pathway in Aspergillus niger Mojzita, Dominik; Koivistoinen, Outi M.; Maaheimo, Hannu Fungal Genetics and Biology, Vol. 49, Issue 2 https://doi.org/10.1016/j.fgb.2011.11.005	journal	February 2012
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Genetic manipulation of Aspergillus nidulans: meiotic progeny for genetic analysis and strain construction Todd, Richard B.; Davis, Meryl A.; Hynes, Michael J. Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.112	journal	April 2007
Isolation and analysis of xln R, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger van Peij, Noël N. M. E.; Visser, Jaap; de Graaff, Leo H. Molecular Microbiology, Vol. 27, Issue 1 https://doi.org/10.1046/j.1365-2958.1998.00666.x	journal	January 1998
The Aspergillus niger transcriptional activator XlnR, which is involved in the degradation of the polysaccharides xylan and cellulose, also regulates d-xylose reductase gene expression Hasper, Alinda A.; Visser, Jaap; de Graaff, Leo H. Molecular Microbiology, Vol. 36, Issue 1 https://doi.org/10.1046/j.1365-2958.2000.01843.x	journal	April 2000
l- xylo -3-Hexulose Reductase Is the Missing Link in the Oxidoreductive Pathway for d-Galactose Catabolism in Filamentous Fungi Mojzita, Dominik; Herold, Silvia; Metz, Benjamin Journal of Biological Chemistry, Vol. 287, Issue 31 https://doi.org/10.1074/jbc.m112.372755	journal	May 2012
L-Arabinose and D-Xylose Catabolism in Aspergillus niger Witteveen, C. F. B.; Busink, R.; Van De Vondervoort, P. Microbiology, Vol. 135, Issue 8 https://doi.org/10.1099/00221287-135-8-2163	journal	August 1989
The d-xylose reductase of Hypocrea jecorina is the major aldose reductase in pentose and d-galactose catabolism and necessary for β-galactosidase and cellulase induction by lactose Seiboth, Bernhard; Gamauf, Christian; Pail, Manuela Molecular Microbiology, Vol. 66, Issue 4 https://doi.org/10.1111/j.1365-2958.2007.05953.x	journal	November 2007
The metabolic role and evolution of l-arabinitol 4-dehydrogenase of Hypocrea jecorina Pail, Manuela; Peterbauer, Thomas; Seiboth, Bernhard European Journal of Biochemistry, Vol. 271, Issue 10 https://doi.org/10.1111/j.1432-1033.2004.04088.x	journal	May 2004
Characterization of an Aspergillus nidulans L-arabitol dehydrogenase mutant Vries, Ronald P.; Flipphi, Michel J. A.; Witteveen, Cor F. B. FEMS Microbiology Letters, Vol. 123, Issue 1-2 https://doi.org/10.1111/j.1574-6968.1994.tb07205.x	journal	October 1994
d-Galactose uptake is nonfunctional in the conidiospores of Aspergillus niger Fekete, Erzsébet; Vries, Ronald P.; Seiboth, Bernhard FEMS Microbiology Letters, Vol. 329, Issue 2 https://doi.org/10.1111/j.1574-6968.2012.02524.x	journal	February 2012
Unique Regulatory Mechanism for d-Galactose Utilization in Aspergillus nidulans Christensen, Ulla; Gruben, Birgit S.; Madrid, Susan Applied and Environmental Microbiology, Vol. 77, Issue 19 https://doi.org/10.1128/aem.05290-11	journal	August 2011
A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production de Vries, R. P.; Burgers, K.; van de Vondervoort, P. J. I. Applied and Environmental Microbiology, Vol. 70, Issue 7 https://doi.org/10.1128/aem.70.7.3954-3959.2004	journal	July 2004
Aspergillus Enzymes Involved in Degradation of Plant Cell Wall Polysaccharides de Vries, R. P.; Visser, J. Microbiology and Molecular Biology Reviews, Vol. 65, Issue 4 https://doi.org/10.1128/mmbr.65.4.497-522.2001	journal	December 2001
Analysis of regulation of pentose utilisation in Aspergillus niger reveals evolutionary adaptations in Eurotiales Battaglia, E.; Visser, L.; Nijssen, A. Studies in Mycology, Vol. 69 https://doi.org/10.3114/sim.2011.69.03	journal	June 2011
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Enzyme lesions in galactose non-utilising mutants of Aspergillus nidulans Roberts, C. F. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 201, Issue 2 https://doi.org/10.1016/0304-4165(70)90301-6	journal	February 1970
Biodiversity and evolution of primary carbon metabolism in Aspergillus nidulans and other Aspergillus spp. Flipphi, Michel; Sun, Jibin; Robellet, Xavier Fungal Genetics and Biology, Vol. 46, Issue 1 https://doi.org/10.1016/j.fgb.2008.07.018	journal	March 2009
The transcriptional activators AraR and XlnR from Aspergillus niger regulate expression of pentose catabolic and pentose phosphate pathway genes Battaglia, Evy; Zhou, Miaomiao; de Vries, Ronald P. Research in Microbiology, Vol. 165, Issue 7 https://doi.org/10.1016/j.resmic.2014.07.013	journal	September 2014
The Aspergillus niger d -xylulose kinase gene is co-expressed with genes encoding arabinan degrading enzymes, and is essential for growth on d -xylose and l -arabinose: Aspergillus niger xylulose kinase vanKuyk, Patricia A.; de Groot, Marco J. L.; Ruijter, George J. G. European Journal of Biochemistry, Vol. 268, Issue 20 https://doi.org/10.1046/j.0014-2956.2001.02482.x	journal	October 2001
Cloning and Expression of a Fungal l-Arabinitol 4-Dehydrogenase Gene Richard, Peter; Londesborough, John; Putkonen, Mikko Journal of Biological Chemistry, Vol. 276, Issue 44 https://doi.org/10.1074/jbc.M104022200	journal	August 2001
Identification of an l-Arabinose Reductase Gene in Aspergillus niger and Its Role in l-Arabinose Catabolism Mojzita, Dominik; Penttilä, Merja; Richard, Peter Journal of Biological Chemistry, Vol. 285, Issue 31 https://doi.org/10.1074/jbc.M110.113399	journal	May 2010
l- xylo -3-Hexulose Reductase Is the Missing Link in the Oxidoreductive Pathway for d-Galactose Catabolism in Filamentous Fungi Mojzita, Dominik; Herold, Silvia; Metz, Benjamin Journal of Biological Chemistry, Vol. 287, Issue 31 https://doi.org/10.1074/jbc.M112.372755	journal	May 2012
The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose. Frey, P. A. The FASEB Journal, Vol. 10, Issue 4 https://doi.org/10.1096/fasebj.10.4.8647345	journal	March 1996
Unique Regulatory Mechanism for d-Galactose Utilization in Aspergillus nidulans Christensen, Ulla; Gruben, Birgit S.; Madrid, Susan Applied and Environmental Microbiology, Vol. 77, Issue 19 https://doi.org/10.1128/AEM.05290-11	journal	August 2011
A New Black Aspergillus Species, A. vadensis, Is a Promising Host for Homologous and Heterologous Protein Production de Vries, R. P.; Burgers, K.; van de Vondervoort, P. J. I. Applied and Environmental Microbiology, Vol. 70, Issue 7 https://doi.org/10.1128/AEM.70.7.3954-3959.2004	journal	July 2004
Aspergillus Enzymes Involved in Degradation of Plant Cell Wall Polysaccharides de Vries, R. P.; Visser, J. Microbiology and Molecular Biology Reviews, Vol. 65, Issue 4 https://doi.org/10.1128/MMBR.65.4.497-522.2001	journal	December 2001
Hemicelluloses Scheller, Henrik Vibe; Ulvskov, Peter Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-042809-112315	journal	June 2010

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Identification of a Novel L-rhamnose Uptake Transporter in the Filamentous Fungus Aspergillus niger Sloothaak, Jasper; Odoni, Dorett I.; Martins dos Santos, Vitor A. P. PLOS Genetics, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pgen.1006468	journal	December 2016
NapA Mediates a Redox Regulation of the Antioxidant Response, Carbon Utilization and Development in Aspergillus nidulans Mendoza-Martínez, Ariann E.; Lara-Rojas, Fernando; Sánchez, Olivia Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00516	journal	March 2017
Carbon Catabolite Repression in Filamentous Fungi Adnan, Muhammad; Zheng, Wenhui; Islam, Waqar International Journal of Molecular Sciences, Vol. 19, Issue 1 https://doi.org/10.3390/ijms19010048	journal	December 2017
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