A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism
Abstract
In Neurospora crassa, the transcription factor COL-26 functions as a regulator of glucose signaling and metabolism. Its loss leads to resistance to carbon catabolite repression. Here, we report that COL-26 is necessary for the expression of amylolytic genes in N. crassa and is required for the utilization of maltose and starch. Additionally, the Δcol-26 mutant shows growth defects on preferred carbon sources, such as glucose, an effect that was alleviated if glutamine replaced ammonium as the primary nitrogen source. This rescue did not occur when maltose was used as a sole carbon source. Transcriptome and metabolic analyses of the Δcol-26 mutant relative to its wild type parental strain revealed that amino acid and nitrogen metabolism, the TCA cycle and GABA shunt were adversely affected. Phylogenetic analysis showed a single col-26 homolog in Sordariales, Ophilostomatales, and the Magnaporthales, but an expanded number of col-26 homologs in other filamentous fungal species. Deletion of the closest homolog of col-26 in Trichoderma reesei, bglR, resulted in a mutant with similar preferred carbon source growth deficiency, and which was alleviated if glutamine was the sole nitrogen source, suggesting conservation of COL-26 and BglR function. Our finding provides novel insight into the role of COL-26 formore »
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1357713
- Alternate Identifier(s):
- OSTI ID: 1355134; OSTI ID: 1379833
- Grant/Contract Number:
- SC0012627; AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Name: PLoS Genetics Journal Volume: 13 Journal Issue: 5; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Xiong, Yi, Wu, Vincent W., Lubbe, Andrea, Qin, Lina, Deng, Siwen, Kennedy, Megan, Bauer, Diane, Singan, Vasanth R., Barry, Kerrie, Northen, Trent R., Grigoriev, Igor V., and Glass, N. Louise. A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism. United States: N. p., 2017.
Web. doi:10.1371/journal.pgen.1006737.
Xiong, Yi, Wu, Vincent W., Lubbe, Andrea, Qin, Lina, Deng, Siwen, Kennedy, Megan, Bauer, Diane, Singan, Vasanth R., Barry, Kerrie, Northen, Trent R., Grigoriev, Igor V., & Glass, N. Louise. A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism. United States. https://doi.org/10.1371/journal.pgen.1006737
Xiong, Yi, Wu, Vincent W., Lubbe, Andrea, Qin, Lina, Deng, Siwen, Kennedy, Megan, Bauer, Diane, Singan, Vasanth R., Barry, Kerrie, Northen, Trent R., Grigoriev, Igor V., and Glass, N. Louise. Wed .
"A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism". United States. https://doi.org/10.1371/journal.pgen.1006737.
@article{osti_1357713,
title = {A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism},
author = {Xiong, Yi and Wu, Vincent W. and Lubbe, Andrea and Qin, Lina and Deng, Siwen and Kennedy, Megan and Bauer, Diane and Singan, Vasanth R. and Barry, Kerrie and Northen, Trent R. and Grigoriev, Igor V. and Glass, N. Louise},
abstractNote = {In Neurospora crassa, the transcription factor COL-26 functions as a regulator of glucose signaling and metabolism. Its loss leads to resistance to carbon catabolite repression. Here, we report that COL-26 is necessary for the expression of amylolytic genes in N. crassa and is required for the utilization of maltose and starch. Additionally, the Δcol-26 mutant shows growth defects on preferred carbon sources, such as glucose, an effect that was alleviated if glutamine replaced ammonium as the primary nitrogen source. This rescue did not occur when maltose was used as a sole carbon source. Transcriptome and metabolic analyses of the Δcol-26 mutant relative to its wild type parental strain revealed that amino acid and nitrogen metabolism, the TCA cycle and GABA shunt were adversely affected. Phylogenetic analysis showed a single col-26 homolog in Sordariales, Ophilostomatales, and the Magnaporthales, but an expanded number of col-26 homologs in other filamentous fungal species. Deletion of the closest homolog of col-26 in Trichoderma reesei, bglR, resulted in a mutant with similar preferred carbon source growth deficiency, and which was alleviated if glutamine was the sole nitrogen source, suggesting conservation of COL-26 and BglR function. Our finding provides novel insight into the role of COL-26 for utilization of starch and in integrating carbon and nitrogen metabolism for balanced metabolic activities for optimal carbon and nitrogen distribution.},
doi = {10.1371/journal.pgen.1006737},
journal = {PLoS Genetics},
number = 5,
volume = 13,
place = {United States},
year = {Wed May 03 00:00:00 EDT 2017},
month = {Wed May 03 00:00:00 EDT 2017}
}
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Works referenced in this record:
Cellodextrin Transport in Yeast for Improved Biofuel Production
journal, September 2010
- Galazka, J. M.; Tian, C.; Beeson, W. T.
- Science, Vol. 330, Issue 6000
Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa
journal, December 2004
- Xie, Xin; Wilkinson, Heather H.; Correa, Alejandro
- Fungal Genetics and Biology, Vol. 41, Issue 12
Neurospora V. A Synthetic Medium Favoring Sexual Reproduction
journal, December 1947
- Westergaard, Mogens; Mitchell, Herschel K.
- American Journal of Botany, Vol. 34, Issue 10
Regulation of nitrogen metabolism and gene expression in fungi.
journal, January 1981
- Marzluf, G. A.
- Microbiological Reviews, Vol. 45, Issue 3
Transcriptomic comparison of Aspergillus niger growing on two different sugars reveals coordinated regulation of the secretory pathway
journal, January 2009
- Jørgensen, Thomas R.; Goosen, Theo; van den Hondel, Cees AMJJ
- BMC Genomics, Vol. 10, Issue 1
Open source clustering software
journal, February 2004
- de Hoon, M. J. L.; Imoto, S.; Nolan, J.
- Bioinformatics, Vol. 20, Issue 9
A broader role for AmyR in Aspergillus niger: regulation of the utilisation of d-glucose or d-galactose containing oligo- and polysaccharides
journal, August 2011
- vanKuyk, Patricia A.; Benen, Jaques A. E.; Wösten, Han A. B.
- Applied Microbiology and Biotechnology, Vol. 93, Issue 1
Functional characterisation of the non-essential protein kinases and phosphatases regulating Aspergillus nidulans hydrolytic enzyme production
journal, January 2013
- Brown, Neil; de Gouvea, Paula; Krohn, Nádia
- Biotechnology for Biofuels, Vol. 6, Issue 1
Enhancing the utilization of host trehalose by fungal trehalase improves the virulence of fungal insecticide
journal, June 2015
- Peng, Guoxiong; Jin, Kai; Liu, Yingchun
- Applied Microbiology and Biotechnology, Vol. 99, Issue 20
Analysis of a conserved cellulase transcriptional regulator reveals inducer-independent production of cellulolytic enzymes in Neurospora crassa
journal, June 2013
- Coradetti, Samuel T.; Xiong, Yi; Glass, N. Louise
- MicrobiologyOpen, Vol. 2, Issue 4
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
The bZIP Transcription Factor HAC-1 Is Involved in the Unfolded Protein Response and Is Necessary for Growth on Cellulose in Neurospora crassa
journal, July 2015
- Montenegro-Montero, Alejandro; Goity, Alejandra; Larrondo, Luis F.
- PLOS ONE, Vol. 10, Issue 7
The cross-pathway control gene of Neurospora crassa, cpc-1, encodes a protein similar to GCN4 of yeast and the DNA-binding domain of the oncogene v-jun-encoded protein.
journal, June 1988
- Paluh, J. L.; Orbach, M. J.; Legerton, T. L.
- Proceedings of the National Academy of Sciences, Vol. 85, Issue 11
Two conidiation-related Zn(II)2Cys6 transcription factor genes in the rice blast fungus
journal, December 2013
- Chung, Hyunjung; Choi, Jaehyuk; Park, Sook-Young
- Fungal Genetics and Biology, Vol. 61
VIB1, a Link between Glucose Signaling and Carbon Catabolite Repression, Is Essential for Plant Cell Wall Degradation by Neurospora crassa
journal, August 2014
- Xiong, Yi; Sun, Jianping; Glass, N. Louise
- PLoS Genetics, Vol. 10, Issue 8
A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei
journal, January 1987
- Penttilä, Merja; Nevalainen, Helena; Rättö, Marjaana
- Gene, Vol. 61, Issue 2, p. 155-164
Regulation of α-amylase formation inAspergillus oryzae andAspergillus nidulans transformants
journal, January 1993
- Lachmund, Astrid; Urmann, Ute; Minol, Klaus
- Current Microbiology, Vol. 26, Issue 1
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Depression of uracil uptake by ammonium in Neurospora crassa.
journal, January 1976
- Magill, J. M.; Edwards, E. S.; Sabina, R. L.
- Journal of Bacteriology, Vol. 127, Issue 3
Synergistic and Dose-Controlled Regulation of Cellulase Gene Expression in Penicillium oxalicum
journal, September 2015
- Li, Zhonghai; Yao, Guangshan; Wu, Ruimei
- PLOS Genetics, Vol. 11, Issue 9
Characterization of the amyR gene encoding a transcriptional activator for the amylase genes in Aspergillus nidulans
journal, February 2001
- Tani, Shuji; Katsuyama, Yoko; Hayashi, Tomoko
- Current Genetics, Vol. 39, Issue 1
Mutants affecting amino acid cross-pathway control in Neurospora crassa
journal, April 1982
- Barthelmess, Ilse B.
- Genetical Research, Vol. 39, Issue 2
Split-Marker Recombination for Efficient Targeted Deletion of Fungal Genes
journal, December 2003
- Catlett, Natalie L.; Lee, Bee-Na; Yoder, O. C.
- Fungal Genetics Reports, Vol. 50, Issue 1
FungiFun2: a comprehensive online resource for systematic analysis of gene lists from fungal species
journal, October 2014
- Priebe, S.; Kreisel, C.; Horn, F.
- Bioinformatics, Vol. 31, Issue 3
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
VIB-1 Is Required for Expression of Genes Necessary for Programmed Cell Death in Neurospora crassa
journal, September 2006
- Dementhon, Karine; Iyer, Gopal; Glass, N. Louise
- Eukaryotic Cell, Vol. 5, Issue 12
Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles
journal, March 2008
- Yuan, Xiao-Lian; van der Kaaij, Rachel M.; van den Hondel, Cees A. M. J. J.
- Molecular Genetics and Genomics, Vol. 279, Issue 6
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Induction and repression of -amylase production in batch and continuous cultures of Aspergillus oryzae
journal, October 1995
- Morkeberg, R.; Carlsen, M.; Nielsen, J.
- Microbiology, Vol. 141, Issue 10
Metabolic fate of glutamate and evaluation of flux through the 4-aminobutyrate (GABA) shunt inAspergillus niger
journal, March 2000
- Kumar, Santosh; Punekar, Narayan S.; SatyaNarayan, V.
- Biotechnology and Bioengineering, Vol. 67, Issue 5
Regulation of the amylolytic and (hemi-)cellulolytic genes in aspergilli
journal, January 2001
- Tsukagoshi, Norihiro; Kobayashi, Tetsuo; Kato, Masashi
- The Journal of General and Applied Microbiology, Vol. 47, Issue 1
Transcriptional comparison of the filamentous fungus Neurospora crassa growing on three major monosaccharides D-glucose, D-xylose and L-arabinose
journal, January 2014
- Li, Jingen; Lin, Liangcai; Li, Huiyan
- Biotechnology for Biofuels, Vol. 7, Issue 1
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
journal, April 2016
- Letunic, Ivica; Bork, Peer
- Nucleic Acids Research, Vol. 44, Issue W1
Long-term strain improvements accumulate mutations in regulatory elements responsible for hyper-production of cellulolytic enzymes
journal, March 2013
- Liu, Guodong; Zhang, Lei; Qin, Yuqi
- Scientific Reports, Vol. 3, Issue 1
Characterization and expression analysis of a maltose-utilizing (MAL) cluster in Aspergillus oryzae
journal, January 2010
- Hasegawa, Sachiko; Takizawa, Masahiro; Suyama, Haruhiko
- Fungal Genetics and Biology, Vol. 47, Issue 1
The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes
journal, October 2004
- Ruepp, A.
- Nucleic Acids Research, Vol. 32, Issue 18
Deletion of homologs of the SREBP pathway results in hyper-production of cellulases in Neurospora crassa and Trichoderma reesei
journal, August 2015
- Reilly, Morgann C.; Qin, Lina; Craig, James P.
- Biotechnology for Biofuels, Vol. 8, Issue 1
Structural Basis for Substrate Targeting and Catalysis by Fungal Polysaccharide Monooxygenases
journal, June 2012
- Li, Xin; Beeson, William T.; Phillips, Christopher M.
- Structure, Vol. 20, Issue 6, p. 1051-1061
The bZIP Transcription Factor MoAP1 Mediates the Oxidative Stress Response and Is Critical for Pathogenicity of the Rice Blast Fungus Magnaporthe oryzae
journal, February 2011
- Guo, Min; Chen, Yue; Du, Yan
- PLoS Pathogens, Vol. 7, Issue 2
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration
journal, April 2012
- Thorvaldsdottir, H.; Robinson, J. T.; Mesirov, J. P.
- Briefings in Bioinformatics, Vol. 14, Issue 2, p. 178-192
Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined?
journal, June 2015
- Michaeli, Simon; Fromm, Hillel
- Frontiers in Plant Science, Vol. 6
Evidence of a Critical Role for Cellodextrin Transporte 2 (CDT-2) in Both Cellulose and Hemicellulose Degradation and Utilization in Neurospora crassa
journal, February 2014
- Cai, Pengli; Gu, Ruimeng; Wang, Bang
- PLoS ONE, Vol. 9, Issue 2
Characterising the Role of GABA and Its Metabolism in the Wheat Pathogen Stagonospora nodorum
journal, November 2013
- Mead, Oliver; Thynne, Eli; Winterberg, Britta
- PLoS ONE, Vol. 8, Issue 11
Regulation of trehalose mobilization in fungi.
journal, January 1984
- Thevelein, J. M.
- Microbiological Reviews, Vol. 48, Issue 1
HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014
- Anders, S.; Pyl, P. T.; Huber, W.
- Bioinformatics, Vol. 31, Issue 2
A family of starch-active polysaccharide monooxygenases
journal, September 2014
- Vu, V. V.; Beeson, W. T.; Span, E. A.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 38
A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors
journal, June 2006
- Colot, H. V.; Park, G.; Turner, G. E.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 27
New Insights into -Aminobutyric Acid Catabolism: Evidence for -Hydroxybutyric Acid and Polyhydroxybutyrate Synthesis in Saccharomyces cerevisiae
journal, May 2009
- Bach, B.; Meudec, E.; Lepoutre, J. -P.
- Applied and Environmental Microbiology, Vol. 75, Issue 13
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
The metabolism of 4-aminobutyrate (GABA) in fungi
journal, April 1997
- Kumar, Santosh; Punekar, Narayan S.
- Mycological Research, Vol. 101, Issue 4
Cellular and molecular responses of Neurospora crassa to non-thermal plasma at atmospheric pressure
journal, February 2012
- Park, Gyungsoon; Ryu, Young H.; Hong, Young J.
- Applied Physics Letters, Vol. 100, Issue 6
FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry
journal, December 2009
- Kind, Tobias; Wohlgemuth, Gert; Lee, Do Yup
- Analytical Chemistry, Vol. 81, Issue 24
The role of glutamine synthetase and glutamine metabolism in nitrogen metabolite repression, a regulatory phenomenon in the lower eukaryote Neurospora crassa
journal, August 1980
- Dunn-Coleman, Nigel S.; Garrett, Reginald H.
- MGG Molecular & General Genetics, Vol. 179, Issue 1
Cyclosporin A-resistance based gene placement system for Neurospora crassa
journal, May 2007
- Bardiya, Nirmala; Shiu, Patrick K. T.
- Fungal Genetics and Biology, Vol. 44, Issue 5
The proteome and phosphoproteome of Neurospora crassa in response to cellulose, sucrose and carbon starvation
journal, November 2014
- Xiong, Yi; Coradetti, Samuel T.; Li, Xin
- Fungal Genetics and Biology, Vol. 72
Transcriptional Profiling of Cross Pathway Control in Neurospora crassa and Comparative Analysis of the Gcn4 and CPC1 Regulons
journal, April 2007
- Tian, Chaoguang; Kasuga, Takao; Sachs, Matthew S.
- Eukaryotic Cell, Vol. 6, Issue 6
Global gene expression analysis of Aspergillus nidulans reveals metabolic shift and transcription suppression under hypoxia
journal, September 2010
- Masuo, Shunsuke; Terabayashi, Yasunobu; Shimizu, Motoyuki
- Molecular Genetics and Genomics, Vol. 284, Issue 6
Direct Target Network of the Neurospora crassa Plant Cell Wall Deconstruction Regulators CLR-1, CLR-2, and XLR-1
journal, October 2015
- Craig, James P.; Coradetti, Samuel T.; Starr, Trevor L.
- mBio, Vol. 6, Issue 5
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Bird Medium: an alternative to Vogel Medium
journal, September 2004
- Metzenberg, Robert L.
- Fungal Genetics Reports, Vol. 51, Issue 1
Evidence that γ-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato
journal, August 2001
- Solomon, Peter S.; Oliver, Richard P.
- Planta, Vol. 214, Issue 3
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
Cellobionic acid utilization: from Neurospora crassa to Saccharomyces cerevisiae
journal, August 2015
- Li, Xin; Chomvong, Kulika; Yu, Vivian Yaci
- Biotechnology for Biofuels, Vol. 8, Issue 1
Cellobiose Dehydrogenase and a Copper-Dependent Polysaccharide Monooxygenase Potentiate Cellulose Degradation by Neurospora crassa
journal, December 2011
- Phillips, Christopher M.; Beeson, William T.; Cate, Jamie H.
- ACS Chemical Biology, Vol. 6, Issue 12, p. 1399-1406
rco-3 , a Gene Involved in Glucose Transport and Conidiation in Neurospora crassa
journal, June 1997
- Madi, Lea; McBride, Sheila A.; Bailey, Lori A.
- Genetics, Vol. 146, Issue 2
Genome-wide analysis of maltose utilization and regulation in aspergilli
journal, August 2009
- Vongsangnak, W.; Salazar, M.; Hansen, K.
- Microbiology, Vol. 155, Issue 12
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
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Transcription factor ART1 mediates starch hydrolysis and mycotoxin production in Fusarium graminearum and F. verticillioides : Roles of ART1 in
journal, December 2015
- Oh, Mira; Son, Hokyoung; Choi, Gyung Ja
- Molecular Plant Pathology, Vol. 17, Issue 5
A new Zn(II)2Cys6-type transcription factor BglR regulates β-glucosidase expression in Trichoderma reesei
journal, May 2012
- Nitta, Mikiko; Furukawa, Takanori; Shida, Yosuke
- Fungal Genetics and Biology, Vol. 49, Issue 5
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing
journal, September 2009
- Le Crom, S.; Schackwitz, W.; Pennacchio, L.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12