Network of nutrient-sensing pathways and a conserved kinase cascade integrate osmolarity and carbon sensing in Neurospora crassa
Abstract
Significance Microbes have evolved complex signaling networks to identify and prioritize utilization of available energy sources. For many fungi, such as Neurospora crassa , this entails distinguishing between an array of carbon sources, including insoluble carbohydrates in plant cell walls. Here, we identified a repressor of the cellulose-response pathway in N . crassa . Using this derepressed mutant, we implicated the conserved hyperosmotic-response MAP kinase pathway in regulating the response of N . crassa to insoluble carbohydrates. We hypothesize that fungal species that degrade plant biomass use osmolarity as a proxy for soluble sugar in the environment to regulate their nutritional responses, enabling tailored production of lignocellulases. This finding could help in battling fungal plant diseases and in the production of second-generation biofuels.
- Authors:
-
[2]
- Plant and Microbial Biology Department, University of California, Berkeley, CA 94720,, Energy Biosciences Institute, University of California, Berkeley, CA 94720,
- Plant and Microbial Biology Department, University of California, Berkeley, CA 94720,, Energy Biosciences Institute, University of California, Berkeley, CA 94720,, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1396060
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 114 Journal Issue: 41; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Huberman, Lori B., Coradetti, Samuel T., and Glass, N. Louise. Network of nutrient-sensing pathways and a conserved kinase cascade integrate osmolarity and carbon sensing in Neurospora crassa. United States: N. p., 2017.
Web. doi:10.1073/pnas.1707713114.
Huberman, Lori B., Coradetti, Samuel T., & Glass, N. Louise. Network of nutrient-sensing pathways and a conserved kinase cascade integrate osmolarity and carbon sensing in Neurospora crassa. United States. https://doi.org/10.1073/pnas.1707713114
Huberman, Lori B., Coradetti, Samuel T., and Glass, N. Louise. Mon .
"Network of nutrient-sensing pathways and a conserved kinase cascade integrate osmolarity and carbon sensing in Neurospora crassa". United States. https://doi.org/10.1073/pnas.1707713114.
@article{osti_1396060,
title = {Network of nutrient-sensing pathways and a conserved kinase cascade integrate osmolarity and carbon sensing in Neurospora crassa},
author = {Huberman, Lori B. and Coradetti, Samuel T. and Glass, N. Louise},
abstractNote = {Significance Microbes have evolved complex signaling networks to identify and prioritize utilization of available energy sources. For many fungi, such as Neurospora crassa , this entails distinguishing between an array of carbon sources, including insoluble carbohydrates in plant cell walls. Here, we identified a repressor of the cellulose-response pathway in N . crassa . Using this derepressed mutant, we implicated the conserved hyperosmotic-response MAP kinase pathway in regulating the response of N . crassa to insoluble carbohydrates. We hypothesize that fungal species that degrade plant biomass use osmolarity as a proxy for soluble sugar in the environment to regulate their nutritional responses, enabling tailored production of lignocellulases. This finding could help in battling fungal plant diseases and in the production of second-generation biofuels.},
doi = {10.1073/pnas.1707713114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 41,
volume = 114,
place = {United States},
year = {2017},
month = {9}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1707713114
https://doi.org/10.1073/pnas.1707713114
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 28 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
ATF-1 transcription factor regulates the expression of ccg-1 and cat-1 genes in response to fludioxonil under OS-2 MAP kinase in Neurospora crassa
journal, December 2008
- Yamashita, Kazuhiro; Shiozawa, Azusa; Watanabe, Setsuko
- Fungal Genetics and Biology, Vol. 45, Issue 12
Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in theos-1 mutants ofNeurospora crassa
journal, January 2001
- Ochiai, Noriyuki; Fujimura, Makoto; Motoyama, Takayuki
- Pest Management Science, Vol. 57, Issue 5
Major Sensing Proteins in Pathogenic Fungi: The Hybrid Histidine Kinase Family
journal, July 2016
- Hérivaux, Anaïs; So, Yee-Seul; Gastebois, Amandine
- PLOS Pathogens, Vol. 12, Issue 7
Interactions among HAMP Domain Repeats Act as an Osmosensing Molecular Switch in Group III Hybrid Histidine Kinases from Fungi
journal, February 2010
- Meena, Netrapal; Kaur, Harsimran; Mondal, Alok K.
- Journal of Biological Chemistry, Vol. 285, Issue 16
Filamentous fungal carbon catabolite repression supports metabolic plasticity and stress responses essential for disease progression
journal, April 2017
- Beattie, Sarah R.; Mark, Kenneth M. K.; Thammahong, Arsa
- PLOS Pathogens, Vol. 13, Issue 4
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
Putative Homologs of SSK22 MAPKK Kinase and PBS2 MAPK Kinase of Saccharomyces cerevisiae Encoded by os-4 and os-5 Genes for Osmotic Sensitivity and Fungicide…
journal, January 2003
- Fujimura, Makoto; Ochiai, Noriyuki; Oshima, Michiyo
- Bioscience, Biotechnology, and Biochemistry, Vol. 67, Issue 1
A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells
journal, August 1994
- Han, J.; Lee, J.; Bibbs, L.
- Science, Vol. 265, Issue 5173
Chemical and physical studies of Neurospora crassa invertase. Molecular weight, amino acid and carbohydrate composition, and quaternary structure
journal, January 1971
- Braymer, H. D.; Meachum, Z. D.; Colvin, H. J.
- Biochemistry, Vol. 10, Issue 2
Yeast HOG1 MAP Kinase Cascade Is Regulated by a Multistep Phosphorelay Mechanism in the SLN1–YPD1–SSK1 “Two-Component” Osmosensor
journal, September 1996
- Posas, Francesc; Wurgler-Murphy, Susannah M.; Maeda, Tatsuya
- Cell, Vol. 86, Issue 6
Carbon Regulation of Ribosomal Genes in Neurospora crassa Occurs by a Mechanism Which Does Not Require Cre-1, the Homologue of the Aspergillus Carbon Catabolite Repressor, CreA
journal, April 1999
- de la Serna, Ivana; Ng, Dean; Tyler, Brett M.
- Fungal Genetics and Biology, Vol. 26, Issue 3
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
Direct Transcriptional Control of a p38 MAPK Pathway by the Circadian Clock in Neurospora crassa
journal, November 2011
- Lamb, Teresa M.; Goldsmith, Charles S.; Bennett, Lindsay
- PLoS ONE, Vol. 6, Issue 11
Glucose Starvation Alters Heat Shock Response, Leading to Death of Wild Type Cells and Survival of MAP Kinase Signaling Mutant
journal, November 2016
- Plesofsky, Nora; Higgins, LeeAnn; Markowski, Todd
- PLOS ONE, Vol. 11, Issue 11
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
Carbon catabolite repression of the Aspergillus nidulans xlnA gene
journal, January 1999
- Orejas, Margarita; MacCabe, Andrew Peter; Perez Gonzalez, Jose Antonio
- Molecular Microbiology, Vol. 31, Issue 1
Different Levels of Catabolite Repression Optimize Growth in Stable and Variable Environments
journal, January 2014
- New, Aaron M.; Cerulus, Bram; Govers, Sander K.
- PLoS Biology, Vol. 12, Issue 1
A Mitogen-Activated Protein Kinase Tmk3 Participates in High Osmolarity Resistance, Cell Wall Integrity Maintenance and Cellulase Production Regulation in Trichoderma reesei
journal, August 2013
- Wang, Mingyu; Zhao, Qiushuang; Yang, Jinghua
- PLoS ONE, Vol. 8, Issue 8
The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research
journal, January 2010
- McCluskey, K.; Wiest, A.; Plamann, M.
- Journal of Biosciences, Vol. 35, Issue 1
N -Acetylglucosamine (GlcNAc)-Inducible Gene GIG2 Is a Novel Component of GlcNAc Metabolism in Candida albicans
journal, November 2013
- Ghosh, Swagata; Hanumantha Rao, Kongara; Bhavesh, Neel Sarovar
- Eukaryotic Cell, Vol. 13, Issue 1
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
Metabolic Respiration Induces AMPK- and Ire1p-Dependent Activation of the p38-Type HOG MAPK Pathway
journal, October 2014
- Adhikari, Hema; Cullen, Paul J.
- PLoS Genetics, Vol. 10, Issue 10
A two-component system that regulates an osmosensing MAP kinase cascade in yeast
journal, May 1994
- Maeda, Tatsuya; Wurgler-Murphy, Susannah M.; Saito, Haruo
- Nature, Vol. 369, Issue 6477
The Wide-Domain Carbon Catabolite Repressor CreA Indirectly Controls Expression of the Aspergillus nidulans xlnB Gene, Encoding the Acidic Endo- -(1,4)-Xylanase X24
journal, March 2001
- Orejas, M.; MacCabe, A. P.; Perez-Gonzalez, J. A.
- Journal of Bacteriology, Vol. 183, Issue 5
Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic and oxidative stresses in Neurospora crassa
journal, January 2007
- Banno, Shinpei; Noguchi, Rieko; Yamashita, Kazuhiro
- Current Genetics, Vol. 51, Issue 3
AMP-activated Protein Kinase and p38 MAPK Activate O -GlcNAcylation of Neuronal Proteins during Glucose Deprivation
journal, March 2008
- Cheung, Win D.; Hart, Gerald W.
- Journal of Biological Chemistry, Vol. 283, Issue 19
Deciphering Transcriptional Regulatory Mechanisms Associated with Hemicellulose Degradation in Neurospora crassa
journal, February 2012
- Sun, Jianping; Tian, Chaoguang; Diamond, Spencer
- Eukaryotic Cell, Vol. 11, Issue 4
Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins
journal, April 2012
- Znameroski, E. A.; Coradetti, S. T.; Roche, C. M.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
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
The Hypocrea jecorina (Trichoderma reesei) hypercellulolytic mutant RUT C30 lacks a 85 kb (29 gene-encoding) region of the wild-type genome
journal, January 2008
- Seidl, Verena; Gamauf, Christian; Druzhinina, Irina S.
- BMC Genomics, Vol. 9, Issue 1
An Inhibitor of Nonhomologous End-Joining Abrogates Double-Strand Break Repair and Impedes Cancer Progression
journal, December 2012
- Srivastava, Mrinal; Nambiar, Mridula; Sharma, Sheetal
- Cell, Vol. 151, Issue 7
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
The genome sequence of the filamentous fungus Neurospora crassa
journal, April 2003
- Galagan, James E.; Calvo, Sarah E.; Borkovich, Katherine A.
- Nature, Vol. 422, Issue 6934
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
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
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010
- McKenna, A.; Hanna, M.; Banks, E.
- Genome Research, Vol. 20, Issue 9
Regulation of the lignocellulolytic response in filamentous fungi
journal, July 2016
- Huberman, Lori B.; Liu, Jason; Qin, Lina
- Fungal Biology Reviews, Vol. 30, Issue 3
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
Osmoregulation and Fungicide Resistance: the Neurospora crassa os-2 Gene Encodes a HOG1 Mitogen-Activated Protein Kinase Homologue
journal, February 2002
- Zhang, Y.; Lamm, R.; Pillonel, C.
- Applied and Environmental Microbiology, Vol. 68, Issue 2
Xylanase production in Aspergillus nidulans: induction and carbon catabolite repression
journal, January 1994
- Piñaga, F.
- FEMS Microbiology Letters, Vol. 115, Issue 2-3
Group III Histidine Kinase Is a Positive Regulator of Hog1-Type Mitogen-Activated Protein Kinase in Filamentous Fungi
journal, November 2005
- Yoshimi, Akira; Kojima, Kaihei; Takano, Yoshitaka
- Eukaryotic Cell, Vol. 4, Issue 11
Characterization of Greenbeard Genes Involved in Long-Distance Kind Discrimination in a Microbial Eukaryote
journal, April 2016
- Heller, Jens; Zhao, Jiuhai; Rosenfield, Gabriel
- PLOS Biology, Vol. 14, Issue 4
Glucose metabolism and cancer
journal, December 2006
- Shaw, Reuben J.
- Current Opinion in Cell Biology, Vol. 18, Issue 6
The S Helix Mediates Signal Transmission as a HAMP Domain Coiled-Coil Extension in the NarX Nitrate Sensor from Escherichia coli K-12
journal, December 2009
- Stewart, V.; Chen, L. -L.
- Journal of Bacteriology, Vol. 192, Issue 3
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
Identification of the CRE-1 Cellulolytic Regulon in Neurospora crassa
journal, September 2011
- Sun, Jianping; Glass, N. Louise
- PLoS ONE, Vol. 6, Issue 9
Nutrient sensing and metabolic decisions
journal, December 2004
- Lindsley, Janet E.; Rutter, Jared
- Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 139, Issue 4
Analysis of Mitogen-Activated Protein Kinase Signaling Specificity in Response to Hyperosmotic Stress: Use of an Analog-Sensitive HOG1 Allele
journal, August 2006
- Westfall, Patrick J.; Thorner, Jeremy
- Eukaryotic Cell, Vol. 5, Issue 8
Identification of OS-2 MAP kinase-dependent genes induced in response to osmotic stress, antifungal agent fludioxonil, and heat shock in Neurospora crassa
journal, March 2007
- Noguchi, Rieko; Banno, Shinpei; Ichikawa, Ryota
- Fungal Genetics and Biology, Vol. 44, Issue 3
Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins.
journal, September 1990
- Nehlin, J. O.; Ronne, H.
- The EMBO Journal, Vol. 9, Issue 9
ISOLATION, CHARACTERIZATION, AND GENETIC ANALYSIS OF OSMOTIC MUTANTS OF NEUROSPORA CRASSA
journal, December 1969
- Mays, Laura Livingston
- Genetics, Vol. 63, Issue 4
The Neurospora crassa OS MAPK pathway-activated transcription factor ASL-1 contributes to circadian rhythms in pathway responsive clock-controlled genes
journal, February 2012
- Lamb, Teresa M.; Finch, Katelyn E.; Bell-Pedersen, Deborah
- Fungal Genetics and Biology, Vol. 49, Issue 2
Isolation and analysis of xln R, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger
journal, January 1998
- van Peij, Noël N. M. E.; Visser, Jaap; de Graaff, Leo H.
- Molecular Microbiology, Vol. 27, Issue 1
The Osmotic-1 Locus of Neurospora crassa Encodes a Putative Histidine Kinase Similar to Osmosensors of Bacteria and Yeast
journal, June 1997
- Schumacher, Marc M.; Enderlin, Carol S.; Selitrennikoff, Claude P.
- Current Microbiology, Vol. 34, Issue 6
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