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Title: 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 » utilization of starch and in integrating carbon and nitrogen metabolism for balanced metabolic activities for optimal carbon and nitrogen distribution.« less

Authors:
 [1];  [1];  [2];  [1]; ORCiD logo [3];  [4];  [4]; ORCiD logo [4];  [4];  [5];  [6]; ORCiD logo [7];  [8]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology, Energy Biosciences Inst.
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology
  3. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology; Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States)
  6. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology, Energy Biosciences Inst.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology
  8. Hudson Alpha Inst. for Biotechnology, Huntsville, AL (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1357713
Alternate Identifier(s):
OSTI ID: 1355134; OSTI ID: 1379833
Grant/Contract Number:  
AC02-05CH11231; SC0012627
Resource Type:
Journal Article: Published Article
Journal Name:
PLoS Genetics
Additional Journal Information:
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., Glass, N. Louise, and Swaminathan, Kankshita. 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, & Swaminathan, Kankshita. A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism. United States. 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, and Swaminathan, Kankshita. Wed . "A fungal transcription factor essential for starch degradation affects integration of carbon and nitrogen metabolism". United States. doi: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 and Swaminathan, Kankshita},
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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1371/journal.pgen.1006737

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Cited by: 1 work
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