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Title: The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus

Abstract

Filamentous fungi, such as Neurospora crassa , are very efficient in deconstructing plant biomass by the secretion of an arsenal of plant cell wall-degrading enzymes, by remodeling metabolism to accommodate production of secreted enzymes, and by enabling transport and intracellular utilization of plant biomass components. Although a number of enzymes and transcriptional regulators involved in plant biomass utilization have been identified, how filamentous fungi sense and integrate nutritional information encoded in the plant cell wall into a regulatory hierarchy for optimal utilization of complex carbon sources is not understood. Here, we performed transcriptional profiling of N. crassa on 40 different carbon sources, including plant biomass, to provide data on how fungi sense simple to complex carbohydrates. From these data, we identified regulatory factors in N. crassa and characterized one (PDR-2) associated with pectin utilization and one with pectin/hemicellulose utilization (ARA-1). Using in vitro DNA affinity purification sequencing (DAP-seq), we identified direct targets of transcription factors involved in regulating genes encoding plant cell wall-degrading enzymes. In particular, our data clarified the role of the transcription factor VIB-1 in the regulation of genes encoding plant cell wall-degrading enzymes and nutrient scavenging and revealed a major role of the carbon catabolite repressor CRE-1more » in regulating the expression of major facilitator transporter genes. These data contribute to a more complete understanding of cross talk between transcription factors and their target genes, which are involved in regulating nutrient sensing and plant biomass utilization on a global level.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1602098
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: 117 Journal Issue: 11; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English

Citation Formats

Wu, Vincent W., Thieme, Nils, Huberman, Lori B., Dietschmann, Axel, Kowbel, David J., Lee, Juna, Calhoun, Sara, Singan, Vasanth R., Lipzen, Anna, Xiong, Yi, Monti, Remo, Blow, Matthew J., O’Malley, Ronan C., Grigoriev, Igor V., Benz, J. Philipp, and Glass, N. Louise. The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus. United States: N. p., 2020. Web. doi:10.1073/pnas.1915611117.
Wu, Vincent W., Thieme, Nils, Huberman, Lori B., Dietschmann, Axel, Kowbel, David J., Lee, Juna, Calhoun, Sara, Singan, Vasanth R., Lipzen, Anna, Xiong, Yi, Monti, Remo, Blow, Matthew J., O’Malley, Ronan C., Grigoriev, Igor V., Benz, J. Philipp, & Glass, N. Louise. The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus. United States. doi:10.1073/pnas.1915611117.
Wu, Vincent W., Thieme, Nils, Huberman, Lori B., Dietschmann, Axel, Kowbel, David J., Lee, Juna, Calhoun, Sara, Singan, Vasanth R., Lipzen, Anna, Xiong, Yi, Monti, Remo, Blow, Matthew J., O’Malley, Ronan C., Grigoriev, Igor V., Benz, J. Philipp, and Glass, N. Louise. Fri . "The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus". United States. doi:10.1073/pnas.1915611117.
@article{osti_1602098,
title = {The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus},
author = {Wu, Vincent W. and Thieme, Nils and Huberman, Lori B. and Dietschmann, Axel and Kowbel, David J. and Lee, Juna and Calhoun, Sara and Singan, Vasanth R. and Lipzen, Anna and Xiong, Yi and Monti, Remo and Blow, Matthew J. and O’Malley, Ronan C. and Grigoriev, Igor V. and Benz, J. Philipp and Glass, N. Louise},
abstractNote = {Filamentous fungi, such as Neurospora crassa , are very efficient in deconstructing plant biomass by the secretion of an arsenal of plant cell wall-degrading enzymes, by remodeling metabolism to accommodate production of secreted enzymes, and by enabling transport and intracellular utilization of plant biomass components. Although a number of enzymes and transcriptional regulators involved in plant biomass utilization have been identified, how filamentous fungi sense and integrate nutritional information encoded in the plant cell wall into a regulatory hierarchy for optimal utilization of complex carbon sources is not understood. Here, we performed transcriptional profiling of N. crassa on 40 different carbon sources, including plant biomass, to provide data on how fungi sense simple to complex carbohydrates. From these data, we identified regulatory factors in N. crassa and characterized one (PDR-2) associated with pectin utilization and one with pectin/hemicellulose utilization (ARA-1). Using in vitro DNA affinity purification sequencing (DAP-seq), we identified direct targets of transcription factors involved in regulating genes encoding plant cell wall-degrading enzymes. In particular, our data clarified the role of the transcription factor VIB-1 in the regulation of genes encoding plant cell wall-degrading enzymes and nutrient scavenging and revealed a major role of the carbon catabolite repressor CRE-1 in regulating the expression of major facilitator transporter genes. These data contribute to a more complete understanding of cross talk between transcription factors and their target genes, which are involved in regulating nutrient sensing and plant biomass utilization on a global level.},
doi = {10.1073/pnas.1915611117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 11,
volume = 117,
place = {United States},
year = {2020},
month = {2}
}

Journal Article:
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DOI: 10.1073/pnas.1915611117

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