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Title: Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition in Neurospora crassa

Abstract

Fungal plant cell wall degradation processes are governed by complex regulatory mechanisms, allowing the organisms to adapt their metabolic program with high specificity to the substrate at hand. While the uptake of representative plant cell wall mono- and disaccharides is known to induce specific transcriptional and translational responses, the processes related to early signal reception and transduction are still enigmatic. A fast and reversible way of transmitting extracellular signals throughout the cell are protein phosphorylations, which could initiate adaptations of the fungal metabolism on a post-translational level. In an effort to elucidate how changes in the initial substrate recognition phase of Neurospora crassa affect the global phosphorylation pattern, phosphoproteomics was performed after a short (2 minute) induction period with several plant cell wall-related mono- and disaccharides. The MS/MS-based peptide analysis revealed a large number of proteins that are phosphorylated or de-phosphorylated in a substrate-specific manner. A protein-protein-interaction network was constructed based on the proteins identified by MS/MS. Using this network, putative interaction partners of several phosphorylated proteins of interest were determined. This led to the discovery of substrate-specific protein-interactions that might be involved in mediating the substrate recognition of N. crassa. Besides a high number of kinases, phosphatases and transcriptionmore » factors to be affected by differential phosphorylation, our data demonstrate, for example, that the cAMP signaling pathway is heavily modified by substrate-specific phosphorylations, including the key component adenylate cyclase CR-1 as well as several G-protein-coupled receptors. In addition, four differentially phosphorylated F-Box proteins were identified in the phospho-proteome. When physiologically characterized using the respective gene deletion strains, Fbx-19 and Fbx-22 were found to be involved in carbon catabolite repression responses. Overall, these results improve our understanding of how fungi respond to environmental cues and provide novel insights into the mechanisms of sensory perception and signal transduction during lignocellulose degradation.« less

Authors:
 [1];  [1];  [2]; ORCiD logo [2]; ORCiD logo [2];  [2]; ORCiD logo [2];  [3];  [4];  [5];  [5];  [6];  [7];  [8];  [9];  [3];  [10];  [11]
  1. Technical Univ. of Munich, Freising (Germany)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Homi Bhabha National Inst. (HBNI), Chennai (India)
  4. Univ. de São Paulo, Ribeirao Preto (Brazil)
  5. Chinese Academy of Sciences (CAS), Tianjin (China)
  6. Univ. of Gottingen, Gottingen (Germany)
  7. Univ. of California, Riverside, CA (United States)
  8. AIT - Austrian Inst. of Technology GmbH, Tulln (Austria)
  9. Pontificia Univ. Catolica de Chile, Santiago (Chile)
  10. Univ. de São Paulo, Ribeirao Preto (Brazil); Technical Univ. of Munich, Garching (Germany)
  11. Technical Univ. of Munich, Freising (Germany); Technical Univ. of Munich, Garching (Germany)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1577974
Report Number(s):
PNNL-SA-143199
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 10; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Horta, Maria Augusta C., Thieme, Nils, Gao, Yuqian, Burnum-Johnson, Kristin E., Nicora, Carrie D., Gritsenko, Marina A., Lipton, Mary S., Mohanraj, Karthikeyan, José de Assis, Leandro, Lin, Liangcai, Tian, Chaoguang, Braus, Gerhard H., Borkovich, Katherine A., Schmoll, Monika, Larrondo, Luis F., Samal, Areejit, Goldman, Gustavo H., and Benz, J. Philipp. Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition in Neurospora crassa. United States: N. p., 2019. Web. doi:10.3389/fmicb.2019.02317.
Horta, Maria Augusta C., Thieme, Nils, Gao, Yuqian, Burnum-Johnson, Kristin E., Nicora, Carrie D., Gritsenko, Marina A., Lipton, Mary S., Mohanraj, Karthikeyan, José de Assis, Leandro, Lin, Liangcai, Tian, Chaoguang, Braus, Gerhard H., Borkovich, Katherine A., Schmoll, Monika, Larrondo, Luis F., Samal, Areejit, Goldman, Gustavo H., & Benz, J. Philipp. Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition in Neurospora crassa. United States. doi:10.3389/fmicb.2019.02317.
Horta, Maria Augusta C., Thieme, Nils, Gao, Yuqian, Burnum-Johnson, Kristin E., Nicora, Carrie D., Gritsenko, Marina A., Lipton, Mary S., Mohanraj, Karthikeyan, José de Assis, Leandro, Lin, Liangcai, Tian, Chaoguang, Braus, Gerhard H., Borkovich, Katherine A., Schmoll, Monika, Larrondo, Luis F., Samal, Areejit, Goldman, Gustavo H., and Benz, J. Philipp. Fri . "Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition in Neurospora crassa". United States. doi:10.3389/fmicb.2019.02317. https://www.osti.gov/servlets/purl/1577974.
@article{osti_1577974,
title = {Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition in Neurospora crassa},
author = {Horta, Maria Augusta C. and Thieme, Nils and Gao, Yuqian and Burnum-Johnson, Kristin E. and Nicora, Carrie D. and Gritsenko, Marina A. and Lipton, Mary S. and Mohanraj, Karthikeyan and José de Assis, Leandro and Lin, Liangcai and Tian, Chaoguang and Braus, Gerhard H. and Borkovich, Katherine A. and Schmoll, Monika and Larrondo, Luis F. and Samal, Areejit and Goldman, Gustavo H. and Benz, J. Philipp},
abstractNote = {Fungal plant cell wall degradation processes are governed by complex regulatory mechanisms, allowing the organisms to adapt their metabolic program with high specificity to the substrate at hand. While the uptake of representative plant cell wall mono- and disaccharides is known to induce specific transcriptional and translational responses, the processes related to early signal reception and transduction are still enigmatic. A fast and reversible way of transmitting extracellular signals throughout the cell are protein phosphorylations, which could initiate adaptations of the fungal metabolism on a post-translational level. In an effort to elucidate how changes in the initial substrate recognition phase of Neurospora crassa affect the global phosphorylation pattern, phosphoproteomics was performed after a short (2 minute) induction period with several plant cell wall-related mono- and disaccharides. The MS/MS-based peptide analysis revealed a large number of proteins that are phosphorylated or de-phosphorylated in a substrate-specific manner. A protein-protein-interaction network was constructed based on the proteins identified by MS/MS. Using this network, putative interaction partners of several phosphorylated proteins of interest were determined. This led to the discovery of substrate-specific protein-interactions that might be involved in mediating the substrate recognition of N. crassa. Besides a high number of kinases, phosphatases and transcription factors to be affected by differential phosphorylation, our data demonstrate, for example, that the cAMP signaling pathway is heavily modified by substrate-specific phosphorylations, including the key component adenylate cyclase CR-1 as well as several G-protein-coupled receptors. In addition, four differentially phosphorylated F-Box proteins were identified in the phospho-proteome. When physiologically characterized using the respective gene deletion strains, Fbx-19 and Fbx-22 were found to be involved in carbon catabolite repression responses. Overall, these results improve our understanding of how fungi respond to environmental cues and provide novel insights into the mechanisms of sensory perception and signal transduction during lignocellulose degradation.},
doi = {10.3389/fmicb.2019.02317},
journal = {Frontiers in Microbiology},
number = ,
volume = 10,
place = {United States},
year = {2019},
month = {11}
}

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