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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Microbiol. | doi: 10.3389/fmicb.2019.02317

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

 Maria A. Crivelente Horta1, Nils Thieme1,  Yuqian Gao2,  Kristin E. Burnum-Johnson2, Carrie D. Nicora2, Mariana A. Gritsenko2, Mary Lipton3, Karthikeyan Mohanraj4,  Leandro J. de Assis5,  Liangcai Lin6,  Chaoguang Tian6,  Gerhard H. Braus7, 8,  Katherine A. Borkovich9,  Monika Schmoll10, Luis F. Larrondo11,  Areejit Samal12,  Gustavo H. Goldman5, 13 and  J. Philipp Benz1, 13*
  • 1Holzforschung München, TUM School of Life Sciences Weihenstephan, Technical University of Munich, Germany
  • 2Biological Sciences Division, Pacific Northwest National Laboratory (DOE), United States
  • 3The Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory (DOE), United States
  • 4Homi Bhabha National Institute, Institute of Mathematical Sciences, Chennai, India
  • 5Faculdade de Ciências Farmacêuticas de Ribeirão Preto, University of São Paulo, Brazil
  • 6Chinese Academy of Sciences, Tianjin Institute of Industrial Biotechnology (CAS), China
  • 7Department of Molecular Microbiology and Genetics, Institute of Microbiology and Genetics, University of Göttingen, Germany
  • 8Göttingen Center for Molecular Biosciences, University of Göttingen, Germany
  • 9Department of Microbiology and Plant Pathology, Institute for Integrative Genome Biology, University of California, Riverside, United States
  • 10Center for Health and Bioresources, Austrian Institute of Technology (AIT), Austria
  • 11Millennium Institute for Integrative Biology (iBio), Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Pontifical Catholic University of Chile, Chile
  • 12Homi Bhabha National Institute, Institute of Mathematical Sciences, India
  • 13Institute for Advanced Study, Technical University of Munich, Germany

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 available substrates. 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 remain largely unkown. A fast and reversible way of signal transmission are post-translational protein modifications, such as phosphorylations, which could initiate rapid adaptations of the fungal metabolism to a new condition. To elucidate how changes in the initial substrate recognition phase of Neurospora crassa affect the global phosphorylation pattern, phospho-proteomics 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 large-scale substrate-specific protein phosphorylation and de-phosphorylations. Using the proteins identified by MS/MS, a protein-protein-interaction (PPI) network was constructed. The differential phosphorylation of a large number of kinases, phosphatases and transcription factors indicate the participation of many known signaling pathways, including circadian responses, two-component regulatory systems, MAP kinases as well as the cAMP-dependent and heterotrimeric G-protein pathways. Adenylate cyclase, a key component of the cAMP pathway, was identified as a potential hub for carbon source-specific differential protein interactions. In addition, four phosphorylated F-Box proteins were identified, two of which, Fbx-19 and Fbx-22, were found to be involved in carbon catabolite repression responses. Overall, these results provide unprecedented and detailed insights into a so far less well known stage of the fungal response to environmental cues and allow to better elucidate the molecular mechanisms of sensory perception and signal transduction during plant cell wall degradation.

Keywords: Neurospora crassa, Fungi, Phosphorylation, Proteomics, substrate recognition, Signal Transduction, Lignocellulose degradation

Received: 15 May 2019; Accepted: 23 Sep 2019.

Copyright: © 2019 Crivelente Horta, Thieme, Gao, Burnum-Johnson, Nicora, Gritsenko, Lipton, Mohanraj, de Assis, Lin, Tian, Braus, Borkovich, Schmoll, Larrondo, Samal, Goldman and Benz. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. J. Philipp Benz, Technical University of Munich, Holzforschung München, TUM School of Life Sciences Weihenstephan, Munich, 80333, Bavaria, Germany, benz@hfm.tum.de