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Title: Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor

Abstract

Background: Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus Laccaria bicolor. Results: We curated the L. bicolor gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The L. bicolor core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungalmore » invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of L. bicolor and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs). Conclusions: Transcriptional regulators required for ECM symbiosis development in L. bicolor have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [2];  [2];  [1];  [1];  [1]
  1. Univ. de Lorraine, Champenoux (France). Interactions Arbres/ Microorganismes, Laboratoire d’Excellence ARBRE; Univ. de Lorraine, Nancy (France). Interactions Arbres/Microorganismes, Laboratoire d’Excellence ARBRE
  2. Univ. degli Studi di Parma (Italy). Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1626809
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 18; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Biotechnology & Applied Microbiology; Genetics & Heredity; Transcription factors; symbiosis; secreted proteins; transcriptional activator trap assay; yeast; transcriptome; ectomycorrhiza development

Citation Formats

Daguerre, Y., Levati, E., Ruytinx, J., Tisserant, E., Morin, E., Kohler, A., Montanini, B., Ottonello, S., Brun, A., Veneault-Fourrey, C., and Martin, F. Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor. United States: N. p., 2017. Web. doi:10.1186/s12864-017-4114-7.
Daguerre, Y., Levati, E., Ruytinx, J., Tisserant, E., Morin, E., Kohler, A., Montanini, B., Ottonello, S., Brun, A., Veneault-Fourrey, C., & Martin, F. Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor. United States. https://doi.org/10.1186/s12864-017-4114-7
Daguerre, Y., Levati, E., Ruytinx, J., Tisserant, E., Morin, E., Kohler, A., Montanini, B., Ottonello, S., Brun, A., Veneault-Fourrey, C., and Martin, F. 2017. "Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor". United States. https://doi.org/10.1186/s12864-017-4114-7. https://www.osti.gov/servlets/purl/1626809.
@article{osti_1626809,
title = {Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor},
author = {Daguerre, Y. and Levati, E. and Ruytinx, J. and Tisserant, E. and Morin, E. and Kohler, A. and Montanini, B. and Ottonello, S. and Brun, A. and Veneault-Fourrey, C. and Martin, F.},
abstractNote = {Background: Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus Laccaria bicolor. Results: We curated the L. bicolor gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The L. bicolor core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of L. bicolor and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs). Conclusions: Transcriptional regulators required for ECM symbiosis development in L. bicolor have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.},
doi = {10.1186/s12864-017-4114-7},
url = {https://www.osti.gov/biblio/1626809}, journal = {BMC Genomics},
issn = {1471-2164},
number = 1,
volume = 18,
place = {United States},
year = {Mon Sep 18 00:00:00 EDT 2017},
month = {Mon Sep 18 00:00:00 EDT 2017}
}

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