Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete H ebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis
Abstract
Summary Extracellular proteins play crucial roles in the interaction between mycorrhizal fungi and their environment. Computational prediction and experimental detection allowed identification of 869 proteins constituting the exoproteome of Hebeloma cylindrosporum . Small secreted proteins ( SSP s) and carbohydrate‐active enzymes ( CAZ ymes) were the two major classes of extracellular proteins. Twenty‐eight per cent of the SSP s were secreted by free‐living mycelia and five of the 10 most abundant extracellular proteins were SSP s. By contrast, 63–75% of enzymes involved in nutrient acquisition were secreted. A total of 150 extracellular protein‐coding genes were differentially expressed between mycorrhizas and free‐living mycelia. SSP s were the most affected. External environmental conditions also affected expression of 199 exoproteome genes in mycorrhizas. SSP s displayed different patterns of regulation in response to presence of a host plant or other environmental signals. Several of the genes most overexpressed in the presence of organic matter encoded oxidoreductases. Hebeloma cylindrosporum has not fully lost its ancestral saprotrophic capacities but rather adapted them not to harm its hosts and to use soil organic nitrogen. The complex and divergent patterns of regulation of SSP s in response to a symbiotic partner and/or organic matter suggest various rolesmore »
- Authors:
-
- Ecologie Microbienne UMR CNRS 5557 USC INRA 1364 Université Lyon 1 Université de Lyon F‐69622 Villeurbanne France
- Proteomics Platform UMR5240 14 impasse Pierre Baizet BP 99163 F‐69263 Lyon Cedex 09 France
- INRA UMR 1136 INRA‐Université de Lorraine Interactions Arbres/Microorganismes INRA‐Nancy 54280 Champenoux France
- Centre National de la Recherche Scientifique UMR 7257 Aix‐Marseille Université 13288 Marseille Cedex 9 France
- US Department of Energy Joint Genome Institute Walnut Creek CA 94598 USA
- Biochimie et Physiologie Moléculaire des Plantes UMR 5004 CNRS/INRA/SupAgro/UM2 Place Viala Montpellier France
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1787127
- Grant/Contract Number:
- DE‐AC02‐05CH11231; AC02-05CH11231; ANR-11-607 LABX-0002-01
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 208 Journal Issue: 4; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Doré, Jeanne, Perraud, Marie, Dieryckx, Cindy, Kohler, Annegret, Morin, Emmanuelle, Henrissat, Bernard, Lindquist, Erika, Zimmermann, Sabine D., Girard, Vincent, Kuo, Alan, Grigoriev, Igor V., Martin, Francis, Marmeisse, Roland, and Gay, Gilles. Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete H ebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis. United Kingdom: N. p., 2015.
Web. doi:10.1111/nph.13546.
Doré, Jeanne, Perraud, Marie, Dieryckx, Cindy, Kohler, Annegret, Morin, Emmanuelle, Henrissat, Bernard, Lindquist, Erika, Zimmermann, Sabine D., Girard, Vincent, Kuo, Alan, Grigoriev, Igor V., Martin, Francis, Marmeisse, Roland, & Gay, Gilles. Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete H ebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis. United Kingdom. https://doi.org/10.1111/nph.13546
Doré, Jeanne, Perraud, Marie, Dieryckx, Cindy, Kohler, Annegret, Morin, Emmanuelle, Henrissat, Bernard, Lindquist, Erika, Zimmermann, Sabine D., Girard, Vincent, Kuo, Alan, Grigoriev, Igor V., Martin, Francis, Marmeisse, Roland, and Gay, Gilles. Tue .
"Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete H ebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis". United Kingdom. https://doi.org/10.1111/nph.13546.
@article{osti_1787127,
title = {Comparative genomics, proteomics and transcriptomics give new insight into the exoproteome of the basidiomycete H ebeloma cylindrosporum and its involvement in ectomycorrhizal symbiosis},
author = {Doré, Jeanne and Perraud, Marie and Dieryckx, Cindy and Kohler, Annegret and Morin, Emmanuelle and Henrissat, Bernard and Lindquist, Erika and Zimmermann, Sabine D. and Girard, Vincent and Kuo, Alan and Grigoriev, Igor V. and Martin, Francis and Marmeisse, Roland and Gay, Gilles},
abstractNote = {Summary Extracellular proteins play crucial roles in the interaction between mycorrhizal fungi and their environment. Computational prediction and experimental detection allowed identification of 869 proteins constituting the exoproteome of Hebeloma cylindrosporum . Small secreted proteins ( SSP s) and carbohydrate‐active enzymes ( CAZ ymes) were the two major classes of extracellular proteins. Twenty‐eight per cent of the SSP s were secreted by free‐living mycelia and five of the 10 most abundant extracellular proteins were SSP s. By contrast, 63–75% of enzymes involved in nutrient acquisition were secreted. A total of 150 extracellular protein‐coding genes were differentially expressed between mycorrhizas and free‐living mycelia. SSP s were the most affected. External environmental conditions also affected expression of 199 exoproteome genes in mycorrhizas. SSP s displayed different patterns of regulation in response to presence of a host plant or other environmental signals. Several of the genes most overexpressed in the presence of organic matter encoded oxidoreductases. Hebeloma cylindrosporum has not fully lost its ancestral saprotrophic capacities but rather adapted them not to harm its hosts and to use soil organic nitrogen. The complex and divergent patterns of regulation of SSP s in response to a symbiotic partner and/or organic matter suggest various roles in the biology of mycorrhizal fungi.},
doi = {10.1111/nph.13546},
journal = {New Phytologist},
number = 4,
volume = 208,
place = {United Kingdom},
year = {Tue Jul 14 00:00:00 EDT 2015},
month = {Tue Jul 14 00:00:00 EDT 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/nph.13546
https://doi.org/10.1111/nph.13546
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
The Mutualist Laccaria bicolor Expresses a Core Gene Regulon During the Colonization of Diverse Host Plants and a Variable Regulon to Counteract Host-Specific Defenses
journal, March 2015
- Plett, Jonathan M.; Tisserant, Emilie; Brun, Annick
- Molecular Plant-Microbe Interactions, Vol. 28, Issue 3
New Phytologist ? an evolving host for mycorrhizal research
journal, April 2007
- Martin, Francis; Slater, Holly
- New Phytologist, Vol. 174, Issue 2
Fungal Effector Proteins
journal, September 2009
- Stergiopoulos, Ioannis; de Wit, Pierre J. G. M.
- Annual Review of Phytopathology, Vol. 47, Issue 1
Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism
journal, December 2010
- Spanu, Pietro D.; Abbott, James C.; Amselem, Joelle
- Science, Vol. 330, Issue 6010
Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs
journal, December 2014
- Lindahl, Björn D.; Tunlid, Anders
- New Phytologist, Vol. 205, Issue 4
Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil
journal, February 2010
- Baldrian, Petr; Voříšková, Jana; Dobiášová, Petra
- Plant and Soil, Vol. 338, Issue 1-2
Locating proteins in the cell using TargetP, SignalP and related tools
journal, April 2007
- Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar
- Nature Protocols, Vol. 2, Issue 4
Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems
journal, April 2014
- Bödeker, Inga T. M.; Clemmensen, Karina E.; de Boer, Wietse
- New Phytologist, Vol. 203, Issue 1
Surface hydrophobin prevents immune recognition of airborne fungal spores
journal, August 2009
- Aimanianda, Vishukumar; Bayry, Jagadeesh; Bozza, Silvia
- Nature, Vol. 460, Issue 7259
Comparative proteomics of extracellular proteinsin vitro andin planta from the pathogenic fungusFusarium graminearum
journal, September 2007
- Paper, Janet M.; Scott-Craig, John S.; Adhikari, Neil D.
- PROTEOMICS, Vol. 7, Issue 17
Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes
journal, September 2010
- Danchin, Etienne G. J.; Rosso, Marie-Noëlle; Vieira, Paulo
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
The Botrytis cinerea early secretome
journal, June 2010
- Espino, José J.; Gutiérrez-Sánchez, Gerardo; Brito, Nélida
- PROTEOMICS, Vol. 10, Issue 16
Secretomes: The fungal strike force
journal, January 2013
- Girard, Vincent; Dieryckx, Cindy; Job, Claudette
- PROTEOMICS, Vol. 13, Issue 3-4
A Catalogue of the Effector Secretome of Plant Pathogenic Oomycetes
journal, September 2006
- Kamoun, Sophien
- Annual Review of Phytopathology, Vol. 44, Issue 1
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Characterization of a Lectin from Lactarius deterrimus (Research on the Possible Involvement of the Fungal Lectin in Recognition between Mushroom and Spruce during the Early Stages of Mycorrhizae Formation)
journal, February 1993
- Giollant, M.; Guillot, J.; Damez, M.
- Plant Physiology, Vol. 101, Issue 2
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011
- Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D.
- Current Biology, Vol. 21, Issue 14
FunSecKB: the Fungal Secretome KnowledgeBase
journal, January 2011
- Lum, G.; Min, X. J.
- Database, Vol. 2011, Issue 0
A Renaissance of Elicitors: Perception of Microbe-Associated Molecular Patterns and Danger Signals by Pattern-Recognition Receptors
journal, June 2009
- Boller, Thomas; Felix, Georg
- Annual Review of Plant Biology, Vol. 60, Issue 1
S URFACE A TTACHMENT AND P RE -P ENETRATION S TAGE D EVELOPMENT BY P LANT P ATHOGENIC F UNGI
journal, September 2001
- Tucker, Sara L.; Talbot, Nicholas J.
- Annual Review of Phytopathology, Vol. 39, Issue 1
Secretome of the Free-living Mycelium from the Ectomycorrhizal Basidiomycete Laccaria bicolor
journal, November 2011
- Vincent, Delphine; Kohler, Annegret; Claverol, Stephane
- Journal of Proteome Research, Vol. 11, Issue 1
Hydrophobins and Repellents: Proteins with Fundamental Roles in Fungal Morphogenesis
journal, February 1998
- Kershaw, Michael J.; Talbot, Nicholas J.
- Fungal Genetics and Biology, Vol. 23, Issue 1
The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry: Organic matter degradation by ectomycorrhizal fungi
journal, March 2012
- Rineau, Francois; Roth, Doris; Shah, Firoz
- Environmental Microbiology, Vol. 14, Issue 6
Small proteins of plant-pathogenic fungi secreted during host colonization
journal, December 2005
- Rep, Martijn
- FEMS Microbiology Letters, Vol. 253, Issue 1
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Structural aspects of ectomycorrhiza of Pinus pinaster (Ait.) Sol. formed by an IAA-overproducer mutant of Hebeloma cylindrosporum Romagnesi
journal, December 1994
- Gea, L.; Normand, L.; Vian, B.
- New Phytologist, Vol. 128, Issue 4
Forest habitat characteristics affect balance between sexual reproduction and clonal propagation of the ectomycorrhizal mushroom Hebeloma cylindrosporum
journal, October 2002
- Guidot, Alice; Gryta, Hervé; Gourbière, François
- Oikos, Vol. 99, Issue 1
The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi
journal, July 2011
- Eastwood, D. C.; Floudas, D.; Binder, M.
- Science, Vol. 333, Issue 6043, p. 762-765
Lectins as Plant Defense Proteins
journal, October 1995
- Peumans, W. J.; Van Damme, Ejm.
- Plant Physiology, Vol. 109, Issue 2
In Vitro Fruiting Under Controlled Conditions of the Ectomycorrhizal Fungus Hebeloma Cylindrosporum Associated with Pinus Pinaster
journal, March 1987
- Debaud, J. C.; Gay, G.
- New Phytologist, Vol. 105, Issue 3
Carbohydrate Metabolism During Morphogenesis of Coprinus lagopus (sensu Buller)
journal, January 1969
- Rao, P. S.; Niederpruem, D. J.
- Journal of Bacteriology, Vol. 100, Issue 3
The Nuclear Ribosomal DNA Intergenic Spacer as a Target Sequence To Study Intraspecific Diversity of the Ectomycorrhizal Basidiomycete Hebeloma cylindrosporum Directly on Pinus Root Systems
journal, March 1999
- Guidot, Alice; Lumini, Erica; Debaud, Jean-Claude
- Applied and Environmental Microbiology, Vol. 65, Issue 3
Pathways of unconventional protein secretion
journal, October 2010
- Nickel, Walter
- Current Opinion in Biotechnology, Vol. 21, Issue 5
Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes
journal, January 2011
- Plett, Jonathan M.; Martin, Francis
- Trends in Genetics, Vol. 27, Issue 1
Comparative Proteomic Analysis of Botrytis cinerea Secretome
journal, January 2009
- Shah, Punit; Atwood, James A.; Orlando, Ron
- Journal of Proteome Research, Vol. 8, Issue 3
Cladosporium fulvum Avr4 Protects Fungal Cell Walls Against Hydrolysis by Plant Chitinases Accumulating During Infection
journal, December 2006
- van den Burg, Harrold A.; Harrison, Stuart J.; Joosten, Matthieu H. A. J.
- Molecular Plant-Microbe Interactions, Vol. 19, Issue 12
Intraspecific variation in use of different organic nitrogen sources by the ectomycorrhizal fungus Hebeloma cylindrosporum
journal, August 2004
- Guidot, Alice; Verner, Marie-Christine; Debaud, Jean-Claude
- Mycorrhiza, Vol. 15, Issue 3
Non-conventional protein secretionin yeast
journal, January 2006
- Nombela, César; Gil, Concha; Chaffin, W. LaJean
- Trends in Microbiology, Vol. 14, Issue 1
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014
- Plett, J. M.; Daguerre, Y.; Wittulsky, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis
journal, November 2013
- Tisserant, E.; Malbreil, M.; Kuo, A.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
Unconventional protein secretion: an evolving mechanism
journal, May 2013
- Malhotra, Vivek
- The EMBO Journal, Vol. 32, Issue 12
Effector-triggered defence against apoplastic fungal pathogens
journal, August 2014
- Stotz, Henrik U.; Mitrousia, Georgia K.; de Wit, Pierre J. G. M.
- Trends in Plant Science, Vol. 19, Issue 8
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015
- Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
- Nature Genetics, Vol. 47, Issue 4
Oomycete and fungal effector entry, a microbial Trojan horse
journal, November 2011
- Kale, Shiv D.
- New Phytologist, Vol. 193, Issue 4
Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment
journal, November 2014
- Veneault-Fourrey, Claire; Commun, Carine; Kohler, Annegret
- Fungal Genetics and Biology, Vol. 72
The secretome of the maize pathogen Ustilago maydis
journal, August 2008
- Mueller, Olaf; Kahmann, Regine; Aguilar, Guillermo
- Fungal Genetics and Biology, Vol. 45
Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus
journal, June 2013
- Rineau, F.; Shah, F.; Smits, M. M.
- The ISME Journal, Vol. 7, Issue 10
MPG1 Encodes a Fungal Hydrophobin Involved in Surface Interactions during Infection-Related Development of Magnaporthe grisea
journal, June 1996
- Talbot, Nicholas J.; Kershaw, Michael J.; Wakley, Gavin E.
- The Plant Cell, Vol. 8, Issue 6
A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy
journal, July 2011
- Kloppholz, Silke; Kuhn, Hannah; Requena, Natalia
- Current Biology, Vol. 21, Issue 14
Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens
journal, August 2009
- Ellis, Jeffrey G.; Rafiqi, Maryam; Gan, Pamela
- Current Opinion in Plant Biology, Vol. 12, Issue 4
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
Unconventional Mechanisms of Protein Transport to the Cell Surface of Eukaryotic Cells
journal, November 2008
- Nickel, Walter; Seedorf, Matthias
- Annual Review of Cell and Developmental Biology, Vol. 24, Issue 1
Common molecular mechanisms of symbiosis and pathogenesis
journal, May 2000
- Hentschel, Ute; Steinert, Michael; Hacker, Jörg
- Trends in Microbiology, Vol. 8, Issue 5
Analytical and computational approaches to define the Aspergillus niger secretome
journal, March 2009
- Tsang, Adrian; Butler, Gregory; Powlowski, Justin
- Fungal Genetics and Biology, Vol. 46, Issue 1, p. S153-S160
A Fungal Conserved Gene from the Basidiomycete Hebeloma cylindrosporum Is Essential for Efficient Ectomycorrhiza Formation
journal, October 2014
- Doré, Jeanne; Marmeisse, Roland; Combier, Jean-Philippe
- Molecular Plant-Microbe Interactions®, Vol. 27, Issue 10
The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots
journal, March 2010
- Downie, J. Allan
- FEMS Microbiology Reviews, Vol. 34, Issue 2
An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data
journal, January 2010
- Braaksma, Machtelt; Martens-Uzunova, Elena S.; Punt, Peter J.
- BMC Genomics, Vol. 11, Issue 1
Unconventional protein secretion
journal, October 2012
- Ding, Yu; Wang, Juan; Wang, Junqi
- Trends in Plant Science, Vol. 17, Issue 10
Novel findings on the role of signal exchange in arbuscular and ectomycorrhizal symbioses
journal, September 2014
- Raudaskoski, Marjatta; Kothe, Erika
- Mycorrhiza, Vol. 25, Issue 4
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition
journal, February 2013
- Talbot, Jennifer M.; Bruns, Thomas D.; Smith, Dylan P.
- Soil Biology and Biochemistry, Vol. 57