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Title: Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins

Abstract

Fungi are major players in the carbon cycle in forest ecosystems due to the wide range of interactions they have with plants either through soil degradation processes by litter decayers or biotrophic interactions with pathogenic and ectomycorrhizal symbionts. Secretion of fungal proteins mediates these interactions by allowing the fungus to interact with its environment and/or host. Ectomycorrhizal (ECM) symbiosis independently appeared several times throughout evolution and involves approximately 80% of trees. Despite extensive physiological studies on ECM symbionts, little is known about the composition and specificities of their secretomes. In this study, we used a bioinformatics pipeline to predict and analyze the secretomes of 49 fungal species, including 11 ECM fungi, wood and soil decayers and pathogenic fungi to tackle the following questions: (1) Are there differences between the secretomes of saprophytic and ECM fungi? (2) Are small-secreted proteins (SSPs) more abundant in biotrophic fungi than in saprophytic fungi? and (3) Are there SSPs shared between ECM, saprotrophic and pathogenic fungi? We showed that the number of predicted secreted proteins is similar in the surveyed species, independently of their lifestyle. The secretome from ECM fungi is characterized by a restricted number of secreted CAZymes, but their repertoires of secreted proteasesmore » and lipases are similar to those of saprotrophic fungi. Focusing on SSPs, we showed that the secretome of ECM fungi is enriched in SSPs compared with other species. Most of the SSPs are coded by orphan genes with no known PFAM domain or similarities to known sequences in databases. Finally, based on the clustering analysis, we identified shared- and lifestyle-specific SSPs between saprotrophic and ECM fungi. The presence of SSPs is not limited to fungi interacting with living plants as the genome of saprotrophic fungi also code for numerous SSPs. As a result, ECM fungi shared lifestyle-specific SSPs likely involved in symbiosis that are good candidates for further functional analyses.« less

Authors:
 [1];  [2];  [2];  [1]
  1. Univ. de Lorraine, Vandoeuvre-les-Nancy (France); Institut National de la Recherche Agronomique, Champenoux (France)
  2. Institut National de la Recherche Agronomique, Champenoux (France)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1241128
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ectomycorrhizal; saprotrophs; secretomics; small-secreted proteins; symbiosis; secretomes

Citation Formats

Pellegrin, Clement, Morin, Emmanuelle, Martin, Francis M., and Veneault-Fourrey, Claire. Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.01278.
Pellegrin, Clement, Morin, Emmanuelle, Martin, Francis M., & Veneault-Fourrey, Claire. Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins. United States. https://doi.org/10.3389/fmicb.2015.01278
Pellegrin, Clement, Morin, Emmanuelle, Martin, Francis M., and Veneault-Fourrey, Claire. Wed . "Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins". United States. https://doi.org/10.3389/fmicb.2015.01278. https://www.osti.gov/servlets/purl/1241128.
@article{osti_1241128,
title = {Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins},
author = {Pellegrin, Clement and Morin, Emmanuelle and Martin, Francis M. and Veneault-Fourrey, Claire},
abstractNote = {Fungi are major players in the carbon cycle in forest ecosystems due to the wide range of interactions they have with plants either through soil degradation processes by litter decayers or biotrophic interactions with pathogenic and ectomycorrhizal symbionts. Secretion of fungal proteins mediates these interactions by allowing the fungus to interact with its environment and/or host. Ectomycorrhizal (ECM) symbiosis independently appeared several times throughout evolution and involves approximately 80% of trees. Despite extensive physiological studies on ECM symbionts, little is known about the composition and specificities of their secretomes. In this study, we used a bioinformatics pipeline to predict and analyze the secretomes of 49 fungal species, including 11 ECM fungi, wood and soil decayers and pathogenic fungi to tackle the following questions: (1) Are there differences between the secretomes of saprophytic and ECM fungi? (2) Are small-secreted proteins (SSPs) more abundant in biotrophic fungi than in saprophytic fungi? and (3) Are there SSPs shared between ECM, saprotrophic and pathogenic fungi? We showed that the number of predicted secreted proteins is similar in the surveyed species, independently of their lifestyle. The secretome from ECM fungi is characterized by a restricted number of secreted CAZymes, but their repertoires of secreted proteases and lipases are similar to those of saprotrophic fungi. Focusing on SSPs, we showed that the secretome of ECM fungi is enriched in SSPs compared with other species. Most of the SSPs are coded by orphan genes with no known PFAM domain or similarities to known sequences in databases. Finally, based on the clustering analysis, we identified shared- and lifestyle-specific SSPs between saprotrophic and ECM fungi. The presence of SSPs is not limited to fungi interacting with living plants as the genome of saprotrophic fungi also code for numerous SSPs. As a result, ECM fungi shared lifestyle-specific SSPs likely involved in symbiosis that are good candidates for further functional analyses.},
doi = {10.3389/fmicb.2015.01278},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Wed Nov 18 00:00:00 EST 2015},
month = {Wed Nov 18 00:00:00 EST 2015}
}

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Soil biodiversity and soil community composition determine ecosystem multifunctionality
journal, March 2014

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Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014

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Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
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Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments
journal, August 2007


CD-HIT Suite: a web server for clustering and comparing biological sequences
journal, January 2010


Genome-Wide Analysis in Three Fusarium Pathogens Identifies Rapidly Evolving Chromosomes and Genes Associated with Pathogenicity
journal, May 2015

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  • Genome Biology and Evolution, Vol. 7, Issue 6
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Mastering ectomycorrhizal symbiosis: the impact of carbohydrates
journal, February 2008


Independent Subtilases Expansions in Fungi Associated with Animals
journal, July 2011

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journal, May 2011

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MycoCosm portal: gearing up for 1000 fungal genomes
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Asynchronous origins of ectomycorrhizal clades of Agaricales
journal, December 2011

  • Ryberg, Martin; Matheny, P. Brandon
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1735
  • DOI: 10.1098/rspb.2011.2428

Effector Biology of Plant-Associated Organisms: Concepts and Perspectives
journal, January 2012

  • Win, J.; Chaparro-Garcia, A.; Belhaj, K.
  • Cold Spring Harbor Symposia on Quantitative Biology, Vol. 77, Issue 0
  • DOI: 10.1101/sqb.2012.77.015933

Secreted Fungal Effector Lipase Releases Free Fatty Acids to Inhibit Innate Immunity-Related Callose Formation during Wheat Head Infection
journal, March 2014

  • Blümke, Antje; Falter, Christian; Herrfurth, Cornelia
  • Plant Physiology, Vol. 165, Issue 1
  • DOI: 10.1104/pp.114.236737

Functional Soil Microbiome: Belowground Solutions to an Aboveground Problem
journal, July 2014

  • Lakshmanan, V.; Selvaraj, G.; Bais, H. P.
  • PLANT PHYSIOLOGY, Vol. 166, Issue 2
  • DOI: 10.1104/pp.114.245811

Small Signaling Peptides in Arabidopsis Development: How Cells Communicate Over a Short Distance
journal, August 2012


A phylogenomic approach to reconstructing the diversification of serine proteases in fungi
journal, November 2004


The molecular components of the extracellular protein-degradation pathways of the ectomycorrhizal fungus Paxillus involutus
journal, July 2013

  • Shah, Firoz; Rineau, Francois; Canbäck, Björn
  • New Phytologist, Vol. 200, Issue 3
  • DOI: 10.1111/nph.12425

Forests trapped in nitrogen limitation - an ecological market perspective on ectomycorrhizal symbiosis
journal, May 2014

  • Franklin, Oskar; Näsholm, Torgny; Högberg, Peter
  • New Phytologist, Vol. 203, Issue 2
  • DOI: 10.1111/nph.12840

The danger of mycorrhizal traps?
journal, June 2014

  • Kuyper, Thomas W.; Kiers, E. Toby
  • New Phytologist, Vol. 203, Issue 2
  • DOI: 10.1111/nph.12883

Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs
journal, December 2014

  • Lindahl, Björn D.; Tunlid, Anders
  • New Phytologist, Vol. 205, Issue 4
  • DOI: 10.1111/nph.13201

Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses
journal, April 2015

  • Garcia, Kevin; Delaux, Pierre‐Marc; Cope, Kevin R.
  • New Phytologist, Vol. 208, Issue 1
  • DOI: 10.1111/nph.13423

The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi
journal, July 2011


The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012


Abolishing Cell Wall Glycosylphosphatidylinositol-Anchored Proteins in Candida albicans Enhances Recognition by Host Dectin-1
journal, April 2015

  • Shen, Hui; Chen, Si Min; Liu, Wei
  • Infection and Immunity, Vol. 83, Issue 7
  • DOI: 10.1128/iai.00097-15

Fungal Effectors and Plant Susceptibility
journal, April 2015


Fungal Effector Proteins
journal, September 2009


Evolution of a subtilisin-like protease gene family in the grass endophytic fungus Epichloë festucae
journal, January 2009

  • Bryant, Michelle K.; Schardl, Christopher L.; Hesse, Uljana
  • BMC Evolutionary Biology, Vol. 9, Issue 1
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Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi
journal, January 2014


Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation
journal, January 2014

  • Krijger, Jorrit-Jan; Thon, Michael R.; Deising, Holger B.
  • BMC Genomics, Vol. 15, Issue 1
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Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013

  • Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
  • Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
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Using Hierarchical Clustering of Secreted Protein Families to Classify and Rank Candidate Effectors of Rust Fungi
journal, January 2012


The Irreversible Loss of a Decomposition Pathway Marks the Single Origin of an Ectomycorrhizal Symbiosis
journal, July 2012


Carbohydrate-Active Enzymes in Pythium and Their Role in Plant Cell Wall and Storage Polysaccharide Degradation
journal, September 2013


Microbial control over carbon cycling in soil
journal, January 2012


Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling
journal, June 2014


Works referencing / citing this record:

Molecular Signalling During the Ectomycorrhizal Symbiosis
book, January 2019


Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016

  • Martin, Francis; Kohler, Annegret; Murat, Claude
  • Nature Reviews Microbiology, Vol. 14, Issue 12
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A role for small secreted proteins (SSPs) in a saprophytic fungal lifestyle: Ligninolytic enzyme regulation in Pleurotus ostreatus
journal, November 2017


Transcriptomic atlas of mushroom development reveals conserved genes behind complex multicellularity in fungi
journal, March 2019

  • Krizsán, Krisztina; Almási, Éva; Merényi, Zsolt
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 15
  • DOI: 10.1073/pnas.1817822116

Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis
journal, July 2019

  • Pellegrin, Clément; Daguerre, Yohann; Ruytinx, Joske
  • Environmental Microbiology, Vol. 21, Issue 10
  • DOI: 10.1111/1462-2920.14727

Secretion of small proteins is species-specific within Aspergillus sp
journal, May 2016

  • Valette, Nicolas; Benoit-Gelber, Isabelle; Falco, Marcos Di
  • Microbial Biotechnology, Vol. 10, Issue 2
  • DOI: 10.1111/1751-7915.12361

A new promising phylogenetic marker to study the diversity of fungal communities: The Glycoside Hydrolase 63 gene
journal, May 2017

  • Pérez-Izquierdo, L.; Morin, E.; Maurice, J. P.
  • Molecular Ecology Resources, Vol. 17, Issue 6
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Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists
journal, January 2018

  • Martino, Elena; Morin, Emmanuelle; Grelet, Gwen-Aëlle
  • New Phytologist, Vol. 217, Issue 3
  • DOI: 10.1111/nph.14974

Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis?
journal, May 2018

  • Perotto, Silvia; Daghino, Stefania; Martino, Elena
  • New Phytologist, Vol. 220, Issue 4
  • DOI: 10.1111/nph.15218

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis
journal, May 2018

  • Lanfranco, Luisa; Fiorilli, Valentina; Gutjahr, Caroline
  • New Phytologist, Vol. 220, Issue 4
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Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota
journal, January 2019

  • Chang, Ying; Desirò, Alessandro; Na, Hyunsoo
  • New Phytologist, Vol. 222, Issue 1
  • DOI: 10.1111/nph.15613

Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina
journal, February 2019

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  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15687

Comparative genomics reveals unique wood‐decay strategies and fruiting body development in the Schizophyllaceae
journal, June 2019

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  • New Phytologist, Vol. 224, Issue 2
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Manipulating the Expression of Small Secreted Protein 1 (Ssp1) Alters Patterns of Development and Metabolism in the White-Rot Fungus Pleurotus ostreatus
journal, May 2019

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  • Applied and Environmental Microbiology, Vol. 85, Issue 15
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Apophysomyces variabilis: draft genome sequence and comparison of predictive virulence determinants with other medically important Mucorales
journal, September 2017

  • Prakash, Hariprasath; Rudramurthy, Shivaprakash Mandya; Gandham, Prasad S.
  • BMC Genomics, Vol. 18, Issue 1
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The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata
journal, July 2019


Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis
journal, December 2019


Trees, fungi and bacteria: tripartite metatranscriptomics of a root microbiome responding to soil contamination
journal, March 2018


Arabidopsis thaliana responds to colonisation of Piriformospora indica by secretion of symbiosis-specific proteins
journal, December 2018


Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response
journal, April 2016


Secretome Analysis from the Ectomycorrhizal Ascomycete Cenococcum geophilum
journal, February 2018

  • de Freitas Pereira, Maíra; Veneault-Fourrey, Claire; Vion, Patrice
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.00141

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics
journal, January 2020

  • Vincent, Delphine; Rafiqi, Maryam; Job, Dominique
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.01626

Laccaria bicolor MiSSP8 is a small-secreted protein decisive for the establishment of the ectomycorrhizal symbiosis
journal, May 2019

  • Pellegrin, Cl??ment; Daguerre, Yohann; Ruytinx, Joske
  • Environmental Microbiology
  • DOI: 10.1101/218131

The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata
text, January 2019

  • Armaleo, Daniele; Müller, Olaf; Lutzoni, François
  • BioMed Central
  • DOI: 10.14288/1.0380051

Orchids and their mycorrhizal fungi: an insufficiently explored relationship
journal, January 2020

  • Favre-Godal, Quentin; Gourguillon, Lorène; Lordel-Madeleine, Sonia
  • Mycorrhiza, Vol. 30, Issue 1
  • DOI: 10.1007/s00572-020-00934-2

The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata
text, January 2019

  • Daniele, Armaleo,; Olaf, Müller,; François, Lutzoni,
  • BioMed Central
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Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita
journal, September 2018

  • Hess, Jaqueline; Skrede, Inger; Chaib De Mares, Maryam
  • Molecular Biology and Evolution
  • DOI: 10.1093/molbev/msy179

Secretion of small proteins is species-specific within Aspergillus sp
journal, May 2016

  • Valette, Nicolas; Benoit-Gelber, Isabelle; Falco, Marcos Di
  • Microbial Biotechnology, Vol. 10, Issue 2
  • DOI: 10.1111/1751-7915.12361

The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata
journal, July 2019


Trees, fungi and bacteria: tripartite metatranscriptomics of a root microbiome responding to soil contamination
journal, March 2018


Recent Insights on Biological and Ecological Aspects of Ectomycorrhizal Fungi and Their Interactions
journal, February 2018


The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics
journal, January 2020

  • Vincent, Delphine; Rafiqi, Maryam; Job, Dominique
  • Frontiers in Plant Science, Vol. 10
  • DOI: 10.3389/fpls.2019.01626