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Title: Expanding genomics of mycorrhizal symbiosis

Abstract

The mycorrhizal symbiosis between soil fungi and plant roots is a ubiquitous mutualism that plays key roles in plant nutrition, soil health, and carbon cycling. The symbiosis evolved repeatedly and independently as multiple morphotypes [e.g., arbuscular mycorrhizae (AM), ectomycorrhizal (ECM)] in multiple fungal clades (e.g., phyla Glomeromycota, Ascomycota, Basidiomycota). The accessibility and cultivability of many mycorrhizal partners make them ideal models for symbiosis studies. Alongside molecular, physiological, and ecological investigations, sequencing led to the first three mycorrhizal fungal genomes, representing two morphotypes and three phyla. The genome of the ECM basidiomycete Laccaria bicolor showed that the mycorrhizal lifestyle can evolve through loss of plant cell wall-degrading enzymes (PCWDEs) and expansion of lineage-specific gene families such as short secreted protein (SSP) effectors. The genome of the ECM ascomycete Tuber melanosporum showed that the ECM type can evolve without expansion of families as in Laccaria, and thus a different set of symbiosis genes. The genome of the AM glomeromycete Rhizophagus irregularis showed that despite enormous phylogenetic distance and morphological difference from the other two fungi, symbiosis can involve similar solutions as symbiosis-induced SSPs and loss of PCWDEs. The three genomes provide a solid base for addressing fundamental questions about the nature andmore » role of a vital mutualism.« less

Authors:
 [1];  [2];  [2];  [1]
  1. United States Department of Energy Joint Genome Institute, Walnut Creek, CA (United States)
  2. Universite de Lorraine, Nancy (France). Lab. of Excellence for Advanced Research on the Biology of Tree and Forest Ecosystems
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1213050
Alternate Identifier(s):
OSTI ID: 1424218
Report Number(s):
LBNL-177928
Journal ID: ISSN 1664-302X
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; mycorrhizae; Laccaria; Tuber; Rhizophagus; Glomus

Citation Formats

Kuo, Alan, Kohler, Annegret, Martin, Francis M., and Grigoriev, Igor V. Expanding genomics of mycorrhizal symbiosis. United States: N. p., 2014. Web. doi:10.3389/fmicb.2014.00582.
Kuo, Alan, Kohler, Annegret, Martin, Francis M., & Grigoriev, Igor V. Expanding genomics of mycorrhizal symbiosis. United States. https://doi.org/10.3389/fmicb.2014.00582
Kuo, Alan, Kohler, Annegret, Martin, Francis M., and Grigoriev, Igor V. Tue . "Expanding genomics of mycorrhizal symbiosis". United States. https://doi.org/10.3389/fmicb.2014.00582. https://www.osti.gov/servlets/purl/1213050.
@article{osti_1213050,
title = {Expanding genomics of mycorrhizal symbiosis},
author = {Kuo, Alan and Kohler, Annegret and Martin, Francis M. and Grigoriev, Igor V.},
abstractNote = {The mycorrhizal symbiosis between soil fungi and plant roots is a ubiquitous mutualism that plays key roles in plant nutrition, soil health, and carbon cycling. The symbiosis evolved repeatedly and independently as multiple morphotypes [e.g., arbuscular mycorrhizae (AM), ectomycorrhizal (ECM)] in multiple fungal clades (e.g., phyla Glomeromycota, Ascomycota, Basidiomycota). The accessibility and cultivability of many mycorrhizal partners make them ideal models for symbiosis studies. Alongside molecular, physiological, and ecological investigations, sequencing led to the first three mycorrhizal fungal genomes, representing two morphotypes and three phyla. The genome of the ECM basidiomycete Laccaria bicolor showed that the mycorrhizal lifestyle can evolve through loss of plant cell wall-degrading enzymes (PCWDEs) and expansion of lineage-specific gene families such as short secreted protein (SSP) effectors. The genome of the ECM ascomycete Tuber melanosporum showed that the ECM type can evolve without expansion of families as in Laccaria, and thus a different set of symbiosis genes. The genome of the AM glomeromycete Rhizophagus irregularis showed that despite enormous phylogenetic distance and morphological difference from the other two fungi, symbiosis can involve similar solutions as symbiosis-induced SSPs and loss of PCWDEs. The three genomes provide a solid base for addressing fundamental questions about the nature and role of a vital mutualism.},
doi = {10.3389/fmicb.2014.00582},
journal = {Frontiers in Microbiology},
number = ,
volume = 5,
place = {United States},
year = {Tue Nov 04 00:00:00 EST 2014},
month = {Tue Nov 04 00:00:00 EST 2014}
}

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Cited by: 23 works
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Works referenced in this record:

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Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
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journal, July 2012


Harnessing ectomycorrhizal genomics for ecological insights
journal, August 2009


A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy
journal, July 2011


Genomic profiling of carbohydrate metabolism in the ectomycorrhizal fungus Tuber melanosporum
journal, October 2010


Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs
journal, January 2001


The Ectomycorrhizal Fungus Laccaria bicolor Stimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling
journal, October 2009

  • Felten, Judith; Kohler, Annegret; Morin, Emmanuelle
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Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum
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Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus
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Asynchronous origins of ectomycorrhizal clades of Agaricales
journal, December 2011

  • Ryberg, Martin; Matheny, P. Brandon
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  • DOI: 10.1098/rspb.2011.2428

Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus
journal, November 2004


Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes
journal, January 2011


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
  • DOI: 10.1021/pr200895f

Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria bicolor
journal, March 2012

  • Plett, Jonathan M.; Gibon, Julien; Kohler, Annegret
  • Fungal Genetics and Biology, Vol. 49, Issue 3
  • DOI: 10.1016/j.fgb.2012.01.002

Genome-wide analysis of cell wall-related genes in Tuber melanosporum
journal, April 2012


Agrobacterium-mediated transformation of the ectomycorrhizal symbiont Laccaria bicolor S238N
journal, August 2005


Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages
journal, September 2009


Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome
journal, January 2011

  • Larsen, Peter E.; Sreedasyam, Avinash; Trivedi, Geetika
  • BMC Systems Biology, Vol. 5, Issue 1
  • DOI: 10.1186/1752-0509-5-70

Imaging mycorrhizal fungal transformants that express EGFP during ericoid endosymbiosis
journal, June 2007


The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N
journal, October 2008


Survey and analysis of simple sequence repeats in the Laccaria bicolor genome, with development of microsatellite markers
journal, December 2010


Characterization of Transposable Elements in the Ectomycorrhizal Fungus Laccaria bicolor
journal, August 2012


Works referencing / citing this record:

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

Molecular Signalling During the Ectomycorrhizal Symbiosis
book, January 2019


Fungal evolution: major ecological adaptations and evolutionary transitions
journal, April 2019

  • Naranjo‐Ortiz, Miguel A.; Gabaldón, Toni
  • Biological Reviews
  • DOI: 10.1111/brv.12510

Tracing the origin and evolution of pseudokinases across the tree of life
journal, April 2019