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Title: Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates

Abstract

The family Russulaceae is considered an iconic lineage of mostly mushroom-forming basidiomycetes due to their importance as edible mushrooms in many parts of the world, and their ubiquity as ectomycorrhizal symbionts in both temperate and tropical forested biomes. Although much research has been focused on this group, a comprehensive or cohesive synthesis by which to understand the functional diversity of the group has yet to develop. Interest in ectomycorrhizal fungi, of which Russulaceae is a key lineage, is prodigious due to the important roles they play as plant root mutualists in ecosystem functioning, global carbon sequestration, and a potential role in technology development toward environmental sustainability. As one of the most species-diverse ectomycorrhizal lineages, the Russulaceae has recently been the focus of a dense sampling and genome sequencing initiative with the Joint Genome Institute aimed at untangling their functional roles and testing whether functional niche specialization exists for independent lineages of ectomycorrhizal fungi. In this paper, we present a review of important studies on this group to contextualize what we know about its members' evolutionary history and ecosystem functions, as well as to generate hypotheses establishing the Russulaceae as a valuable experimental system.

Authors:
ORCiD logo [1];  [2];  [2]; ORCiD logo [3]; ORCiD logo [4];  [5]; ORCiD logo [6]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Ecology and Evolutionary Biology; National Inst. for Agricultural Research (INRA) and Univ. of Lorraine, Champenoux (France). Lab. ARBRE (Advanced Research on the Biology of Tree and Forest Ecosystems)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  3. Univ. of Helsinki (Finland). Finnish Museum of Natural History
  4. National Inst. for Agricultural Research (INRA) and Univ. of Lorraine, Champenoux (France). Lab. ARBRE (Advanced Research on the Biology of Tree and Forest Ecosystems)
  5. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Ecology and Evolutionary Biology
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry and Cellular and Molecular Biology
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States); National Inst. for Agricultural Research (INRA) and Univ. of Lorraine, Champenoux (France)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Workforce Development for Teachers and Scientists (WDTS); National Science Foundation (NSF); National Agency for Research (ANR) (France)
OSTI Identifier:
1474699
Alternate Identifier(s):
OSTI ID: 1418720
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231; SC0014664; DEB-1501293; ANR-11-LABX-0002-01
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 218; Journal Issue: 1; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; decomposition; functional diversity; fungal niche; secondary metabolism; symbiosis

Citation Formats

Looney, Brian P., Meidl, Peter, Piatek, Marek J., Miettinen, Otto, Martin, Francis M., Matheny, P. Brandon, and Labbé, Jessy L. Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates. United States: N. p., 2018. Web. https://doi.org/10.1111/nph.15001.
Looney, Brian P., Meidl, Peter, Piatek, Marek J., Miettinen, Otto, Martin, Francis M., Matheny, P. Brandon, & Labbé, Jessy L. Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates. United States. https://doi.org/10.1111/nph.15001
Looney, Brian P., Meidl, Peter, Piatek, Marek J., Miettinen, Otto, Martin, Francis M., Matheny, P. Brandon, and Labbé, Jessy L. Tue . "Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates". United States. https://doi.org/10.1111/nph.15001. https://www.osti.gov/servlets/purl/1474699.
@article{osti_1474699,
title = {Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates},
author = {Looney, Brian P. and Meidl, Peter and Piatek, Marek J. and Miettinen, Otto and Martin, Francis M. and Matheny, P. Brandon and Labbé, Jessy L.},
abstractNote = {The family Russulaceae is considered an iconic lineage of mostly mushroom-forming basidiomycetes due to their importance as edible mushrooms in many parts of the world, and their ubiquity as ectomycorrhizal symbionts in both temperate and tropical forested biomes. Although much research has been focused on this group, a comprehensive or cohesive synthesis by which to understand the functional diversity of the group has yet to develop. Interest in ectomycorrhizal fungi, of which Russulaceae is a key lineage, is prodigious due to the important roles they play as plant root mutualists in ecosystem functioning, global carbon sequestration, and a potential role in technology development toward environmental sustainability. As one of the most species-diverse ectomycorrhizal lineages, the Russulaceae has recently been the focus of a dense sampling and genome sequencing initiative with the Joint Genome Institute aimed at untangling their functional roles and testing whether functional niche specialization exists for independent lineages of ectomycorrhizal fungi. In this paper, we present a review of important studies on this group to contextualize what we know about its members' evolutionary history and ecosystem functions, as well as to generate hypotheses establishing the Russulaceae as a valuable experimental system.},
doi = {10.1111/nph.15001},
journal = {New Phytologist},
number = 1,
volume = 218,
place = {United States},
year = {2018},
month = {1}
}

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Figures / Tables:

Table 1 Table 1: Russulaceae genome sampling with pertinent metadata (Joint Genome Initiative (JGI) identifier, taxon with strain identifier, source of sequencing, JGI project number, location collected and GenBank internal transcribed spacer (ITS) region accession numbers)

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Works referenced in this record:

High speciation rate at temperate latitudes explains unusual diversity gradients in a clade of ectomycorrhizal fungi: CAESAR'S MUSHROOMS: LATITUDE AND DIVERSIFICATION
journal, August 2015

  • Sánchez-Ramírez, Santiago; Etienne, Rampal S.; Moncalvo, Jean-Marc
  • Evolution, Vol. 69, Issue 8
  • DOI: 10.1111/evo.12722

A total synthesis of (+)-isovelleral. The absolute configuration of the russulaceae sesquiterpenes
journal, January 1990

  • Bergman, R.; Hansson, T.; Sterner, O.
  • Journal of the Chemical Society, Chemical Communications, Issue 12
  • DOI: 10.1039/c39900000865

The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis
journal, March 2008


Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation?
journal, June 2011


Extreme specificity in epiparasitic Monotropoideae (Ericaceae): widespread phylogenetic and geographical structure
journal, September 2001


Systematics of Pleurotoid Russulaceae from Guyana and Japan, with Notes on Their Ectomycorrhizal Status
journal, November 2000

  • Henkel, Terry W.; Aime, M. Catherine; Miller, Steven L.
  • Mycologia, Vol. 92, Issue 6
  • DOI: 10.2307/3761479

Mycorrhizal vs saprotrophic status of fungi: the isotopic evidence
journal, June 2001


Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types
journal, June 2009


The Sesquiterpenes of Lactarius vellereus and Their Role in a Proposed Chemical Defense System
journal, March 1985

  • Sterner, Olov; Bergman, Rolf; Kihlberg, Jan
  • Journal of Natural Products, Vol. 48, Issue 2
  • DOI: 10.1021/np50038a013

Macrofungi from six habitats over five years in Clayoquot Sound, Vancouver Island
journal, October 2004

  • Roberts, Christine; Ceska, Oluna; Kroeger, Paul
  • Canadian Journal of Botany, Vol. 82, Issue 10
  • DOI: 10.1139/b04-114

Modelling the influence of ectomycorrhizal decomposition on plant nutrition and soil carbon sequestration in boreal forest ecosystems
journal, October 2016

  • Baskaran, Preetisri; Hyvönen, Riitta; Berglund, S. Linnea
  • New Phytologist, Vol. 213, Issue 3
  • DOI: 10.1111/nph.14213

Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break
journal, July 2007


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

Phylogenetic relationships of russuloid basidiomycetes with emphasis on aphyllophoralean taxa
journal, November 2003


Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi
journal, January 2016

  • Looney, Brian P.; Ryberg, Martin; Hampe, Felix
  • Molecular Ecology, Vol. 25, Issue 2
  • DOI: 10.1111/mec.13506

Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present
journal, April 2001


Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture
journal, February 2015

  • Ditengou, Franck A.; Müller, Anna; Rosenkranz, Maaria
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7279

Perspectives in the new Russulales
journal, November 2006


Endosymbiont-Dependent Host Reproduction Maintains Bacterial-Fungal Mutualism
journal, May 2007

  • Partida-Martinez, Laila P.; Monajembashi, Shamci; Greulich, Karl-Otto
  • Current Biology, Vol. 17, Issue 9
  • DOI: 10.1016/j.cub.2007.03.039

The evolution of fungus-growing termites and their mutualistic fungal symbionts
journal, October 2002

  • Aanen, D. K.; Eggleton, P.; Rouland-Lefevre, C.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 23
  • DOI: 10.1073/pnas.222313099

Towards global patterns in the diversity and community structure of ectomycorrhizal fungi: GLOBAL METASTUDY OF ECTOMYCORRHIZAL FUNGI
journal, May 2012


A.B. Frank and mycorrhizae: the challenge to evolutionary and ecologic theory
journal, October 2004


The mycorrhiza helper bacteria revisited
journal, October 2007


Molecular inference, multivariate morphometrics and ecological assessment are applied in concert to delimit species in the Russula clavipes complex
journal, July 2016

  • Adamčík, Slavomír; Slovák, Marek; Eberhardt, Ursula
  • Mycologia, Vol. 108, Issue 4
  • DOI: 10.3852/15-194

Identification of laccase-like genes in ectomycorrhizal basidiomycetes and transcriptional regulation by nitrogen in Piloderma byssinum
journal, March 2003


Belowground Ectomycorrhizal Fungal Community Change over a Nitrogen Deposition Gradient in Alaska
journal, January 2002


ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi
journal, July 2009

  • Bödeker, Inga T. M.; Nygren, Cajsa M. R.; Taylor, Andy F. S.
  • The ISME Journal, Vol. 3, Issue 12
  • DOI: 10.1038/ismej.2009.77

Temporal Changes in the Ectomycorrhizal Community in Two Soil Horizons of a Temperate Oak Forest
journal, July 2008

  • Courty, P. -E.; Franc, A.; Pierrat, J. -C.
  • Applied and Environmental Microbiology, Vol. 74, Issue 18
  • DOI: 10.1128/AEM.01592-08

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


Evidence for strong inter- and intracontinental phylogeographic structure in Amanita muscaria, a wind-dispersed ectomycorrhizal basidiomycete
journal, August 2008

  • Geml, József; Tulloss, Rodham E.; Laursen, Gary A.
  • Molecular Phylogenetics and Evolution, Vol. 48, Issue 2
  • DOI: 10.1016/j.ympev.2008.04.029

The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens
journal, January 1988


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


Fungal endophytes: modifiers of plant disease
journal, December 2015


A Laccase from the Wild Mushroom, Russula Foetens
journal, June 1940

  • Gregg, Donald C.; Miller, Wilbur H.
  • Journal of the American Chemical Society, Vol. 62, Issue 6
  • DOI: 10.1021/ja01863a013

Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest
journal, May 2008


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
  • DOI: 10.1073/pnas.1322671111

Lactarius subgenus Russularia (Basidiomycota, Russulales): novel Asian species, worldwide phylogeny and evolutionary relationships
journal, December 2016


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


Bacteria associated with Pinus sylvestris-Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro
journal, September 2001


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


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
  • DOI: 10.1038/ng.3223

Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013


Identification of genes for lignin peroxidases and manganese peroxidases in ectomycorrhizal fungi
journal, October 2001


Sequestrate Lactarius species from tropical Africa: L. angiocarpus sp. nov. and L. dolichocaulis comb. nov.
journal, September 2004


Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters
journal, May 2017

  • Pellitier, Peter T.; Zak, Donald R.
  • New Phytologist, Vol. 217, Issue 1
  • DOI: 10.1111/nph.14598

Screening for Putative PGPR to Improve Establishment of the Symbiosis Lactarius deliciosus-Pinus sp.
journal, July 2005


Terpenoids from Russula lepida and R. amarissima (Basidiomycota, Russulaceae)
journal, December 2012


Fungi from decayed wood as ectomycorrhizal symbionts of western hemlock
journal, March 1982

  • Kropp, Bradley R.
  • Canadian Journal of Forest Research, Vol. 12, Issue 1
  • DOI: 10.1139/x82-005

Exploration types of ectomycorrhizae
journal, June 2001


Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria
journal, November 2016

  • Wilson, Andrew W.; Hosaka, Kentaro; Mueller, Gregory M.
  • New Phytologist, Vol. 213, Issue 4
  • DOI: 10.1111/nph.14270

Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest
journal, November 2006


Ectomycorrhizal fungal succession in mixed temperate forests
journal, October 2007


On temporal partitioning of a community of ectomycorrhizal fungi
journal, April 2007


Diversity and classification of mycorrhizal associations
journal, January 1999


Development of the Poplar -Laccaria bicolor Ectomycorrhiza Modifies Root Auxin Metabolism, Signaling, and Response
journal, June 2015

  • Vayssières, Alice; Pěnčík, Ales; Felten, Judith
  • Plant Physiology, Vol. 169, Issue 1
  • DOI: 10.1104/pp.114.255620

Growth on nitrate and occurrence of nitrate reductase-encoding genes in a phylogenetically diverse range of ectomycorrhizal fungi
journal, December 2008


Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors
journal, November 2015

  • Shah, Firoz; Nicolás, César; Bentzer, Johan
  • New Phytologist, Vol. 209, Issue 4
  • DOI: 10.1111/nph.13722

Assays of the biological activities of guaiane sesquiterpenoids isolated from the fruit bodies of edible lactarius species
journal, January 1989


Endemism and functional convergence across the North American soil mycobiome
journal, April 2014

  • Talbot, J. M.; Bruns, T. D.; Taylor, J. W.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1402584111

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
  • DOI: 10.1093/nar/gkt1183

A multi-gene phylogeny of Lactifluus ( Basidiomycota , Russulales ) translated into a new infrageneric classification of the genus
journal, June 2017

  • De Crop, E.; Nuytinck, J.; Van de Putte, K.
  • Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 38, Issue 1
  • DOI: 10.3767/003158517X693255

Fungal symbioses in bryophytes: New insights in the Twenty First Century
journal, September 2010


Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014

  • Riley, Robert; Salamov, Asaf A.; Brown, Daren W.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
  • DOI: 10.1073/pnas.1400592111

Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition
journal, February 2013


Sequencing the fungal tree of life: Letters
journal, March 2011


Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016

  • Martin, Francis; Kohler, Annegret; Murat, Claude
  • Nature Reviews Microbiology, Vol. 14, Issue 12
  • DOI: 10.1038/nrmicro.2016.149

    Works referencing / citing this record:

    Fungal communities do not recover after removing invasive Alliaria petiolata (garlic mustard)
    journal, June 2019


    Notes, outline and divergence times of Basidiomycota
    journal, November 2019


    The quest for a globally comprehensible Russula language
    journal, October 2019


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.