Intra‐species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus
Abstract
Summary Ectomycorrhizal (ECM) fungi are integral to boreal and temperate forest ecosystem functioning and nutrient cycling. ECM fungi, however, originate from diverse saprotrophic lineages and the impacts of genetic variation across species, and especially within a given ECM species, on function and interactions with the environment is not well understood. Here, we explore the extent of intra‐species variation between four isolates of the ECM fungus Pisolithus microcarpus , in terms of gene regulation, carbon metabolism and growth, and interactions with a host, Eucalyptus grandis . We demonstrate that, while a core response to the host is maintained by all of the isolates tested, they have distinct patterns of gene expression and carbon metabolism, resulting in the differential expression of isolate‐specific response pathways in the host plant. Together, these results highlight the importance of using a wider range of individuals within a species to understand the broader ecological roles of ECM fungi and their host interactions.
- Authors:
-
- Hawkesbury Institute for the Environment Western Sydney University Richmond NSW 2753 Australia
- Université de Lorraine, INRAE, UMR Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRAE GrandEst‐Nancy Champenoux 54280 France
- Royal Botanic Gardens Victoria Melbourne VIC 3004 Australia, Botanic Gardens and State Herbarium of South Australia Adelaide SA 5000 Australia
- US Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA 94720 USA
- US Department of Energy Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA 94720 USA, Department of Plant and Microbial Biology University of California Berkeley CA 94720 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1804926
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Name: Environmental Microbiology Journal Volume: 23 Journal Issue: 4; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Plett, Krista L., Kohler, Annegret, Lebel, Teresa, Singan, Vasanth R., Bauer, Diane, He, Guifen, Ng, Vivian, Grigoriev, Igor V., Martin, Francis, Plett, Jonathan M., and Anderson, Ian C. Intra‐species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus. United Kingdom: N. p., 2020.
Web. doi:10.1111/1462-2920.15320.
Plett, Krista L., Kohler, Annegret, Lebel, Teresa, Singan, Vasanth R., Bauer, Diane, He, Guifen, Ng, Vivian, Grigoriev, Igor V., Martin, Francis, Plett, Jonathan M., & Anderson, Ian C. Intra‐species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus. United Kingdom. https://doi.org/10.1111/1462-2920.15320
Plett, Krista L., Kohler, Annegret, Lebel, Teresa, Singan, Vasanth R., Bauer, Diane, He, Guifen, Ng, Vivian, Grigoriev, Igor V., Martin, Francis, Plett, Jonathan M., and Anderson, Ian C. Wed .
"Intra‐species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus". United Kingdom. https://doi.org/10.1111/1462-2920.15320.
@article{osti_1804926,
title = {Intra‐species genetic variability drives carbon metabolism and symbiotic host interactions in the ectomycorrhizal fungus Pisolithus microcarpus},
author = {Plett, Krista L. and Kohler, Annegret and Lebel, Teresa and Singan, Vasanth R. and Bauer, Diane and He, Guifen and Ng, Vivian and Grigoriev, Igor V. and Martin, Francis and Plett, Jonathan M. and Anderson, Ian C.},
abstractNote = {Summary Ectomycorrhizal (ECM) fungi are integral to boreal and temperate forest ecosystem functioning and nutrient cycling. ECM fungi, however, originate from diverse saprotrophic lineages and the impacts of genetic variation across species, and especially within a given ECM species, on function and interactions with the environment is not well understood. Here, we explore the extent of intra‐species variation between four isolates of the ECM fungus Pisolithus microcarpus , in terms of gene regulation, carbon metabolism and growth, and interactions with a host, Eucalyptus grandis . We demonstrate that, while a core response to the host is maintained by all of the isolates tested, they have distinct patterns of gene expression and carbon metabolism, resulting in the differential expression of isolate‐specific response pathways in the host plant. Together, these results highlight the importance of using a wider range of individuals within a species to understand the broader ecological roles of ECM fungi and their host interactions.},
doi = {10.1111/1462-2920.15320},
journal = {Environmental Microbiology},
number = 4,
volume = 23,
place = {United Kingdom},
year = {Wed Nov 18 00:00:00 EST 2020},
month = {Wed Nov 18 00:00:00 EST 2020}
}
https://doi.org/10.1111/1462-2920.15320
Works referenced in this record:
Digging Deeper: In Search of the Mechanisms of Carbon and Nitrogen Exchange in Ectomycorrhizal Symbioses
journal, January 2020
- Stuart, Emiko K.; Plett, Krista L.
- Frontiers in Plant Science, Vol. 10
Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth: Functional variability in AMF populations
journal, November 2005
- Koch, Alexander M.; Croll, Daniel; Sanders, Ian R.
- Ecology Letters, Vol. 9, Issue 2
Study of nitrogen and carbon transfer from soil organic matter to Tuber melanosporum mycorrhizas and ascocarps using 15N and 13C soil labelling and whole-genome oligoarrays
journal, June 2015
- Le Tacon, François; Zeller, Bernd; Plain, Caroline
- Plant and Soil, Vol. 395, Issue 1-2
Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs
journal, December 2014
- Lindahl, Björn D.; Tunlid, Anders
- New Phytologist, Vol. 205, Issue 4
Feedbacks between plant N demand and rhizosphere priming depend on type of mycorrhizal association
journal, July 2017
- Sulman, Benjamin N.; Brzostek, Edward R.; Medici, Chiara
- Ecology Letters, Vol. 20, Issue 8
The Biotrophic Development of Ustilago maydis Studied by RNA-Seq Analysis
journal, January 2018
- Lanver, Daniel; Müller, André N.; Happel, Petra
- The Plant Cell, Vol. 30, Issue 2
High functional diversity within species of arbuscular mycorrhizal fungi is associated with differences in phosphate and nitrogen uptake and fungal phosphate metabolism
journal, February 2015
- Mensah, Jerry A.; Koch, Alexander M.; Antunes, Pedro M.
- Mycorrhiza, Vol. 25, Issue 7
WGCNA: an R package for weighted correlation network analysis
journal, December 2008
- Langfelder, Peter; Horvath, Steve
- BMC Bioinformatics, Vol. 9, Issue 1
Mannitol biosynthesis is required for plant pathogenicity by Alternaria alternata
journal, August 2008
- Vélëz, Heriberto; Glassbrook, Norman J.; Daub, Margaret E.
- FEMS Microbiology Letters, Vol. 285, Issue 1
Mannitol metabolism during pathogenic fungal–host interactions under stressed conditions
journal, September 2015
- Meena, Mukesh; Prasad, Vishal; Zehra, Andleeb
- Frontiers in Microbiology, Vol. 6
Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes
journal, September 2000
- Hibbett, David S.; Gilbert, Luz-Beatriz; Donoghue, Michael J.
- Nature, Vol. 407, Issue 6803
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
Intra- and interspecific variation in patterns of organic and inorganic nitrogen utilization by three Australian Pisolithus species
journal, December 1999
- Anderson, I. C.; Chambers, S. M.; Cairney, J. W. G.
- Mycological Research, Vol. 103, Issue 12
Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits
journal, October 2020
- Miyauchi, Shingo; Kiss, Enikő; Kuo, Alan
- Nature Communications, Vol. 11, Issue 1
Strain Identity of the Ectomycorrhizal Fungus Laccaria bicolor Is More Important than Richness in Regulating Plant and Fungal Performance under Nutrient Rich Conditions
journal, September 2017
- Hazard, Christina; Kruitbos, Laura; Davidson, Hazel
- Frontiers in Microbiology, Vol. 8
Trehalose synthesis in ectomycorrhizas – a driving force of carbon gain for fungi?
journal, March 2007
- Wiemken, Verena
- New Phytologist, Vol. 174, Issue 2
Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment: Organic nutrient uptake enhances soil C
journal, March 2011
- Orwin, Kate H.; Kirschbaum, Miko U. F.; St John, Mark G.
- Ecology Letters, Vol. 14, Issue 5
A systems biology view of wood formation in Eucalyptus grandis trees submitted to different potassium and water regimes
journal, April 2019
- Ployet, Raphael; Veneziano Labate, Mônica T.; Regiani Cataldi, Thais
- New Phytologist, Vol. 223, Issue 2
Using plant, microbe, and soil fauna traits to improve the predictive power of biogeochemical models
journal, October 2018
- Fry, Ellen L.; De Long, Jonathan R.; Álvarez Garrido, Lucía
- Methods in Ecology and Evolution, Vol. 10, Issue 1
Genetic isolation between two recently diverged populations of a symbiotic fungus
journal, April 2015
- Branco, Sara; Gladieux, Pierre; Ellison, Christopher E.
- Molecular Ecology, Vol. 24, Issue 11
Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground
journal, December 2013
- Tedersoo, Leho; Smith, Matthew E.
- Fungal Biology Reviews, Vol. 27, Issue 3-4
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
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
Ecological consequences of genetic diversity: Ecological effects of genetic diversity
journal, April 2008
- Hughes, A. Randall; Inouye, Brian D.; Johnson, Marc T. J.
- Ecology Letters, Vol. 11, Issue 6
Carbohydrate and Amino Acid Metabolism in the Eucalyptus globulus-Pisolithus tinctorius Ectomycorrhiza during Glucose Utilization
journal, October 1998
- Martin, Francis; Boiffin, Vincent; Pfeffer, Philip E.
- Plant Physiology, Vol. 118, Issue 2
The genome of Eucalyptus grandis
journal, June 2014
- Myburg, Alexander A.; Grattapaglia, Dario; Tuskan, Gerald A.
- Nature, Vol. 510, Issue 7505
The major pathways of carbohydrate metabolism in the ectomycorrhizal basidiomycete Laccaria bicolor S238N
journal, October 2008
- Deveau, A.; Kohler, A.; Frey-Klett, P.
- New Phytologist, Vol. 180, Issue 2
High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis
journal, January 2018
- Chen, Eric C. H.; Morin, Emmanuelle; Beaudet, Denis
- New Phytologist, Vol. 220, Issue 4
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
Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review: Fungal carbohydrates in the ectomycorrhizal symbiosis
journal, February 2010
- Nehls, U.; Göhringer, F.; Wittulsky, S.
- Plant Biology, Vol. 12, Issue 2
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 effect of elevated carbon dioxide on the interaction between Eucalyptus grandis and diverse isolates of Pisolithus sp. is associated with a complex shift in the root transcriptome
journal, November 2014
- Plett, Jonathan M.; Kohler, Annegret; Khachane, Amit
- New Phytologist, Vol. 206, Issue 4
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
Low-temperature-induced changes in trehalose, mannitol and arabitol associated with enhanced tolerance to freezing in ectomycorrhizal basidiomycetes ( Hebeloma spp.)
journal, October 2002
- M., Tibbett; F., Sanders; J., Cairney
- Mycorrhiza, Vol. 12, Issue 5
Creating the CIPRES Science Gateway for inference of large phylogenetic trees
conference, November 2010
- Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
- 2010 Gateway Computing Environments Workshop (GCE)
Genetic variation and evolutionary history of a mycorrhizal fungus regulate the currency of exchange in symbiosis with the food security crop cassava
journal, February 2020
- Savary, Romain; Dupuis, Cindy; Masclaux, Frédéric G.
- The ISME Journal, Vol. 14, Issue 6
Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest
journal, November 2006
- Lindahl, Björn D.; Ihrmark, Katarina; Boberg, Johanna
- New Phytologist, Vol. 173, Issue 3
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
Two new species of Pisolithus (Sclerodermataceae) from Australasia, and an assessment of the confused nomenclature of P. tinctorius
journal, May 2018
- Lebel, Teresa; Pennycook, Shaun; Barrett, Matthew
- Phytotaxa, Vol. 348, Issue 3
Variation in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated on to Eucalyptus grandis W. Hill ex Maiden
journal, August 1994
- Burgess, T.; Dell, B.; Malajczuk, N.
- New Phytologist, Vol. 127, Issue 4
Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus
journal, November 2004
- Duplessis, Sébastien; Courty, Pierre-Emmanuel; Tagu, Denis
- New Phytologist, Vol. 165, Issue 2
Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance?
journal, March 2003
- Read, D. J.; Perez-Moreno, J.
- New Phytologist, Vol. 157, Issue 3
Arbuscular mycorrhizal fungi: intraspecific diversity and pangenomes
journal, June 2018
- Mathieu, Stephanie; Cusant, Loïc; Roux, Christophe
- New Phytologist, Vol. 220, Issue 4
Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer
journal, December 2019
- Plett, Krista L.; Singan, Vasanth R.; Wang, Mei
- New Phytologist, Vol. 226, Issue 1
The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development
journal, April 2018
- Zhang, Feng; Anasontzis, George E.; Labourel, Aurore
- New Phytologist, Vol. 220, Issue 4
Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests
journal, December 2014
- Clemmensen, Karina E.; Finlay, Roger D.; Dahlberg, Anders
- New Phytologist, Vol. 205, Issue 4
Evolutionary history of mycorrhizal symbioses and global host plant diversity
journal, January 2018
- Brundrett, Mark C.; Tedersoo, Leho
- New Phytologist, Vol. 220, Issue 4
Integration of biological networks and gene expression data using Cytoscape
journal, September 2007
- Cline, Melissa S.; Smoot, Michael; Cerami, Ethan
- Nature Protocols, Vol. 2, Issue 10
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
Exploring the role of ectomycorrhizal fungi in soil carbon dynamics
journal, February 2019
- Zak, Donald R.; Pellitier, Peter T.; Argiroff, WilliamA.
- New Phytologist, Vol. 223, Issue 1
The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems
journal, March 2012
- Johnson, David; Martin, Francis; Cairney, John W. G.
- New Phytologist, Vol. 194, Issue 3
Variation in nitrogen source utilisation by nine Amanita muscaria genotypes from Australian Pinus radiata plantations
journal, August 2003
- Sawyer, Nicole A.; Chambers, Susan M.; Cairney, John W. G.
- Mycorrhiza, Vol. 13, Issue 4
Increased trehalose biosynthesis in Hartig net hyphae of ectomycorrhizas
journal, January 2007
- López, Mónica Fajardo; Männer, Philipp; Willmann, Anita
- New Phytologist, Vol. 174, Issue 2
Mycorrhizal effector PaMiSSP10b alters polyamine biosynthesis in Eucalyptus root cells and promotes root colonization
journal, September 2020
- Plett, Jonathan M.; Plett, Krista L.; Wong‐Bajracharya, Johanna
- New Phytologist, Vol. 228, Issue 2
The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling
journal, February 2013
- Ekblad, A.; Wallander, H.; Godbold, D. L.
- Plant and Soil, Vol. 366, Issue 1-2
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Role of plant–fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi
journal, July 2017
- Hortal, Sara; Plett, Krista Lynn; Plett, Jonathan Michael
- The ISME Journal, Vol. 11, Issue 12
Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016
- Martin, Francis; Kohler, Annegret; Murat, Claude
- Nature Reviews Microbiology, Vol. 14, Issue 12