Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer
Abstract
Forest trees are able to thrive in nutrient-poor soils in part because they obtain growth-limiting nutrients, especially nitrogen (N), through mutualistic symbiosis with ectomycorrhizal (ECM) fungi. Addition of inorganic N into these soils is known to disrupt this mutualism and reduce the diversity of ECM fungi. Despite its ecological impact, the mechanisms governing the observed effects of elevated inorganic N on mycorrhizal communities remain unknown. Here, we address this by using a compartmentalized in vitro system to independently alter nutrients to each symbiont. Using stable isotopes, we traced the nutrient flux under different nutrient regimes between Eucalyptus grandis and its ectomycorrhizal symbiont, Pisolithus albus. We demonstrate that giving E. grandis independent access to N causes a significant reduction in root colonization by P. albus. Transcriptional analysis suggests that the observed reduction in colonization may be caused, in part, by altered transcription of microbe perception genes and defence genes. We show that delivery of N to host leaves is not increased by host nutrient deficiency but by fungal nutrient availability instead. Overall, this advances our understanding of the effects of N fertilization on ECM fungi and the factors governing nutrient transfer in the E. grandis-P. microcarpus interaction.
- Authors:
-
- Western Sydney Univ., Richmond, NSW (Australia)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- INRA, Champenoux (France)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Australian Research Council
- OSTI Identifier:
- 1619172
- Alternate Identifier(s):
- OSTI ID: 1579597
- Grant/Contract Number:
- AC02-05CH11231; DP160102684; CSP1953; AC02‐05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 226; Journal Issue: 1; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ectomycorrhizal (ECM) fungi; nitrogen deposition; nutrient trading; stable isotope tracing; transcriptomic analysis
Citation Formats
Plett, Krista L., Singan, Vasanth R., Wang, Mei, Ng, Vivian, Grigoriev, Igor V., Martin, Francis, Plett, Jonathan M., and Anderson, Ian C. Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer. United States: N. p., 2019.
Web. doi:10.1111/nph.16322.
Plett, Krista L., Singan, Vasanth R., Wang, Mei, Ng, Vivian, Grigoriev, Igor V., Martin, Francis, Plett, Jonathan M., & Anderson, Ian C. Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer. United States. https://doi.org/10.1111/nph.16322
Plett, Krista L., Singan, Vasanth R., Wang, Mei, Ng, Vivian, Grigoriev, Igor V., Martin, Francis, Plett, Jonathan M., and Anderson, Ian C. Fri .
"Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer". United States. https://doi.org/10.1111/nph.16322. https://www.osti.gov/servlets/purl/1619172.
@article{osti_1619172,
title = {Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer},
author = {Plett, Krista L. and Singan, Vasanth R. and Wang, Mei and Ng, Vivian and Grigoriev, Igor V. and Martin, Francis and Plett, Jonathan M. and Anderson, Ian C.},
abstractNote = {Forest trees are able to thrive in nutrient-poor soils in part because they obtain growth-limiting nutrients, especially nitrogen (N), through mutualistic symbiosis with ectomycorrhizal (ECM) fungi. Addition of inorganic N into these soils is known to disrupt this mutualism and reduce the diversity of ECM fungi. Despite its ecological impact, the mechanisms governing the observed effects of elevated inorganic N on mycorrhizal communities remain unknown. Here, we address this by using a compartmentalized in vitro system to independently alter nutrients to each symbiont. Using stable isotopes, we traced the nutrient flux under different nutrient regimes between Eucalyptus grandis and its ectomycorrhizal symbiont, Pisolithus albus. We demonstrate that giving E. grandis independent access to N causes a significant reduction in root colonization by P. albus. Transcriptional analysis suggests that the observed reduction in colonization may be caused, in part, by altered transcription of microbe perception genes and defence genes. We show that delivery of N to host leaves is not increased by host nutrient deficiency but by fungal nutrient availability instead. Overall, this advances our understanding of the effects of N fertilization on ECM fungi and the factors governing nutrient transfer in the E. grandis-P. microcarpus interaction.},
doi = {10.1111/nph.16322},
journal = {New Phytologist},
number = 1,
volume = 226,
place = {United States},
year = {2019},
month = {11}
}
Web of Science
Works referenced in this record:
The Role of Nitrogen Deposition in Widespread Plant Community Change Across Semi-natural Habitats
journal, April 2014
- Field, Chris D.; Dise, Nancy B.; Payne, Richard J.
- Ecosystems, Vol. 17, Issue 5
The Influence of Contrasting Microbial Lifestyles on the Pre-symbiotic Metabolite Responses of Eucalyptus grandis Roots
journal, February 2019
- Wong, Johanna W. H.; Lutz, Adrian; Natera, Siria
- Frontiers in Ecology and Evolution, Vol. 7
Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants
journal, May 2014
- Fellbaum, Carl R.; Mensah, Jerry A.; Cloos, Adam J.
- New Phytologist, Vol. 203, Issue 2
Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests
journal, September 2016
- Lin, Guigang; McCormack, M. Luke; Ma, Chengen
- New Phytologist, Vol. 213, Issue 3
Production and turnover of ectomycorrhizal extramatrical mycelial biomass and necromass under elevated CO 2 and nitrogen fertilization
journal, April 2016
- Ekblad, Alf; Mikusinska, Anna; Ågren, Göran I.
- New Phytologist, Vol. 211, Issue 3
Bi-directional transfer of nitrogen between alfalfa and bromegrass: Short and long term evidence
journal, July 1994
- Tomm, Gilberto O.; van Kessel, Chris; Slinkard, Alfred E.
- Plant and Soil, Vol. 164, Issue 1
Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis
journal, January 2012
- Fellbaum, C. R.; Gachomo, E. W.; Beesetty, Y.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 7
A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies
journal, July 2004
- Treseder, Kathleen K.
- New Phytologist, Vol. 164, Issue 2
REVIGO Summarizes and Visualizes Long Lists of Gene Ontology Terms
journal, July 2011
- Supek, Fran; Bošnjak, Matko; Škunca, Nives
- PLoS ONE, Vol. 6, Issue 7
Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest
journal, March 2013
- Clemmensen, K. E.; Bahr, A.; Ovaskainen, O.
- Science, Vol. 339, Issue 6127
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
Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis
journal, August 2011
- Kiers, E. T.; Duhamel, M.; Beesetty, Y.
- Science, Vol. 333, Issue 6044
Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi?
journal, August 2001
- Bidartondo, M. I.; Ek, H.; Wallander, H.
- New Phytologist, Vol. 151, Issue 2
The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events
journal, November 2010
- Balzergue, Coline; Puech-Pagès, Virginie; Bécard, Guillaume
- Journal of Experimental Botany, Vol. 62, Issue 3
Dosage and duration effects of nitrogen additions on ectomycorrhizal sporocarp production and functioning: an example from two N-limited boreal forests
journal, July 2014
- Hasselquist, Niles J.; Högberg, Peter
- Ecology and Evolution, Vol. 4, Issue 15
Production of external mycelium by ectomycorrhizal fungi in a norway spruce forest was reduced in response to nitrogen fertilization
journal, May 2003
- Nilsson, Lars Ola; Wallander, Hakan
- New Phytologist, Vol. 158, Issue 2
Carbon allocation in ectomycorrhizal plants at limited and optimal N supply: an attempt at unraveling conflicting theories
journal, April 2010
- Corrêa, Ana; Hampp, Rüdiger; Magel, Elisabeth
- Mycorrhiza, Vol. 21, Issue 1
Belowground Ectomycorrhizal Fungal Community Change over a Nitrogen Deposition Gradient in Alaska
journal, January 2002
- Lilleskov, Erik A.; Fahey, Timothy J.; Horton, Thomas R.
- Ecology, Vol. 83, Issue 1
Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests?
journal, January 2013
- Näsholm, Torgny; Högberg, Peter; Franklin, Oskar
- New Phytologist, Vol. 198, Issue 1
Mycorrhizas and soil structure
journal, July 2006
- Rillig, Matthias C.; Mummey, Daniel L.
- New Phytologist, Vol. 171, Issue 1
The Development and Ultrastructure of Ectomycorrhizas. iv. Compatible and Incompatible Interactions Between Suillus Grevillei (Klotzsch) Sing. and a Number of Ectomycorrhizal Hosts in Vitro in the Presence of Exogenous Carbohydrate
journal, July 1986
- Duddridge, J. A.
- New Phytologist, Vol. 103, Issue 3
Correction: Phosphorus and Nitrogen Regulate Arbuscular Mycorrhizal Symbiosis in Petunia hybrida
journal, April 2015
- Nouri, Eva; Breuillin-Sessoms, Florence; Feller, Urs
- PLOS ONE, Vol. 10, Issue 4
CO 2 -ENRICHMENT AND NUTRIENT AVAILABILITY ALTER ECTOMYCORRHIZAL FUNGAL COMMUNITIES
journal, September 2006
- Parrent, Jeri Lynn; Morris, William F.; Vilgalys, Rytas
- Ecology, Vol. 87, Issue 9
Nitrogen Cycles: Past, Present, and Future
journal, September 2004
- Galloway, J. N.; Dentener, F. J.; Capone, D. G.
- Biogeochemistry, Vol. 70, Issue 2
Temperate eucalypt forest decline is linked to altered ectomycorrhizal communities mediated by soil chemistry
journal, August 2013
- Horton, Bryony M.; Glen, Morag; Davidson, Neil J.
- Forest Ecology and Management, Vol. 302
Nitrogen transport in the ectomycorrhiza association: The Hebeloma cylindrosporum–Pinus pinaster model
journal, January 2007
- Müller, Tobias; Avolio, Meghan; Olivi, Martin
- Phytochemistry, Vol. 68, Issue 1
A nitrogen fertilization field study of carbon-13 and nitrogen-15 transfers in ectomycorrhizas of Pinus sabiniana
journal, August 2013
- Albarracín, María Victoria; Six, Johan; Houlton, Benjamin Z.
- Oecologia, Vol. 173, Issue 4
Response of plants to ectomycorrhizae in N-limited conditions: which factors determine its variation?
journal, August 2008
- Corrêa, A.; Strasser, R. J.; Martins-Loução, M. A.
- Mycorrhiza, Vol. 18, Issue 8
Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest
journal, June 2006
- Toljander, Jonas F.; Eberhardt, Ursula; Toljander, Ylva K.
- New Phytologist, Vol. 170, Issue 4
Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants
journal, August 2009
- He, X.; Xu, M.; Qiu, G. Y.
- Journal of Plant Ecology, Vol. 2, Issue 3
Genome-Wide Expression Pattern Analyses of the Arabidopsis Leucine-Rich Repeat Receptor-Like Kinases
journal, February 2016
- Wu, Yunzhe; Xun, Qingqing; Guo, Yi
- Molecular Plant, Vol. 9, Issue 2
Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks
journal, July 2018
- Averill, Colin; Dietze, Michael C.; Bhatnagar, Jennifer M.
- Global Change Biology, Vol. 24, Issue 10
Phosphate Treatment Strongly Inhibits New Arbuscule Development But Not the Maintenance of Arbuscule in Mycorrhizal Rice Roots
journal, March 2016
- Kobae, Yoshihiro; Ohmori, Yoshihiro; Saito, Chieko
- Plant Physiology, Vol. 171, Issue 1
The genome of Eucalyptus grandis
journal, June 2014
- Myburg, Alexander A.; Grattapaglia, Dario; Tuskan, Gerald A.
- Nature, Vol. 510, Issue 7505
Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest
journal, December 2015
- Hasselquist, Niles Jacob; Metcalfe, Daniel B.; Inselsbacher, Erich
- Ecology
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
Nitrogen addition alters ectomycorrhizal fungal communities and soil enzyme activities in a tropical montane forest
journal, June 2017
- Corrales, Adriana; Turner, Benjamin L.; Tedersoo, Leho
- Fungal Ecology, Vol. 27
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
Long-Term Change in the Nitrogen Cycle of Tropical Forests
journal, November 2011
- Hietz, P.; Turner, B. L.; Wanek, W.
- Science, Vol. 334, Issue 6056
Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest
journal, April 2010
- Högberg, Mona N.; Briones, Maria J. I.; Keel, Sonja G.
- New Phytologist, Vol. 187, Issue 2
Effects of nitrogen deposition and empirical nitrogen critical loads for ecoregions of the United States
journal, December 2011
- Pardo, Linda H.; Fenn, Mark E.; Goodale, Christine L.
- Ecological Applications, Vol. 21, Issue 8
Carbon and nitrogen fluxes between beech and their ectomycorrhizal assemblage
journal, April 2014
- Valtanen, Kerttu; Eissfeller, Verena; Beyer, Friderike
- Mycorrhiza, Vol. 24, Issue 8
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
Know your enemy, embrace your friend: using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms
journal, January 2018
- Plett, Jonathan M.; Martin, Francis M.
- The Plant Journal, Vol. 93, Issue 4
Regulation of resource exchange in the arbuscular mycorrhizal symbiosis
journal, November 2015
- Walder, Florian; van der Heijden, Marcel G. A.
- Nature Plants, Vol. 1, Issue 11
Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning: Phosphate and Petunia mycorrhiza development and functioning
journal, November 2010
- Breuillin, Florence; Schramm, Jonathan; Hajirezaei, Mohammad
- The Plant Journal, Vol. 64, Issue 6
Mycorrhizal responses in wheat: shading decreases growth but does not lower the contribution of the fungal phosphate uptake pathway
journal, January 2014
- Stonor, Rebecca N.; Smith, Sally E.; Manjarrez, Maria
- Mycorrhiza, Vol. 24, Issue 6
An extracellular network of Arabidopsis leucine-rich repeat receptor kinases
journal, January 2018
- Smakowska-Luzan, Elwira; Mott, G. Adam; Parys, Katarzyna
- Nature, Vol. 553, Issue 7688
Lectin receptor kinases in plant innate immunity
journal, January 2013
- Singh, Prashant; Zimmerli, Laurent
- Frontiers in Plant Science, Vol. 4
Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition
journal, March 2017
- Tang, Dingzhong; Wang, Guoxun; Zhou, Jian-Min
- The Plant Cell, Vol. 29, Issue 4
Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest
journal, October 2016
- Morrison, Eric W.; Frey, Serita D.; Sadowsky, Jesse J.
- Fungal Ecology, Vol. 23
Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments
journal, November 2011
- Phoenix, Gareth K.; Emmett, Bridget A.; Britton, Andrea J.
- Global Change Biology, Vol. 18, Issue 4
Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes
journal, August 2004
- Read, David J.; Leake, Jonathan R.; Perez-Moreno, Jesus
- Canadian Journal of Botany, Vol. 82, Issue 8
Significance of galactinol and raffinose family oligosaccharide synthesis in plants
journal, August 2015
- Sengupta, Sonali; Mukherjee, Sritama; Basak, Papri
- Frontiers in Plant Science, Vol. 6
HISAT: a fast spliced aligner with low memory requirements
journal, March 2015
- Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 12, Issue 4
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
Root-Associated Mycobiomes of Common Temperate Plants (Calluna vulgaris and Holcus lanatus) Are Strongly Affected by Winter Climate Conditions
journal, January 2021
- Dahl, Mathilde Borg; Peršoh, Derek; Jentsch, Anke
- Microbial Ecology, Vol. 82, Issue 2
ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages
journal, June 2020
- Yin, Jinlong; Kim, Sung Soo; Choi, Eunji
- Nature Communications, Vol. 11, Issue 1
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021
- Rajewski, Alex; Carter-House, Derreck; Stajich, Jason
- BMC Genomics, Vol. 22, Issue 1
An extracellular network of Arabidopsis leucine-rich repeat receptor kinases
text, January 2018
- Smakowska-Luzan, Elwira; Mott, G. Adam; Parys, Katarzyna
- Nature Publishing Group
Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning
text, January 2010
- Breuillin, F.; Schramm, J.; Hajirezaei, M.
- Wiley-Blackwell
Nitrogen Transport in the Ectomycorrhiza Association: The Hebeloma cylindrosporom—Pinus pinaster Model
journal, May 2007
- Mueller, Tobias; Avolio, Meghan; Olivi, Martin
- ChemInform, Vol. 38, Issue 22
Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest
journal, December 2015
- Hasselquist, Niles J.; Metcalfe, Daniel B.; Inselsbacher, Erich
- Ecology