Benefits of symbiotic ectomycorrhizal fungi to plant water relations depend on plant genotype in pinyon pine

Sevanto, Sanna; Gehring, Catherine A.; Ryan, Max G.; Patterson, Adair; Losko, Adrian S.; Vogel, Sven C.; Carter, Kelsey R.; Dickman, L. Turin; Espy, Michelle A.; Kuske, Cheryl R.

doi:10.1038/s41598-023-41191-5

Benefits of symbiotic ectomycorrhizal fungi to plant water relations depend on plant genotype in pinyon pine

Journal Article · Sat Sep 02 04:00:00 EDT 2023 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-023-41191-5· OSTI ID:2000928

Sevanto, Sanna ^[1]; Gehring, Catherine A. ^[2]; Ryan, Max G. ^[3]; Patterson, Adair ^[2]; Losko, Adrian S. ^[4]; Vogel, Sven C. ^[1]; Carter, Kelsey R. ^[1]; Dickman, L. Turin ^[1]; Espy, Michelle A. ^[1]; Kuske, Cheryl R. ^[1]

Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Northern Arizona University, Flagstaff, AZ (United States)
Integral Ecology Group, Duncan, BC (Canada); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Forschungs-Neutronenquelle Heinz Maier-Leibnitz, Garching (Germany)

Rhizosphere microbes, such as root-associated fungi, can improve plant access to soil resources, affecting plant health, productivity, and stress tolerance. While mycorrhizal associations are ubiquitous, plant–microbe interactions can be species specific. Here we show that the specificity of the effects of microbial symbionts on plant function can go beyond species level: colonization of roots by ectomycorrhizal fungi (EMF) of the genus Geopora has opposite effects on water uptake, and stomatal control of desiccation in drought tolerant and intolerant genotypes of pinyon pine (Pinus edulis Engelm.). These results demonstrate, for the first time, that microorganisms can have significant and opposite effects on important plant functional traits like stomatal control of desiccation that are associated with differential mortality and growth in nature. They also highlight that appropriate pairing of plant genotypes and microbial associates will be important for mitigating climate change impacts on vegetation.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 2000928

Report Number(s):: LA-UR--21-31041

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 13; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Do mycorrhizal network benefits to survival and growth of interior Douglas-fir seedlings increase with soil moisture stress? Bingham, Marcus A.; Simard, Suzanne W. Ecology and Evolution, Vol. 1, Issue 3 https://doi.org/10.1002/ece3.24	journal	October 2011
Mycorrhizas and root architecture Hetrick, B. A. D. Experientia, Vol. 47, Issue 4 https://doi.org/10.1007/BF01972077	journal	April 1991
Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family Tagu, D.; Bastien, C.; Faivre-Rampant, P. Mycorrhiza, Vol. 15, Issue 2 https://doi.org/10.1007/s00572-004-0302-9	journal	March 2004
Ectomycorrhizal community structure of different genotypes of Scots pine under forest nursery conditions Leski, Tomasz; Aučina, Algis; Skridaila, Audrius Mycorrhiza, Vol. 20, Issue 7 https://doi.org/10.1007/s00572-010-0298-2	journal	February 2010
Ectomycorrhizas and water relations of trees: a review Lehto, Tarja; Zwiazek, Janusz J. Mycorrhiza, Vol. 21, Issue 2 https://doi.org/10.1007/s00572-010-0348-9	journal	December 2010
Plant species differ in early seedling growth and tissue nutrient responses to arbuscular and ectomycorrhizal fungi Holste, Ellen K.; Kobe, Richard K.; Gehring, Catherine A. Mycorrhiza, Vol. 27, Issue 3 https://doi.org/10.1007/s00572-016-0744-x	journal	November 2016
Anisohydric behaviour in grapevines results in better performance under moderate water stress and recovery than isohydric behaviour Pou, Alícia; Medrano, Hipólito; Tomàs, Magdalena Plant and Soil, Vol. 359, Issue 1-2 https://doi.org/10.1007/s11104-012-1206-7	journal	March 2012
Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics White, T. J.; Bruns, T.; Lee, S. PCR Protocols https://doi.org/10.1016/B978-0-12-372180-8.50042-1	book	January 1990
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Drought and ecosystem carbon cycling van der Molen, M. K.; Dolman, A. J.; Ciais, P. Agricultural and Forest Meteorology, Vol. 151, Issue 7 https://doi.org/10.1016/j.agrformet.2011.01.018	journal	July 2011
Mycorrhizal mycelium as a global carbon pool Hawkins, Heidi-Jayne; Cargill, Rachael I. M.; Van Nuland, Michael E. Current Biology, Vol. 33, Issue 11 https://doi.org/10.1016/j.cub.2023.02.027	journal	June 2023
Tree genotype influences ectomycorrhizal fungal community structure: Ecological and evolutionary implications Lamit, L. J.; Holeski, L. M.; Flores-Rentería, L. Fungal Ecology, Vol. 24 https://doi.org/10.1016/j.funeco.2016.05.013	journal	December 2016
Plant phenotypic plasticity in a changing climate Nicotra, A. B.; Atkin, O. K.; Bonser, S. P. Trends in Plant Science, Vol. 15, Issue 12 https://doi.org/10.1016/j.tplants.2010.09.008	journal	December 2010
Iso/Anisohydry: A Plant–Environment Interaction Rather Than a Simple Hydraulic Trait Hochberg, Uri; Rockwell, Fulton E.; Holbrook, N. Michele Trends in Plant Science, Vol. 23, Issue 2 https://doi.org/10.1016/j.tplants.2017.11.002	journal	February 2018
Soil Rather Than Xylem Vulnerability Controls Stomatal Response to Drought Carminati, Andrea; Javaux, Mathieu Trends in Plant Science, Vol. 25, Issue 9 https://doi.org/10.1016/j.tplants.2020.04.003	journal	September 2020
Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine Gehring, Catherine A.; Whitham, Thomas G. Nature, Vol. 353, Issue 6344 https://doi.org/10.1038/353556a0	journal	October 1991
Multi-scale predictions of massive conifer mortality due to chronic temperature rise McDowell, N. G.; Williams, A. P.; Xu, C. Nature Climate Change, Vol. 6, Issue 3 https://doi.org/10.1038/nclimate2873	journal	December 2015
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis Bonfante, Paola; Genre, Andrea Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1046	journal	July 2010
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum Peter, Martina; Kohler, Annegret; Ohm, Robin A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12662	journal	September 2016
Unearthing the roots of ectomycorrhizal symbioses Martin, Francis; Kohler, Annegret; Murat, Claude Nature Reviews Microbiology, Vol. 14, Issue 12 https://doi.org/10.1038/nrmicro.2016.149	journal	October 2016
A stomatal safety-efficiency trade-off constrains responses to leaf dehydration Henry, Christian; John, Grace P.; Pan, Ruihua Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11006-1	journal	July 2019
Water deficits and hydraulic limits to leaf water supply Sperry, J. S.; Hacke, U. G.; Oren, R. Plant, Cell and Environment, Vol. 25, Issue 2 https://doi.org/10.1046/j.0016-8025.2001.00799.x	journal	February 2002
Hydraulic architecture of trees: main concepts and results Cruiziat, Pierre; Cochard, Herv�; Am�glio, Thierry Annals of Forest Science, Vol. 59, Issue 7 https://doi.org/10.1051/forest:2002060	journal	November 2002
Resource limitation is a driver of local adaptation in mycorrhizal symbioses Johnson, N. C.; Wilson, G. W. T.; Bowker, M. A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 5 https://doi.org/10.1073/pnas.0906710107	journal	January 2010
Predicting plant vulnerability to drought in biodiverse regions using functional traits Skelton, Robert Paul; West, Adam G.; Dawson, Todd E. Proceedings of the National Academy of Sciences, Vol. 112, Issue 18 https://doi.org/10.1073/pnas.1503376112	journal	April 2015
Tree genetics defines fungal partner communities that may confer drought tolerance Gehring, Catherine A.; Sthultz, Christopher M.; Flores-Rentería, Lluvia Proceedings of the National Academy of Sciences, Vol. 114, Issue 42 https://doi.org/10.1073/pnas.1704022114	journal	September 2017
Global imprint of mycorrhizal fungi on whole-plant nutrient economics Averill, Colin; Bhatnagar, Jennifer M.; Dietze, Michael C. Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1906655116	journal	October 2019
The pipe model theory half a century on: a review Lehnebach, Romain; Beyer, Robert; Letort, Véronique Annals of Botany, Vol. 121, Issue 5 https://doi.org/10.1093/aob/mcx194	journal	January 2018
Effect of poplar genotypes on mycorrhizal infection and secreted enzyme activities in mycorrhizal and non-mycorrhizal roots Courty, P. E.; Labbé, J.; Kohler, A. Journal of Experimental Botany, Vol. 62, Issue 1 https://doi.org/10.1093/jxb/erq274	journal	September 2010
Growth and physiological responses of isohydric and anisohydric poplars to drought Attia, Ziv; Domec, Jean-Christophe; Oren, Ram Journal of Experimental Botany, Vol. 66, Issue 14 https://doi.org/10.1093/jxb/erv195	journal	May 2015
Carbon and nitrogen allocation in ectomycorrhizal and non-mycorrhizal Pinus sylvestris L. seedlings Colpaert, J. V.; van Laere, A.; van Assche, J. A. Tree Physiology, Vol. 16, Issue 9 https://doi.org/10.1093/treephys/16.9.787	journal	September 1996
Stomatal response of an anisohydric grapevine cultivar to evaporative demand, available soil moisture and abscisic acid Rogiers, S. Y.; Greer, D. H.; Hatfield, J. M. Tree Physiology, Vol. 32, Issue 3 https://doi.org/10.1093/treephys/tpr131	journal	December 2011
Abscisic Acid Mediates a Divergence in the Drought Response of Two Conifers Brodribb, T. J.; McAdam, S. A. M. PLANT PHYSIOLOGY, Vol. 162, Issue 3 https://doi.org/10.1104/pp.113.217877	journal	May 2013
The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours Klein, Tamir Functional Ecology, Vol. 28, Issue 6 https://doi.org/10.1111/1365-2435.12289	journal	May 2014
Functional outcomes of fungal community shifts driven by tree genotype and spatial-temporal factors in Mediterranean pine forests Pérez-Izquierdo, Leticia; Zabal-Aguirre, Mario; Flores-Rentería, Dulce Environmental Microbiology, Vol. 19, Issue 4 https://doi.org/10.1111/1462-2920.13690	journal	March 2017
Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance Meinzer, Frederick C.; Johnson, Daniel M.; Lachenbruch, Barbara Functional Ecology, Vol. 23, Issue 5 https://doi.org/10.1111/j.1365-2435.2009.01577.x	journal	October 2009
Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species Sthultz, Christopher M.; Gehring, Catherine A.; Whitham, Thomas G. Global Change Biology, Vol. 15, Issue 8 https://doi.org/10.1111/j.1365-2486.2009.01901.x	journal	August 2009
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294X.1993.tb00005.x	journal	April 1993
A method for measuring hydraulic conductivity and embolism in xylem Sperry, J. S.; Donnelly, J. R.; Tyree, M. T. Plant, Cell and Environment, Vol. 11, Issue 1 https://doi.org/10.1111/j.1365-3040.1988.tb01774.x	journal	January 1988
Intra- and inter-plant variation in xylem cavitation in Betula occidentalis Sperry, J. S.; Saliendra, N. Z. Plant, Cell and Environment, Vol. 17, Issue 11 https://doi.org/10.1111/j.1365-3040.1994.tb02021.x	journal	November 1994
Dynamics of water transport and storage in conifers studied with deuterium and heat tracing techniques Meinzer, F. C.; Brooks, J. R.; Domec, J. -C. Plant, Cell and Environment, Vol. 29, Issue 1 https://doi.org/10.1111/j.1365-3040.2005.01404.x	journal	January 2006
Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees Maherali, Hafiz; Moura, Catarina F.; Caldeira, Maria C. Plant, Cell and Environment, Vol. 29, Issue 4 https://doi.org/10.1111/j.1365-3040.2005.01433.x	journal	April 2006
The role of Ectomycorrhizas in Drought Tolerance of Douglas-Fir Seedlings * Parke, Ennifer L.; Linderman, R. G.; Black, C. H. New Phytologist, Vol. 95, Issue 1 https://doi.org/10.1111/j.1469-8137.1983.tb03471.x	journal	September 1983
Distribution of photosynthetically fixed carbon within root systems of Eucalyptus pilularis plants ectomycorrhizal with Pisolithus tinctorius Cairney, J. W. G.; Ashford, A. E.; Allaway, W. G. New Phytologist, Vol. 112, Issue 4 https://doi.org/10.1111/j.1469-8137.1989.tb00343.x	journal	August 1989
Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? McDowell, Nate; Pockman, William T.; Allen, Craig D. New Phytologist, Vol. 178, Issue 4 https://doi.org/10.1111/j.1469-8137.2008.02436.x	journal	June 2008
Do thick leaves avoid thermal damage in critically low wind speeds? Leigh, A.; Sevanto, S.; Ball, M. C. New Phytologist, Vol. 194, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04058.x	journal	February 2012
Plant genetics and interspecific competitive interactions determine ectomycorrhizal fungal community responses to climate change Gehring, Catherine; Flores-Rentería, Dulce; Sthultz, Christopher M. Molecular Ecology, Vol. 23, Issue 6 https://doi.org/10.1111/mec.12503	journal	October 2013
Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality Mitchell, Patrick J.; O'Grady, Anthony P.; Tissue, David T. New Phytologist, Vol. 197, Issue 3 https://doi.org/10.1111/nph.12064	journal	December 2012
Leaf vein xylem conduit diameter influences susceptibility to embolism and hydraulic decline Scoffoni, Christine; Albuquerque, Caetano; Brodersen, Craig R. New Phytologist, Vol. 213, Issue 3 https://doi.org/10.1111/nph.14256	journal	November 2016
Common garden experiments disentangle plant genetic and environmental contributions to ectomycorrhizal fungal community structure Patterson, Adair; Flores-Rentería, Lluvia; Whipple, Amy New Phytologist, Vol. 221, Issue 1 https://doi.org/10.1111/nph.15352	journal	July 2018
How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die? Sevanto, Sanna; Mcdowell, Nate G.; Dickman, L. Turin Plant, Cell & Environment, Vol. 37, Issue 1 https://doi.org/10.1111/pce.12141	journal	June 2013
Stomatal kinetics and photosynthetic gas exchange along a continuum of isohydric to anisohydric regulation of plant water status: Leaf gas exchange and anisohydry Meinzer, Frederick C.; Smith, Duncan D.; Woodruff, David R. Plant, Cell & Environment, Vol. 40, Issue 8 https://doi.org/10.1111/pce.12970	journal	May 2017
Tree water dynamics in a drying and warming world: Future tree water dynamics Grossiord, Charlotte; Sevanto, Sanna; Borrego, Isaac Plant, Cell & Environment, Vol. 40, Issue 9 https://doi.org/10.1111/pce.12991	journal	June 2017
Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests Bonan, G. B. Science, Vol. 320, Issue 5882 https://doi.org/10.1126/science.1155121	journal	June 2008
Vulnerability of Xylem to Cavitation and Embolism Tyree, M. T.; Sperry, J. S. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 40, Issue 1 https://doi.org/10.1146/annurev.pp.40.060189.000315	journal	June 1989
Carbon Allocation to Ectomycorrhizal Fungi Correlates with Belowground Allocation in Culture Studies Hobbie, Erik A. Ecology, Vol. 87, Issue 3 https://doi.org/10.1890/05-0755	journal	March 2006
Extraction of high-molecular-weight genomic DNA for long-read sequencing of single molecules Mayjonade, Baptiste; Gouzy, Jérôme; Donnadieu, Cécile BioTechniques, Vol. 61, Issue 4 https://doi.org/10.2144/000114460	journal	October 2016
A Dynamic Optimality Principle for Water Use Strategies Explains Isohydric to Anisohydric Plant Responses to Drought Mrad, Assaad; Sevanto, Sanna; Domec, Jean-Christophe Frontiers in Forests and Global Change, Vol. 2 https://doi.org/10.3389/ffgc.2019.00049	journal	August 2019
In vivo Observation of Tree Drought Response with Low-Field NMR and Neutron Imaging Malone, Michael W.; Yoder, Jacob; Hunter, James F. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00564	journal	May 2016
Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils Gil-Martínez, Marta; López-García, Álvaro; Domínguez, María T. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01682	journal	November 2018
Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance Begum, Naheeda; Qin, Cheng; Ahanger, Muhammad Abass Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01068	journal	September 2019
Fungal Aquaporins in Ectomycorrhizal Root Water Transport Xu, Hao; Zwiazek, Janusz J. Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.00302	journal	March 2020
Ectomycorrhizal and Dark Septate Fungal Associations of Pinyon Pine Are Differentially Affected by Experimental Drought and Warming Gehring, Catherine; Sevanto, Sanna; Patterson, Adair Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.582574	journal	October 2020
Neutron Imaging at LANSCE—From Cold to Ultrafast Nelson, Ronald; Vogel, Sven; Hunter, James Journal of Imaging, Vol. 4, Issue 2 https://doi.org/10.3390/jimaging4020045	journal	February 2018
Detection of phytohormones in temperate forest fungi predicts consistent abscisic acid production and a common pathway for cytokinin biosynthesis Morrison, Erin N.; Knowles, Sarah; Hayward, Allison Mycologia, Vol. 107, Issue 2 https://doi.org/10.3852/14-157	journal	March 2015
Potential applications of plant probiotic microorganisms in agriculture and forestry Porto de Souza Vandenberghe, Luciana; Marcela Blandon Garcia, Lina AIMS Microbiology, Vol. 3, Issue 3 https://doi.org/10.3934/microbiol.2017.3.629	journal	January 2017
Risk-taking plants: Anisohydric behavior as a stress-resistance trait Sade, Nir; Gebremedhin, Alem; Moshelion, Menachem Plant Signaling & Behavior, Vol. 7, Issue 7 https://doi.org/10.4161/psb.20505	journal	July 2012

Similar Records

Ectomycorrhizal and Dark Septate Fungal Associations of Pinyon Pine Are Differentially Affected by Experimental Drought and Warming

Journal Article · Tue Oct 20 00:00:00 EDT 2020 · Frontiers in Plant Science · OSTI ID:1688771

Fungal-Bacterial Networks in the Populus Rhizobiome Are Impacted by Soil Properties and Host Genotype

Journal Article · Fri Mar 29 00:00:00 EDT 2019 · Frontiers in Microbiology · OSTI ID:1505327

Ectomycorrhizal fungal community structure of pinyon pines growing in two environmental extremes

Journal Article · Wed Jul 01 00:00:00 EDT 1998 · Ecology · OSTI ID:638269

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biological Science
Earth Sciences
Ecology
Microbiology
Plant sciences

Benefits of symbiotic ectomycorrhizal fungi to plant water relations depend on plant genotype in pinyon pine

Citation Formats

References (67)

Similar Records

Related Subjects