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

Abstract

Changing climates can cause shifts in temperature and precipitation, resulting in warming and drought in some regions. Although each of these factors has been shown to detrimentally affect forest ecosystems worldwide, information on the impacts of the combined effects of warming and drought is lacking. Forest trees rely on mutualistic root-associated fungi that contribute significantly to plant health and protection against climate stresses. We used a six-year, ecosystem-scale temperature and precipitation manipulation experiment targeted to simulate the climate in 2100 in the Southwestern United States to quantify the effects of drought, warming and combined drought and warming on the root colonization (abundance), species composition and diversity of ectomycorrhizal fungi (EMF), and dark septate fungal endophytes in a widespread woodland tree, pinyon pine (Pinus edulis E.). Our results show that pinyon shoot growth after 6 years of these treatments was reduced more by drought than warming. The combined drought and warming treatment reduced the abundance and diversity of EMF more than either treatment alone. Individual ectomycorrhizal fungal taxa, including the drought tolerant Cenococcum geophilum, were present in all treatments but the combined drought and warming treatment. The combined drought and warming treatment also reduced the abundance of dark septate endophytes (DSE),more » but did not affect their diversity or species composition. The current year shoot growth of the trees correlated positively with ectomycorrhizal fungal diversity, highlighting the importance of diversity in mutualistic relationships to plant growth. Our results suggest that EMF may be more important than DSE to aboveground growth in P. edulis, but also more susceptible to the negative effects of combined climate stressors.« less

Authors:
 [1]; ORCiD logo [2];  [1];  [3]; ORCiD logo [2]
  1. Northern Arizona Univ., Flagstaff, AZ (United States)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. Montana State Univ., Bozeman, MT (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1688771
Report Number(s):
LA-UR-20-25014
Journal ID: ISSN 1664-462X
Grant/Contract Number:  
89233218CNA000001; ER20160373
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 11; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; dark septate endophytes; ectomycorrhizal fungi; fungal diversity; root-associated fungi; tree drought response; pinyon pine; dryland ecosystems; climate change

Citation Formats

Gehring, Catherine, Sevanto, Sanna Annika, Patterson, Adair, Ulrich, Danielle E. M., and Kuske, Cheryl Rae. Ectomycorrhizal and Dark Septate Fungal Associations of Pinyon Pine Are Differentially Affected by Experimental Drought and Warming. United States: N. p., 2020. Web. doi:10.3389/fpls.2020.582574.
Gehring, Catherine, Sevanto, Sanna Annika, Patterson, Adair, Ulrich, Danielle E. M., & Kuske, Cheryl Rae. Ectomycorrhizal and Dark Septate Fungal Associations of Pinyon Pine Are Differentially Affected by Experimental Drought and Warming. United States. https://doi.org/10.3389/fpls.2020.582574
Gehring, Catherine, Sevanto, Sanna Annika, Patterson, Adair, Ulrich, Danielle E. M., and Kuske, Cheryl Rae. Tue . "Ectomycorrhizal and Dark Septate Fungal Associations of Pinyon Pine Are Differentially Affected by Experimental Drought and Warming". United States. https://doi.org/10.3389/fpls.2020.582574. https://www.osti.gov/servlets/purl/1688771.
@article{osti_1688771,
title = {Ectomycorrhizal and Dark Septate Fungal Associations of Pinyon Pine Are Differentially Affected by Experimental Drought and Warming},
author = {Gehring, Catherine and Sevanto, Sanna Annika and Patterson, Adair and Ulrich, Danielle E. M. and Kuske, Cheryl Rae},
abstractNote = {Changing climates can cause shifts in temperature and precipitation, resulting in warming and drought in some regions. Although each of these factors has been shown to detrimentally affect forest ecosystems worldwide, information on the impacts of the combined effects of warming and drought is lacking. Forest trees rely on mutualistic root-associated fungi that contribute significantly to plant health and protection against climate stresses. We used a six-year, ecosystem-scale temperature and precipitation manipulation experiment targeted to simulate the climate in 2100 in the Southwestern United States to quantify the effects of drought, warming and combined drought and warming on the root colonization (abundance), species composition and diversity of ectomycorrhizal fungi (EMF), and dark septate fungal endophytes in a widespread woodland tree, pinyon pine (Pinus edulis E.). Our results show that pinyon shoot growth after 6 years of these treatments was reduced more by drought than warming. The combined drought and warming treatment reduced the abundance and diversity of EMF more than either treatment alone. Individual ectomycorrhizal fungal taxa, including the drought tolerant Cenococcum geophilum, were present in all treatments but the combined drought and warming treatment. The combined drought and warming treatment also reduced the abundance of dark septate endophytes (DSE), but did not affect their diversity or species composition. The current year shoot growth of the trees correlated positively with ectomycorrhizal fungal diversity, highlighting the importance of diversity in mutualistic relationships to plant growth. Our results suggest that EMF may be more important than DSE to aboveground growth in P. edulis, but also more susceptible to the negative effects of combined climate stressors.},
doi = {10.3389/fpls.2020.582574},
journal = {Frontiers in Plant Science},
number = ,
volume = 11,
place = {United States},
year = {2020},
month = {10}
}

Works referenced in this record:

Swarm: robust and fast clustering method for amplicon-based studies
journal, January 2014

  • Mahé, Frédéric; Rognes, Torbjørn; Quince, Christopher
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.593

Methodology and performance of a rainfall manipulation experiment in a piñon–juniper woodland
journal, April 2012

  • Pangle, Robert E.; Hill, Judson P.; Plaut, Jennifer A.
  • Ecosphere, Vol. 3, Issue 4
  • DOI: 10.1890/ES11-00369.1

Long-term response of forest productivity to climate change is mostly driven by change in tree species composition
journal, April 2018


A meta-analysis of plant responses to dark septate root endophytes
journal, January 2011


Amelioration of nitrate uptake under salt stress by ectomycorrhiza with and without a Hartig net
journal, March 2019

  • Sa, Gang; Yao, Jun; Deng, Chen
  • New Phytologist, Vol. 222, Issue 4
  • DOI: 10.1111/nph.15740

Temperature as a potent driver of regional forest drought stress and tree mortality
journal, September 2012

  • Park Williams, A.; Allen, Craig D.; Macalady, Alison K.
  • Nature Climate Change, Vol. 3, Issue 3
  • DOI: 10.1038/nclimate1693

Accurate Estimation of Fungal Diversity and Abundance through Improved Lineage-Specific Primers Optimized for Illumina Amplicon Sequencing
journal, October 2016

  • Taylor, D. Lee; Walters, William A.; Lennon, Niall J.
  • Applied and Environmental Microbiology, Vol. 82, Issue 24
  • DOI: 10.1128/AEM.02576-16

Prolonged warming and drought modify belowground interactions for water among coexisting plants
journal, September 2018

  • Grossiord, Charlotte; Sevanto, Sanna; Bonal, Damien
  • Tree Physiology, Vol. 39, Issue 1
  • DOI: 10.1093/treephys/tpy080

Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements
journal, May 2009

  • Breshears, David D.; Myers, Orrin B.; Meyer, Clifton W.
  • Frontiers in Ecology and the Environment, Vol. 7, Issue 4
  • DOI: 10.1890/080016

How do trees die? A test of the hydraulic failure and carbon starvation hypotheses: How do trees die?
journal, June 2013

  • Sevanto, Sanna; Mcdowell, Nate G.; Dickman, L. Turin
  • Plant, Cell & Environment, Vol. 37, Issue 1
  • DOI: 10.1111/pce.12141

Predicting Abundance of 80 Tree Species Following Climate Change in the Eastern United States
journal, November 1998

  • Iverson, Louis R.; Prasad, Anantha M.
  • Ecological Monographs, Vol. 68, Issue 4
  • DOI: 10.2307/2657150

Hidden Fungi, Emergent Properties: Endophytes and Microbiomes
journal, September 2011


The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications
journal, October 2018

  • Nilsson, Rolf Henrik; Larsson, Karl-Henrik; Taylor, Andy F. S.
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1022

Tree genetics defines fungal partner communities that may confer drought tolerance
journal, September 2017

  • Gehring, Catherine A.; Sthultz, Christopher M.; Flores-Rentería, Lluvia
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 42
  • DOI: 10.1073/pnas.1704022114

Responses to chronic N fertilization of ectomycorrhizal piñon but not arbuscular mycorrhizal juniper in a piñon-juniper woodland
journal, October 2010


Genetically based susceptibility to herbivory influences the ectomycorrhizal fungal communities of a foundation tree species
journal, November 2009


Ectomycorrhizal fungi and the biotrophy–saprotrophy continuum
journal, April 2008


A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi
journal, July 1990


Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine
journal, October 1991

  • Gehring, Catherine A.; Whitham, Thomas G.
  • Nature, Vol. 353, Issue 6344
  • DOI: 10.1038/353556a0

Girdling Affects Ectomycorrhizal Fungal (EMF) Diversity and Reveals Functional Differences in EMF Community Composition in a Beech Forest
journal, January 2010

  • Pena, R.; Offermann, C.; Simon, J.
  • Applied and Environmental Microbiology, Vol. 76, Issue 6
  • DOI: 10.1128/AEM.01703-09

Fungal symbionts alter plant responses to global change
journal, July 2013

  • Kivlin, Stephanie N.; Emery, Sarah M.; Rudgers, Jennifer A.
  • American Journal of Botany, Vol. 100, Issue 7
  • DOI: 10.3732/ajb.1200558

Ectomycorrhizal fungal diversity increases phosphorus uptake efficiency of European beech
journal, May 2018

  • Köhler, Julia; Yang, Nan; Pena, Rodica
  • New Phytologist, Vol. 220, Issue 4
  • DOI: 10.1111/nph.15208

Tree water dynamics in a drying and warming world: Future tree water dynamics
journal, June 2017

  • Grossiord, Charlotte; Sevanto, Sanna; Borrego, Isaac
  • Plant, Cell & Environment, Vol. 40, Issue 9
  • DOI: 10.1111/pce.12991

Fungal melanins: a review
journal, December 1998

  • Butler, M. J.; Day, A. W.
  • Canadian Journal of Microbiology, Vol. 44, Issue 12
  • DOI: 10.1139/w98-119

Plant phenotypic plasticity in a changing climate
journal, December 2010


The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress
journal, December 2013


Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture
journal, January 2012


Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress
journal, September 2013


Fungal relationships and structural identity of their ectomycorrhizae
journal, June 2006


Consequences for ectomycorrhizal fungi of the selective loss or gain of pine across landscapes
journal, December 2014

  • Karst, Justine; Randall, Morgan J.; Gehring, Catherine A.
  • Botany, Vol. 92, Issue 12
  • DOI: 10.1139/cjb-2014-0063

Lineages of ectomycorrhizal fungi revisited: Foraging strategies and novel lineages revealed by sequences from belowground
journal, December 2013


Towards a unified paradigm for sequence-based identification of fungi
journal, September 2013

  • Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy
  • Molecular Ecology, Vol. 22, Issue 21
  • DOI: 10.1111/mec.12481

Associations between fungal root endophytes and grass dominance in arid highlands
journal, June 2020


Temperature niche position and breadth of ectomycorrhizal fungi: Reduced diversity under warming predicted by a nested community structure
journal, October 2018

  • Miyamoto, Yumiko; Terashima, Yoshie; Nara, Kazuhide
  • Global Change Biology, Vol. 24, Issue 12
  • DOI: 10.1111/gcb.14446

Ectomycorrhizal fungal response to warming is linked to poor host performance at the boreal‐temperate ecotone
journal, September 2016

  • Fernandez, Christopher W.; Nguyen, Nhu H.; Stefanski, Artur
  • Global Change Biology, Vol. 23, Issue 4
  • DOI: 10.1111/gcb.13510

Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review
journal, August 2014


A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests
journal, February 2010

  • Allen, Craig D.; Macalady, Alison K.; Chenchouni, Haroun
  • Forest Ecology and Management, Vol. 259, Issue 4
  • DOI: 10.1016/j.foreco.2009.09.001

Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought?
journal, June 2008


Experimental drought and heat can delay phenological development and reduce foliar and shoot growth in semiarid trees
journal, September 2015

  • Adams, Henry D.; Collins, Adam D.; Briggs, Samuel P.
  • Global Change Biology, Vol. 21, Issue 11
  • DOI: 10.1111/gcb.13030

Genetically informed ecological niche models improve climate change predictions
journal, September 2016

  • Ikeda, Dana H.; Max, Tamara L.; Allan, Gerard J.
  • Global Change Biology, Vol. 23, Issue 1
  • DOI: 10.1111/gcb.13470

Extraction of high-molecular-weight genomic DNA for long-read sequencing of single molecules
journal, October 2016

  • Mayjonade, Baptiste; Gouzy, Jérôme; Donnadieu, Cécile
  • BioTechniques, Vol. 61, Issue 4
  • DOI: 10.2144/000114460

Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios: Carbohydrate dynamics in piñon-juniper woodland
journal, October 2014

  • Dickman, Lee T.; Mcdowell, Nate G.; Sevanto, Sanna
  • Plant, Cell & Environment, Vol. 38, Issue 4
  • DOI: 10.1111/pce.12441

Regulation and acclimation of leaf gas exchange in a piñon-juniper woodland exposed to three different precipitation regimes: Rainfall manipulation in piñon-juniper woodland
journal, March 2013

  • Limousin, Jean-Marc; Bickford, Christopher P.; Dickman, Lee T.
  • Plant, Cell & Environment, Vol. 36, Issue 10
  • DOI: 10.1111/pce.12089

Manipulative experiments demonstrate how long-term soil moisture changes alter controls of plant water use
journal, August 2018


Localization of helotialean fungi on ectomycorrhizae of Castanopsis cuspidata visualized by in situ hybridization
journal, October 2017


Widespread Increase of Tree Mortality Rates in the Western United States
journal, January 2009


Lack of acclimation of leaf area:sapwood area ratios in piñon pine and juniper in response to precipitation reduction and warming
journal, September 2018

  • McBranch, Natalie A.; Grossiord, Charlotte; Adams, Henry
  • Tree Physiology, Vol. 39, Issue 1
  • DOI: 10.1093/treephys/tpy066

Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought: Hydraulic limits in a piñon-juniper woodland
journal, April 2012


Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species
journal, August 2009


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Warming combined with more extreme precipitation regimes modifies the water sources used by trees
journal, September 2016

  • Grossiord, Charlotte; Sevanto, Sanna; Dawson, Todd E.
  • New Phytologist, Vol. 213, Issue 2
  • DOI: 10.1111/nph.14192

Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought
journal, April 2009

  • Adams, Henry D.; Guardiola-Claramonte, Maite; Barron-Gafford, Greg A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 17
  • DOI: 10.1073/pnas.0901438106

Pezizalean mycorrhizas and sporocarps in ponderosa pine (Pinus ponderosa) after prescribed fires in eastern Oregon, USA
journal, August 2004


Context dependent effects of ectomycorrhizal species richness on tree seedling productivity
journal, June 2001


Climate change influences mycorrhizal fungal–plant interactions, but conclusions are limited by geographical study bias
journal, February 2020

  • Bennett, Alison E.; Classen, Aimée T.
  • Ecology, Vol. 101, Issue 4
  • DOI: 10.1002/ecy.2978

Pulse dynamics and microbial processes in aridland ecosystems: Pulse dynamics in aridland soils
journal, March 2008


Common garden experiments disentangle plant genetic and environmental contributions to ectomycorrhizal fungal community structure
journal, July 2018

  • Patterson, Adair; Flores-Rentería, Lluvia; Whipple, Amy
  • New Phytologist, Vol. 221, Issue 1
  • DOI: 10.1111/nph.15352

Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: A review
journal, March 2019


Regional vegetation die-off in response to global-change-type drought
journal, October 2005

  • Breshears, D. D.; Cobb, N. S.; Rich, P. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 42
  • DOI: 10.1073/pnas.0505734102

Precipitation, not air temperature, drives functional responses of trees in semi-arid ecosystems
journal, October 2016

  • Grossiord, Charlotte; Sevanto, Sanna; Adams, Henry D.
  • Journal of Ecology, Vol. 105, Issue 1
  • DOI: 10.1111/1365-2745.12662

Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi
journal, October 1998


Legacy effects of tree mortality mediated by ectomycorrhizal fungal communities
journal, June 2019

  • Mueller, Rebecca C.; Scudder, Crescent M.; Whitham, Thomas G.
  • New Phytologist, Vol. 224, Issue 1
  • DOI: 10.1111/nph.15993

Mycorrhizal Fungi as Mediators of Soil Organic Matter Dynamics
journal, November 2019


Promotion of mycorrhiza formation and growth of willows by the bacterial strain Sphingomonas sp. 23L on fly ash
journal, December 2008


Ectomycorrhizas and water relations of trees: a review
journal, December 2010


Stem radial growth and water storage responses to heat and drought vary between conifers with differing hydraulic strategies: Semiarid conifers responses to drought and heat
journal, June 2018

  • Manrique-Alba, Àngela; Sevanto, Sanna; Adams, Henry D.
  • Plant, Cell & Environment, Vol. 41, Issue 8
  • DOI: 10.1111/pce.13340

Novel Root Fungal Consortium Associated with a Dominant Desert Grass
journal, March 2008

  • Porras-Alfaro, A.; Herrera, J.; Sinsabaugh, R. L.
  • Applied and Environmental Microbiology, Vol. 74, Issue 9
  • DOI: 10.1128/AEM.02769-07

Survival of Mycorrhiza Formed by Cenococcum Geophilum fr. in dry Soils
journal, December 1982


Plant genetics and interspecific competitive interactions determine ectomycorrhizal fungal community responses to climate change
journal, October 2013

  • Gehring, Catherine; Flores-Rentería, Dulce; Sthultz, Christopher M.
  • Molecular Ecology, Vol. 23, Issue 6
  • DOI: 10.1111/mec.12503

Contrasting effects of intra- and interspecific identity and richness of ectomycorrhizal fungi on host plants, nutrient retention and multifunctionality
journal, September 2016

  • Hazard, Christina; Kruitbos, Laura; Davidson, Hazel
  • New Phytologist, Vol. 213, Issue 2
  • DOI: 10.1111/nph.14184

Paraphoma root rot of alfalfa ( Medicago sativa ) in Inner Mongolia, China
journal, November 2019

  • Cao, S.; Liang, Q. W.; Nzabanita, C.
  • Plant Pathology, Vol. 69, Issue 2
  • DOI: 10.1111/ppa.13131

Reductions in tree performance during hotter droughts are mitigated by shifts in nitrogen cycling: Mitigation of hotter droughts
journal, August 2018

  • Grossiord, Charlotte; Gessler, Arthur; Reed, Sasha C.
  • Plant, Cell & Environment, Vol. 41, Issue 11
  • DOI: 10.1111/pce.13389