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Warming Disrupts Plant–Fungal Endophyte Symbiosis More Severely in Leaves Than Roots

  • Joseph D. Edwards
  • , Melanie R. Kazenel
  • , Yiqi Luo
  • , Joshua S. Lynn
  • , Rebecca L. McCulley
  • , Lara Souza
  • , Carolyn Young
  • , Jennifer A. Rudgers
  • , Stephanie N. Kivlin

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

Disruptions to functionally important symbionts with global change will negatively impact plant fitness, with broader consequences for species' abundances, distribution, and community composition. Fungal endophytes that live inside plant leaves and roots could potentially mitigate plant heat stress from global warming. Conversely, disruptions of these symbioses could exacerbate the negative impacts of warming. To better understand the consistency and strength of warming-induced changes to fungal endophytes, we examined fungal leaf and root endophytes in three grassland warming experiments in the US ranging from 2 to 25 years and spanning 2000 km, 12°C of mean annual temperature, and 600 mm of precipitation. We found that experimental warming disrupted symbiosis between plants and fungal endophytes. Colonization of plant tissues by septate fungi decreased in response to warming by 90% in plant leaves and 35% in roots. Warming also reduced fungal diversity and changed community composition in plant leaves, but not roots. The strength, but not direction, of warming effects on fungal endophytes varied by up to 75% among warming experiments. Finally, warming decoupled fungal endophytes from host metabolism by decreasing the correlation between endophyte community and host metabolome dissimilarity. These effects were strongest in the shorter-term experiment, suggesting endophyte-host metabolome function may acclimate to warming over decades. Overall, warming-driven disruption of fungal endophyte community structure and function suggests that this symbiosis may not be a reliable mechanism to promote plant resilience and ameliorate stress responses under global change.

Original languageEnglish
Article numbere70207
JournalGlobal Change Biology
Volume31
Issue number4
DOIs
StatePublished - Apr 2025

Bibliographical note

Publisher Copyright:
© 2025 John Wiley & Sons Ltd.

Funding

J.D.E. was supported by the U.S. National Science Foundation Division of Environmental Biology grant no. 2305863. S.N.K. was supported by NSF grants DEB2217353, DEB 2106065, and DEB1936195 and the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Sciences program under award number DE‐FOA‐0002392. J.A.R. was supported by NSF no. 1354972. RLM was supported by U.S. Department of Energy (08‐SC‐NICCR‐1073), NSF (DEB1021222), the Kentucky Agricultural Experiment Station (KY006045), and a cooperative agreement with the USDA‐ARS Forage Animal Production Research Unit (58‐6440‐7‐135). Funding: J.D.E. was supported by the U.S. National Science Foundation Division of Environmental Biology grant no. 2305863. S.N.K. was supported by NSF grants DEB2217353, DEB 2106065, and DEB1936195 and the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Sciences program under award number DE‐FOA‐0002392. J.A.R. was supported by NSF no. 1354972. R.L.M. was supported by U.S. Department of Energy (08‐SC‐NICCR‐1073), NSF (DEB1021222), the Kentucky Agricultural Experiment Station (KY006045), and a cooperative agreement with the USDA‐ARS Forage Animal Production Research Unit (58‐6440‐7‐135). Funding: J.D.E. was supported by the U.S. National Science Foundation Division of Environmental Biology grant no. 2305863. S.N.K. was supported by NSF grants DEB2217353, DEB 2106065, and DEB1936195 and the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Sciences program under award number DE-FOA-0002392. J.A.R. was supported by NSF no. 1354972. RLM was supported by U.S. Department of Energy (08-SC-NICCR-1073), NSF (DEB1021222), the Kentucky Agricultural Experiment Station (KY006045), and a cooperative agreement with the USDA-ARS Forage Animal Production Research Unit (58-6440-7-135). J.D.E. was supported by the U.S. National Science Foundation Division of Environmental Biology grant no. 2305863. S.N.K. was supported by NSF grants DEB2217353, DEB 2106065, and DEB1936195 and the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Sciences program under award number DE-FOA-0002392. J.A.R. was supported by NSF no. 1354972. R.L.M. was supported by U.S. Department of Energy (08-SC-NICCR-1073), NSF (DEB1021222), the Kentucky Agricultural Experiment Station (KY006045), and a cooperative agreement with the USDA-ARS Forage Animal Production Research Unit (58-6440-7-135).

FundersFunder number
U.S. Department of Energy EPSCoR
Office of Science Programs
USDA-ARS Forage-Animal Production Research Unit58‐6440‐7‐135
National Science Foundation Arctic Social Science ProgramDEB 2106065, DEB2217353, DEB1936195
Biological and Environmental ResearchDEB1021222, DE‐FOA‐0002392, 1354972, 08‐SC‐NICCR‐1073
Kentucky Agricultural Experiment StationKY006045
Division of Environmental Biology2305863

    UN SDGs

    This output contributes to the following UN Sustainable Development Goals (SDGs)

    1. SDG 13 - Climate Action
      SDG 13 Climate Action

    Keywords

    • climate warming
    • community composition
    • fungal endophytes
    • grassland
    • metabolome
    • symbiosis

    ASJC Scopus subject areas

    • Global and Planetary Change
    • Environmental Chemistry
    • Ecology
    • General Environmental Science

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