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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.
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Increasing prevalence of plant-fungal symbiosis across two centuries of environmental change
Species' distributions and abundances are shifting in response to climate change. Most species harbor microbial symbionts that have the potential to influence these responses. Mutualistic microbial symbionts may provide resilience to environmental change by protecting their hosts from increasing stress. However, environmental change that disrupts these interactions may lead to declines in hosts or symbionts. Microbes preserved within herbarium specimens offer a unique opportunity to quantify changes in microbial symbiosis across broad temporal and spatial scales. We asked how the prevalence of seed-transmitted fungal symbionts of grasses (Epichloe endophytes), which can protect hosts from abiotic stress, have changed over time in response to climate change, and how these changes vary across host species' ranges. Specifically, we analyzed 2,346 herbarium specimens of three grass host species collected over the last two centuries (1824 -- 2019) for the presence or absence of endophyte symbiosis, and evaluated spatial and temporal trends in endophyte prevalence. We found that endophytes increased in prevalence over the last two centuries from ca. 25% prevalence to ca. 75% prevalence, on average, across three host species. We also found that changes in prevalence were associated with observed changes in seasonal climate drivers; notably increasing precipitation corresponding to each host species' peak growing season and changes in off-peak season variability in precipitation. Our analysis performed favorably in an out-of-sample predictive test with contemporary data, however we identified greater local-scale variability in endophyte prevalence in contemporary data compared to historic data, suggesting that model fusion may be an important step moving forward. Our results provide novel evidence for a cryptic biological response to climate change that may contribute to the resilience of host-microbe symbiosis through context-dependent benefits that confer a fitness advantage to symbiotic hosts under environmental change.
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- Award ID(s):
- 2208857
- PAR ID:
- 10609730
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Posted Content:
- https://doi.org/10.1101/2024.09.05.611506
