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Abstract Climate change is rapidly altering the distribution of suitable habitats for many species as well as their pathogenic microbes. For many pathogens, including vector‐borne diseases of humans and agricultural pathogens, climate change is expected to increase transmission and lead to pathogen range expansions. However, if pathogens have a lower heat tolerance than their host, increased warming could generate so‐called thermal refugia for hosts. Predicting the outcomes of warming on disease transmission requires detailed knowledge of the thermal tolerances of both the host and the pathogen. Such thermal tolerance studies are generally lacking for fungal pathogens of wild plant populations, despite the fact that plants form the base of all terrestrial communities. Here, we quantified three aspects of the thermal tolerance (growth, infection, and propagule production) of the naturally occurring fungal pathogenMicrobotryum lychnidis‐dioicae, which causes a sterilizing anther‐smut disease on the herbaceous plantSilene latifolia. We also quantified two aspects of host thermal tolerance: seedling survival and flowering rate. We found that temperatures >30°C reduced the ability of anther‐smut spores to germinate, grow, and conjugate in vitro. In addition, we found that high temperatures (30°C) during or shortly after the time of inoculation strongly reduced the likelihood of infection in seedlings. Finally, we found that high summer temperatures in the field temporarily cured infected plants, likely reducing transmission. Notably, high temperatures did not reduce survival or flowering of the host plants. Taken together, our results show that the fungus is considerably more sensitive to high temperatures than its host plant. A warming climate could therefore result in reduced disease spread or even local pathogen extirpation, leading to thermal refugia for the host.
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Mechanisms of Pine Disease Susceptibility Under Experimental Climate Change
Climate change (CC) conditions projected for many temperate areas of the world, expressed by way of excessive temperatures and low water availability, will impact forest health directly by means of abiotic stress but also by predisposing trees to pathogenic attack. However, we do not yet know how such environmental conditions alter the physiology and metabolism of trees to render them more susceptible to pathogens. To explore these mechanisms, we conditioned 3-year-old Austrian pine saplings to a simulated CC environment (combined drought and elevated temperatures), followed by pathogenic inoculation with two sister fungal species characterized by contrasting aggressiveness, Diplodia sapinea (aggressive) and D. scrobiculata (less aggressive). Lesion lengths resulting from infection were measured after 3 weeks to determine phenotypes, while dual transcriptomics analysis was conducted on tissues collected from the margins of developing lesions on separate branches 72 h post inoculation. As expected, climate change conditions enhanced host susceptibility to the less aggressive pathogen, D. scrobiculata , to a level that was not statistically different from the more aggressive D. sapinea . Under controlled climate conditions, D. sapinea induced suppression of critical pathways associated with host nitrogen and carbon metabolism, while enhancing its own carbon assimilation. This was accompanied by suppression of host defense-associated pathways. In contrast, D. scrobiculata infection induced host nitrogen and fatty acid metabolism as well as host defense response. The CC treatment, on the other hand, was associated with suppression of critical host carbon and nitrogen metabolic pathways, alongside defense associated pathways, in response to either pathogen. We propose a new working model integrating concurrent host and pathogen responses, connecting the weakened host phenotype under CC treatment with specific metabolic compartments. Our results contribute to a richer understanding of the mechanisms underlying the oft-observed increased susceptibility to fungal infection in trees under conditions of low water availability and open new areas of investigation to further integrate our knowledge in this critical aspect of tree physiology and ecology.
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- Award ID(s):
- 1638999
- PAR ID:
- 10373357
- Date Published:
- Journal Name:
- Frontiers in Forests and Global Change
- Volume:
- 5
- ISSN:
- 2624-893X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/ffgc.2022.872584
