Abstract:
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.
