Effect of temperature on circadian clock functioning of trees in the context of global warming

Abstract

Plant survival in a warmer world requires the timely adjustment of biological processes to cyclical changes in the new environment. Circadian oscillators have been proposed to contribute to thermal adaptation and plasticity in plants, due to their ability to maintain periodicity in biological rhythms over a wide temperature range, promoting fitness. However, the influence of temperature and circadian clock performance on plant behaviour in natural ecosystems is not well understood. Here we used two co-occurring Nothofagus tree species from the Patagonian forests that are adapted to contrasting thermal environments derived from their different altitudinal profiles. We revealed that the upper thermal limits for accurate clock function are linked to the species' thermal niches and contribute to seedling plasticity in natural environments. We computationally identified 24 circadian clock-related genes, which showed a high degree of structural conservation with clock genes from both annual and perennial species, and very similar patterns of gene expression to those of Arabidopsis thaliana. Warm temperatures produced a strong transcriptomic rearrangement, which affected the expression of clock-related genes and direct clock targets, evidencing the extent of clock functioning disruption by temperature. N. pumilio, the species from colder environments, showed reduced ability to keep rhythmicity at high temperatures compared to N. obliqua, which inhabits warmer zones. Accordingly, N. pumilio, but not N. obliqua, showed a limited oscillator function in warmer zones of the forest, reduced survival, and growth. Together, our results highlight the potential role of a resonating oscillator in ecological adaptation to a warming environment.