Circadian clock‐ and temperature‐associated genes contribute to overall genomic differentiation along elevation in lichenized fungi

Abstract

Circadian regulation is linked to local environmental adaptation, and many species with broad climatic niches display variation in circadian genes. Here, we hypothesize that lichenizing fungi occupying different climate zones tune their metabolism to local environmental conditions with the help of their circadian systems. We study two species of the genus Umbilicaria occupying similar climatic niches (Mediterranean and the cold temperate) in different continents. Using homology to Neurospora crassa genes, we identify gene sets associated with circadian rhythms (11 core, 39 peripheral genes) as well as temperature response (37 genes). Nucleotide diversity of these genes is significantly correlated with mean annual temperature, minimum temperature of the coldest month and mean temperature of the coldest quarter. Furthermore, we identify altitudinal clines in allele frequencies in several non‐synonymous substitutions in core clock components, for example, white collar‐like, frh‐like and various ccg‐like genes. A dN/dS approach revealed a few significant peripheral clock‐ and temperature‐associated genes (e.g. ras‐1‐like, gna‐1‐like) that may play a role in fine‐tuning the circadian clock and temperature‐response machinery. An analysis of allele frequency changes demonstrated the strongest evidence for differentiation above the genomic background in the clock‐associated genes in U. pustulata. These results highlight the likely relevance of the circadian clock in environmental adaptation, particularly frost tolerance, of lichens. Whether or not the fungal clock modulates the symbiotic interaction within the lichen consortium remains to be investigated. We corroborate the finding of genetic variation in clock components along altitude—not only latitude—as has been reported in other species.

Genetic basis of local adaptation in the cold-tolerant mangrove Kandelia obovata

“…This supports the notion that winter temperature shapes mangrove distributions and assemblage composition in China ( Wu et al., 2018 ). Local temperature has been consistently identified as significant drivers of varying selective pressures in many organisms, such as grey mangrove ( Friis et al., 2024 ), lichen-forming fungi ( Valim et al., 2023 ), and mountain pine ( Méndez-Cea et al., 2023 ). In this study, the Fuding and Shenzhen populations showed a higher proportion of fixation in temperature-associated SNPs ( Figure 5C ) compared with genome-wide SNPs ( Figure 1C ), implying that natural selection has facilitated the rapid evolution of genes related to local adaptation.…”