Identification and expression of functionally conserved circadian clock genes in lichen-forming fungi

Abstract

Lichen-forming fungi establish stable symbioses with green algae or cyanobacteria. Many species have broad distributions, both in geographic and ecological space, making them ideal subjects to study organism-environment interactions. However, little is known about the specific mechanisms that contribute to environmental adaptation in lichen-forming fungi. The circadian clock provides a well-described mechanism that contributes to regional adaptation across a variety of species, including fungi. Here, we identify the putative circadian clock components in phylogenetically divergent lichen-forming fungi. The core circadian genes (frq, wc-1, wc-2, frh) are present across the Fungi, including 31 lichen-forming species, and their evolutionary trajectories mirror overall fungal evolution. Comparative analyses of the clock genes indicate conserved domain architecture among lichen- and non-lichen-forming taxa. We used RT-qPCR to examine the core circadian loop of two unrelated lichen-forming fungi, Umbilicaria pustulata (Lecanoromycetes) and Dermatocarpon miniatum (Eurotiomycetes), to determine that the putative frq gene is activated in a light-dependent manner similar to the model fungus Neurospora crassa. Together, these results demonstrate that lichen-forming fungi retain functional light-responsive mechanisms, including a functioning circadian clock. Our findings provide a stepping stone into investigating the circadian clock in the lichen symbiosis, e.g. its role in adaptation, and in synchronizing the symbiotic interaction.

Synchronization of Circadian Clock Gene Expression inArabidopsisandHyaloperonospora arabidopsidisand its Impact on Host-Pathogen Interactions

“…Circadian rhythms have long been known to govern various aspects of plant physiology, from growth, differentiation, metabolism and flowering to responses to environmental stresses (Annunziata et al, 2018;Luklova et al, 2019;Liang et al, 2022;Zhu et al, 2022). Similarly, microbial microorganisms including fungi and cyanobacteria have their own circadian rhythms that influence processes such as metabolism, nutrient uptake and virulence (Brody, 2019;Valim et al, 2022). Previously we showed that light plays a significant role in the development of Hpa (Telli et al, 2020).…”

Circadian clock and temperature-associated genes vary along climate gradients in lichenized fungi

“…Previous work has elucidated the existing variation within species ofUmbilicaria and shown that different ecotypes are associated with distinct climate zones along elevation gradients (Dal Grande et al, 2017;Rolshausen et al, 2022). The putative core clock components have been identified in several lichen species, including theUmbilicaria species above, and the functional conservation of the FRQ-WCC core circadian clock loop has been implicated by experimental evidence (Valim et al, 2022). To examine whether the circadian clock -and light-and temperature-mediated responses more generally -are associated with the distinct ecotypes observed in U. pustulata,and U. phaea populations, we asked the following questions: Is there variation in the core circadian clock genes along elevation gradients?…”

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

“…Previous work has elucidated the existing variation within species of Umbilicaria and shown that different ecotypes are associated with distinct climate zones along elevation gradients (Dal Grande et al., 2017; Rolshausen et al., 2022). The putative core clock components have been identified in several lichen species, including the Umbilicaria species above, and the functional conservation of the FRQ‐WCC core circadian clock loop has been implicated by experimental evidence (Valim et al., 2022). To examine whether the circadian clock—and light‐ and temperature‐mediated responses more generally—are associated with the distinct ecotypes observed in U. pustulata , and U. phaea populations, we asked the following questions: Is there variation in the core circadian clock genes along elevation gradients?…”