The Gain and Loss of Cryptochrome/Photolyase Family Members during Evolution

Abstract

The cryptochrome/photolyase (CRY/PL) family represents an ancient group of proteins fulfilling two fundamental functions. While photolyases repair UV-induced DNA damages, cryptochromes mainly influence the circadian clock. In this study, we took advantage of the large number of already sequenced and annotated genes available in databases and systematically searched for the protein sequences of CRY/PL family members in all taxonomic groups primarily focusing on metazoans and limiting the number of species per taxonomic order to five. Using BLASTP searches and subsequent phylogenetic tree and motif analyses, we identified five distinct photolyases (CPDI, CPDII, CPDIII, 6-4 photolyase, and the plant photolyase PPL) and six cryptochrome subfamilies (DASH-CRY, mammalian-type MCRY, Drosophila-type DCRY, cnidarian-specific ACRY, plant-specific PCRY, and the putative magnetoreceptor CRY4. Manually assigning the CRY/PL subfamilies to the species studied, we have noted that over evolutionary history, an initial increase of various CRY/PL subfamilies was followed by a decrease and specialization. Thus, in more primitive organisms (e.g., bacteria, archaea, simple eukaryotes, and in basal metazoans), we find relatively few CRY/PL members. As species become more evolved (e.g., cnidarians, mollusks, echinoderms, etc.), the CRY/PL repertoire also increases, whereas it appears to decrease again in more recent organisms (humans, fruit flies, etc.). Moreover, our study indicates that all cryptochromes, although largely active in the circadian clock, arose independently from different photolyases, explaining their different modes of action.

Co‐action of COP1, SPA and cryptochrome in light signal transduction and photomorphogenesis of the moss Physcomitrium patens

“…In that regard, PpCRY1 behaved similar to Arabidopsis CRY1 and differently from Arabidopsis CRY2. In angiosperms, cryptochromes underwent a gene duplication event resulting in CRY1 and CRY2 with partially overlapping but distinct functions in Arabidopsis (Deppisch et al., 2022; Lariguet & Dunand, 2005; Ponnu & Hoecker, 2022). Importantly, they differ in their interactions with the SPA proteins: although the CCE domain of CRY1 interacts with the WD‐repeat domain of SPA1, CRY2 interacts via its PHR domain with the kinase domain of SPA1 (Lian et al., 2011; Liu et al., 2011; Zuo et al., 2011).…”

Light signaling in plants—a selective history

“…Studies of the evolutionary history of photolyase/cryptochrome families indicate that ancient DNA photolyases may have duplicated multiple times during evolution, resulting in expansion of the photolyase/cryptochrome families and divergence of plant and animal CRYs more than 1 billion years ago ( Lin and Todo 2005 ; Kim et al 2014 ; Mei and Dvornyk 2015 ; Deppisch et al 2022 ). This is consistent with the hypothesis that CRYs are the first sensory photoreceptors that evolved in plants ( Han et al 2019 ).…”

“…It appears that CRYs in different eukaryotes may have arisen independently from different photolyases, which would explain the different modes of action of the different CRYs in different eukaryotes, despite their common role in regulating the circadian clock ( Cashmore 2003 ; Sancar 2016 ). Up to now, neither canonical CRY nor CRY-DASH DNA photolyase has been found in Archaea ( Deppisch et al 2022 ). Thus CRYs might not have existed 2 billion years ago when eukaryotes diverged from Archaea ( Doolittle 1997 ; Williams et al 2013 ), making the evolutionary history of CRYs about 1 to 2 billion years old.…”

The structural and functional roles of the flavin cofactor FAD in mammalian cryptochromes

“…It is commonly accepted that cryptochromes are evolutionary related to DNA photolyases ( Miles et al, 2020 ; Deppisch et al, 2022 ). Both protein groups share structural homology and thus are usually considered as one cryptochrome/photolyase family.…”