Deppisch P et al. , The Gain and Loss of Cryptochrome/Photolyase Fa...

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Genes (Basel) null;139:. doi: 10.3390/genes13091613.

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

Deppisch P , Helfrich-Förster C , Senthilan PR .

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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.

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	Figure 1. Schematic overview of six main members of the CRY/PL family based on their function in major model organisms and references given in the introduction. (A,B) The photosensitive photolyases repair UV-induced pyrimidine-pyrimidone dimer mutations in DNA using blue light. Depending on the type of mutation they repair, they are called 6-4 photolyases (pyrimidine-pyrimidone-6-4 photoproduct) or CPD photolyases (cyclobutane-pyrimidine dimer). Plant PCRYs (C) are photosensitive and directly or indirectly affect the transcription of several genes whose functions are also linked to the circadian clock. The Drosophila light-sensitive cryptochrome (DCRY) is activated by blue light and destabilizes TIMELESS, resulting in a resetting of the circadian clock (D). The mammalian light insensitive MCRY, which is also involved in the circadian clock, acts as an indirect transcription factor, and inhibits its own expression (E). DASH-CRYs (F) act as a link between different members of the CRY/PL family. They appear to be involved in both the circadian clock and the repair of mutations in single-stranded DNA.
	Figure 2. Unrooted phylogenetic tree revealing the four main clusters formed by CRY/PL family members. The 6-4 photolyase cluster (I) includes the mammalian type MCRY (red), the Drosophila-type DCRY (blue), CRY4 involved in magnetoreception (purple) and the 6-4 photolyase itself (pink). The CPDII cluster (II) consists of CPDII photolyases (light green). The CPDI/III cluster (III) includes the CPDI (dark brown) & CPDIII photolyase (light brown), the plant cryptochrome PCRY (dark green), and the PCRY-like (turquoise). The DASH cluster (IV) consists of DASH-CRY (orange) and the plant photolyase PPL (yellow). Branches we could not precisely assign are shown in grey.
	Figure 3. Schematic representation of the CRY/PL subfamilies along with their most frequent motifs. Only motifs that occur with a frequency of at least 50% are shown. A detailed list of all motifs, their sequences and references can be found in Supplementary Materials S4, and protein sequence alignments of all subfamilies can be found in Supplementary Materials S5. In the case of m2pl, both insect (13%) and non-insect (68%) data were combined, and for cc3, data from microorganisms & animals (59%) were summed with those from plants (5%).
	Figure 4. CRY/PL distribution within the metazoan phylum. The prevalence of a subfamily within a phylum is indicated in percent, with only percentages > 10% shown for clarity. The total number of animals examined in each phylum is given in parentheses beside the phylum name. See Supplementary Materials S8 for more details.
	Figure 5. (A) Distribution of CRY/PL subfamilies within Chordata. Cephalochordata and Tunicata are shown with gray lines, while animals belonging to the subphylum Craniata are labeled with dark red lines. The prevalence of a CRY/PL subfamily within a taxon is given as a percentage. For clarity, only percentages above 10% are given. The total number of animals studied in each taxon is given in parentheses next to its name. Nearly all animals studied, with only a few exceptions, have an MCRY duplication leading to MCRY1 (light red) and MCRY2 (dark red). (B) Characteristic motifs of MCRY1, MCRY2 and the standard MCRYs (MCRY st) found in non-chordates. Type-specific motifs are shown in color. The motifs mnc, I, II, and 4a are novel motifs. All other motifs are explained in Figure 3.
	Figure 6. Distribution of CRY/PL subfamilies within the orders of Arthropoda. The occurrence rate of a subfamily within an order is given as a percentage, only percentages > 10% are shown for clarity. The total number of animals studied in each phylum is given in parentheses next to the order name. Chelicerates, crustaceans, and hexapods form the main arthropod subgroup. The major CRY/PL members of arthropods are MCRY, DCRY, and the photolyases 6-4 and CPDII. Many crustaceans also carry the DASH CRY. The four major CRY/PLs are found in all subgroups of the Hexapoda substrain, even though they are not equally abundant in all groups. MCRY is the most important CRY/PL of the hexapods. In Collembola and in individual insects of the cohort Paraneoptera and Holometabola the DASH-CRY is also present.
	Figure 7. The origin of the CRY/PL members. (I) All three photolyases 6-4, CPDII and CPDI/III are found in all three domains of Eukaryota, Bacteria and Archaea. (II) DASH-CRY is mainly found in Eukaryota and in Bacteria. However, one archaeon is known to have DASH-CRY as well. (III) In eukaryotes, the PCRY-like protein arose next. It is found in all kingdoms except fungi. We assume that it has been lost in the fungi studied. (IV) Origin of PCRY and PPL in some algae and in Viridiplantae. (V) Origin of MCRY, which occurs in both Cnidaria and Bilateria. Its origin is therefore attributed to planulozoans. (VI) Origin of ACRY in certain cnidarians. (VII) Origin of DCRY, which occurs only in Bilateria, but in both Deuterostomia and Protostomia. (VIII) Origin of CRY4 in some chordates. The number of organisms tested is shown in parentheses next to the taxonomy name. The archaeon Halorhabdus utahensis and the hemichordate Ptychodera flava (both marked with *) were investigated in the studies by Mei and Dvornyk (2015) [19] and Kotwica-Rolinska et al. (2021) [43].

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