Origin and evolution of the blue light receptor cryptochromes (CRY1/2) in aquatic angiosperms

Abstract Cryptochromes (CRYs), which are responsible for sensing blue light in plants, play a critical role in regulating blue light signals and circadian rhythms. However, their functions extend beyond light detection, as they also aid plants in adapting to stress and potentially other regulatory mechanisms. Aquatic angiosperms, which independently evolved from various angiosperm lineages, have developed specific adaptations to unique light qualities and environmental stressors found in aquatic habitats compared to terrestrial ones. It was hypothesized that the sequences and regulatory networks of angiosperm CRY1/2 underwent adaptive evolution in different aquatic angiosperm lineages. To test this hypothesis, we compiled comprehensive datasets consisting of 55 green plant genomes (including 37 angiosperm genomes), 80 angiosperm transcriptomes, and 4 angiosperm expression networks. Through comparative analysis, we found that CRY1 originated from a common ancestor of seed plants, whereas CRY2 originated from a common ancestor of land plants. In angiosperms, the CRY1/2 sequences of aquatic lineages exhibited positive selection, and the conserved valine-proline (VP) motif of CRY2 showed a convergent loss in two aquatic species. Co-expressed genes associated with blue light receptors (CRY) showed adaptations to aquatic environments, specifically in relation to flooding and osmotic stress. These discoveries shed light on the adaptive evolution of CRY1/2, encompassing their origins, sequences, and regulatory networks. Furthermore, these results provide valuable insights for investigating the uncharacterized functions and regulatory pathways of CRY and offer potential targets for enhancing growth and adaptation in agricultural plants.