Expansion of Cyclin D and CDK1 Paralogs in Oikopleura dioica, a Chordate Employing Diverse Cell Cycle Variants

Abstract

Proliferative and endoreduplicative cell cycles are used to variable extents during the ontogeny of individual organisms and in different evolutionary lineages. Chordate growth and development is typically dominated by proliferative cycles, but the urochordate, Oikopleura dioica, has systemically elaborated a number of endocycling modes to support rapid development and growth in an extraordinarily short chordate life cycle. Here, we identify the O. dioica cyclin and cyclin-dependent kinase (CDK) complements and assess their deployment with respect to mitotic, meiotic, and endoreduplicative life cycle phases. Oikopleura dioica's "transcriptional" cyclin and CDK complements are similar to other complex invertebrates, whereas both the "cell cycle" cyclin and CDK complements display astonishing amplifications centered on the cyclin D, cyclin B, and CDK1 families. Somatic endocycles in O. dioica involve downregulation of cyclins B and A, as in other endocycle model systems, but are also characterized by overlapping expression of an array of cyclin D isoforms. Amplification of the mitotic CDK1 family to five paralogs, which continue to be expressed in endocycling phases, is unexpected as suppression of CDK1 activity is central to endocycle transitions in Drosophila and mammals. This amplification is unique among metazoans, and substitutions in odCDK1 paralogs in the nearly invariant cyclin interaction PSTAIRE helix show striking parallels to those in the only other known eukaryotic CDK1 paralogs, plant CDKA and CDKB. As plant CDK1 paralogs exhibit an expanded repertoire of cyclin partners, including cyclin D, the evolutionary coexpansion of odCDK1 and odCyclin D families suggests that multiple CDK1-cyclin D complexes may modulate spatiotemporal control of kinase activity and substrate specificity in diverse cell cycle variants.