Abstract

BackgroundThe molecular history of animal evolution from single-celled ancestors remains a major question in biology, and little is known regarding the evolution of cell cycle regulation during animal emergence. In this study, we conducted a comprehensive evolutionary analysis of CDK and cyclin proteins in metazoans and their unicellular relatives.ResultsOur analysis divided the CDK family into eight subfamilies. Seven subfamilies (CDK1/2/3, CDK5, CDK7, CDK 20, CDK8/19, CDK9, and CDK10/11) are conserved in metazoans and fungi, with the remaining subfamily, CDK4/6, found only in eumetazoans. With respect to cyclins, cyclin C, H, L, Y subfamilies, and cyclin K and T as a whole subfamily, are generally conserved in animal, fungi, and amoeba Dictyostelium discoideum. In contrast, cyclin subfamilies B, A, E, and D, which are cell cycle-related, have distinct evolutionary histories. The cyclin B subfamily is generally conserved in D. discoideum, fungi, and animals, whereas cyclin A and E subfamilies are both present in animals and their unicellular relatives such as choanoflagellate Monosiga brevicollis and filasterean Capsaspora owczarzaki, but are absent in fungi and D. discoideum. Although absent in fungi and D. discoideum, cyclin D subfamily orthologs can be found in the early-emerging, non-opisthokont apusozoan Thecamonas trahens. Within opisthokonta, the cyclin D subfamily is conserved only in eumetazoans, and is absent in fungi, choanoflagellates, and the basal metazoan Amphimedon queenslandica.ConclusionsOur data indicate that the CDK4/6 subfamily and eumetazoans emerged simultaneously, with the evolutionary conservation of the cyclin D subfamily also tightly linked with eumetazoan appearance. Establishment of the CDK4/6-cyclin D complex may have been the key step in the evolution of cell cycle control during eumetazoan emergence.

Highlights

  • The molecular history of animal evolution from single-celled ancestors remains a major question in biology, and little is known regarding the evolution of cell cycle regulation during animal emergence

  • We first analyzed Cyclin-dependent kinases (CDKs) sequences from H. sapiens, N. vectensis, T. adhaerens, A. queenslandica, M. brevicollis, and S. rosetta7 as one group (Figure 1)

  • We found that orthologs of seven CDK subfamilies (CDK7, CDK20, CDK8/19, CDK9/12/13, CDK10/11, CDK1/2/3, and CDK5) are present in basal metazoans T. adhaerens and A. queenslandica, the choanoflagellate M. brevicollis, and/or S. rosetta (Figure 1)

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Summary

Introduction

The molecular history of animal evolution from single-celled ancestors remains a major question in biology, and little is known regarding the evolution of cell cycle regulation during animal emergence. We conducted a comprehensive evolutionary analysis of CDK and cyclin proteins in metazoans and their unicellular relatives. The evolution of metazoans from protozoans is a major milestone in the history of life. Based on a comprehensive phylogenetic analysis of sponge Amphimedon queenslandica proteins, it has been proposed that the emergence of metazoan multicellularity may have been related to the evolution of various genes functioning in cell cycling and growth, programmed cell death, cell-cell and cell-matrix adhesion, developmental signaling and gene regulation, allorecognition and innate immunity, and cell type specialization [28]

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