Evolution of cytokinesis-related protein localization during the emergence of multicellularity in volvocine green algae

Abstract

BackgroundThe volvocine lineage, containing unicellular Chlamydomonas reinhardtii and differentiated multicellular Volvox carteri, is a powerful model for comparative studies aiming at understanding emergence of multicellularity. Tetrabaena socialis is the simplest multicellular volvocine alga and belongs to the family Tetrabaenaceae that is sister to more complex multicellular volvocine families, Goniaceae and Volvocaceae. Thus, T. socialis is a key species to elucidate the initial steps in the evolution of multicellularity. In the asexual life cycle of C. reinhardtii and multicellular volvocine species, reproductive cells form daughter cells/colonies by multiple fission. In embryogenesis of the multicellular species, daughter protoplasts are connected to one another by cytoplasmic bridges formed by incomplete cytokinesis during multiple fission. These bridges are important for arranging the daughter protoplasts in appropriate positions such that species-specific integrated multicellular individuals are shaped. Detailed comparative studies of cytokinesis between unicellular and simple multicellular volvocine species will help to elucidate the emergence of multicellularity from the unicellular ancestor. However, the cytokinesis-related genes between closely related unicellular and multicellular species have not been subjected to a comparative analysis.ResultsHere we focused on dynamin-related protein 1 (DRP1), which is known for its role in cytokinesis in land plants. Immunofluorescence microscopy using an antibody against T. socialis DRP1 revealed that volvocine DRP1 was localized to division planes during cytokinesis in unicellular C. reinhardtii and two simple multicellular volvocine species T. socialis and Gonium pectorale. DRP1 signals were mainly observed in the newly formed division planes of unicellular C. reinhardtii during multiple fission, whereas in multicellular T. socialis and G. pectorale, DRP1 signals were observed in all division planes during embryogenesis.ConclusionsThese results indicate that the molecular mechanisms of cytokinesis may be different in unicellular and multicellular volvocine algae. The localization of DRP1 during multiple fission might have been modified in the common ancestor of multicellular volvocine algae. This modification may have been essential for the re-orientation of cells and shaping colonies during the emergence of multicellularity in this lineage.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1091-z) contains supplementary material, which is available to authorized users.

Embryogenesis of flattened colonies implies the innovation required for the evolution of spheroidal colonies in volvocine green algae

“…We used T. socialis strain NIES-571 [43] to observe embryogenesis in Tetrabaena . As the Gonium strains used in recent genome [15] and morphological studies [34, 44] frequently show abnormal morphology in vegetative colonies and no formation of completely flattened 16-celled colonies (data not shown), we established several new strains of Gonium . We used one of these new strains, G. pectorale strain 2017–0423-IsgGo1, in the present study (Additional file 6: Figure S6).…”

The four-celled Volvocales green alga Tetrabaena socialis exhibits weak photobehavior and high-photoprotection ability

“…Tetrabaena socialis is a volvocine alga, described as the simplest known multicellular organism, comprised of only four cells [ 27 , 28 ]. T .…”

Dynamin-Like Protein B of Dictyostelium Contributes to Cytokinesis Cooperatively with Other Dynamins

“…Arabidopsis has 16 dynamin-like proteins, which are grouped into six subfamilies, of which DRP1, DRP2, and DRP5 are involved in cytokinesis [9,10,11]. Recently, a dynamin-like protein has been reported to contribute to cytokinesis in green algae [12]. In addition, in Streptomyces , dynamin-like proteins (DynA and DynB) stabilize FtsZ rings, thus playing an important role in cytokinesis [13].…”