Cleavage, incomplete inversion, and cytoplasmic bridges in Gonium pectorale (Volvocales, Chlorophyta)

Abstract

Multicellularity arose several times in evolution of eukaryotes. The volvocine algae have full range of colonial organization from unicellular to colonies, and thus these algae are well-known models for examining the evolution and mechanisms of multicellularity. Gonium pectorale is a multicellular species of Volvocales and is thought to be one of the first small colonial organisms among the volvocine algae. In these algae, a cytoplasmic bridge is one of the key traits that arose during the evolution of multicellularity. Here, we observed the inversion process and the cytoplasmic bridges in G. pectorale using time-lapse, fluorescence, and electron microscopy. The cytoplasmic bridges were located in the middle region of the cell in 2-, 4-, 8-, and 16-celled stages and in inversion stages. However, there were no cytoplasmic bridges in the mature adult stage. Cytoplasmic bridges and cortical microtubules in G. pectorale suggest that a mechanism of kinesin-microtubule machinery similar to that in other volvocine algae is responsible for inversion in this species.

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

“…4f, j , 5f , j , n ). Each cell division during multiple fission of multicellular T. socialis [ 5 ], G. pectorale [ 12 ], and other multicellular volvocine algae [ 13 , 43 – 45 ] proceeds through incomplete cytokinesis and the resulting daughter protoplasts are connected to one another by cytoplasmic bridges, whereas daughter protoplasts of C. reinhardtii are completely separated from one another by means of complete cytokinesis [ 9 , 10 ] . The division planes of multicellular volvocine species are therefore different from those of unicellular C. reinhardtii at subcellular and molecular levels.…”

“…The unicellular species C. reinhardtii forms 2 n (n: number of rounds of cell divisions) daughter cells depending on the size of the mother cell [ 11 ], whereas reproductive cells of multicellular volvocine members form 2 n daughter protoplasts that are regulated by mother cell size and genetic control [ 4 ]. These daughter protoplasts are connected to one another by cytoplasmic bridges, which are important for the arrangement of cells within the daughter colony of multicellular volvocine algae [ 4 ] like T. socialis [ 5 ], G. pectorale [ 12 ] and V. carteri [ 13 ]. Considering that both of these multicellular member-specific traits (modulation of daughter cell number and incomplete cytokinesis) are recognized in the tetrabaenacean species T. socialis , comparative molecular analyses of multiple fission between unicellular and multicellular forms is essential to understand the initial steps to multicellularity in this lineage.…”

Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation

“…It is also worth noting that nearly all multicellular volvocine species undergo some form of inversion after cell division (see Hoops and Floyd (1982) and Arakaki et al, (2013) for two interesting exceptions). Gonium is the only genus in which inversion is “incomplete” meaning that a curved sheet of post-mitotic embryonic cells reverses its curvature so that the initially concave face where flagella will form becomes the convex face; but the post-inversion cell sheet never closes into a ball (Iida et al, 2013). In the larger-sized genera with complete inversion— Pandorina , Eudorina , and Pleodorina —embryos start out bowl-shaped and also reverse their curvature, but then undergo a process of closure where the free edges of the embryo join together to form an enclosed ball shape (Hallmann, 2006; Kikuchi, 1978; Marchant, 1977).…”

Volvocine Algae: From Simple to Complex Multicellularity

“…In all members of the Goniaceae and Volvocaceae, during early embryonic development cells are connected through cytoplasmic bridges resulting from incomplete cytokinesis (Gerisch 1959;Bisalputra and Stein 1966;Gottlieb and Goldstein 1977;Marchant 1977;Fulton 1978;Green et al 1981;Iida et al 2013). These bridges ensure the stability of the early embryo.…”