“…During the inversion of Volvox carteri , InvA, a kinesin, is localized in the cytoplasmic bridges connecting daughter protoplasts and interacts with cortical microtubules to move cell bodies against the cytoplasmic bridges, which produces the force that drives the bending of the cell sheet [17]. As embryos of Astrephomene also have cytoplasmic bridges between daughter protoplasts [28], it is possible that an InvA homolog or a similar motor protein localized in cytoplasmic bridges interacts with cortical microtubules; this would occur between, rather than after, cell divisions to rotate daughter protoplasts. Further developmental analyses of Astrephomene should aim to identify the molecular mechanism underlying the rotation of daughter protoplasts in Astrephomene .Fig.…”
BackgroundVolvocine algae, which range from the unicellular Chlamydomonas to the multicellular Volvox with a germ–soma division of labor, are a model for the evolution of multicellularity. Within this group, the spheroidal colony might have evolved in two independent lineages: Volvocaceae and the goniacean Astrephomene. Astrephomene produces spheroidal colonies with posterior somatic cells. The feature that distinguishes Astrephomene from the volvocacean algae is lack of inversion during embryogenesis; the volvocacean embryo undergoes inversion after successive divisions to orient flagella toward the outside. The mechanisms of inversion at the molecular and cellular levels in volvocacean algae have been assessed in detail, particularly in Volvox carteri. However, embryogenesis in Astrephomene has not been subjected to such investigations.ResultsThis study relied on light microscopy time-lapse imaging using an actively growing culture of a newly established strain to conduct a developmental analysis of Astrephomene as well as to perform a comparison with the similar spheroidal volvocacean Eudorina. During the successive divisions involved in Astrephomene embryogenesis, gradual rotation of daughter protoplasts resulted in movement of their apical portions toward the embryonic posterior, forming a convex-to-spheroidal cell sheet with the apical ends of protoplasts on the outside. Differentiation of the posterior somatic cells from the embryo periphery was traced based on cell lineages during embryogenesis. In contrast, in Eudorina, the rotation of daughter protoplasts did not occur during successive cell divisions; however, inversion occurred after such divisions, and a spheroidal embryo was formed. Indirect immunofluorescence microscopy of basal bodies and nuclei verified this difference between Astrephomene and Eudorina in the movement of embryonic protoplasts.ConclusionsThese results suggest different tactics for spheroidal colony formation between the two lineages: rotation of daughter protoplasts during successive cell divisions in Astrephomene, and inversion after cell divisions in Eudorina. This study will facilitate further research into the molecular and genetic mechanisms of the parallel evolution of the spheroidal colony in volvocine algae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0794-x) contains supplementary material, which is available to authorized users.
“…During the inversion of Volvox carteri , InvA, a kinesin, is localized in the cytoplasmic bridges connecting daughter protoplasts and interacts with cortical microtubules to move cell bodies against the cytoplasmic bridges, which produces the force that drives the bending of the cell sheet [17]. As embryos of Astrephomene also have cytoplasmic bridges between daughter protoplasts [28], it is possible that an InvA homolog or a similar motor protein localized in cytoplasmic bridges interacts with cortical microtubules; this would occur between, rather than after, cell divisions to rotate daughter protoplasts. Further developmental analyses of Astrephomene should aim to identify the molecular mechanism underlying the rotation of daughter protoplasts in Astrephomene .Fig.…”
BackgroundVolvocine algae, which range from the unicellular Chlamydomonas to the multicellular Volvox with a germ–soma division of labor, are a model for the evolution of multicellularity. Within this group, the spheroidal colony might have evolved in two independent lineages: Volvocaceae and the goniacean Astrephomene. Astrephomene produces spheroidal colonies with posterior somatic cells. The feature that distinguishes Astrephomene from the volvocacean algae is lack of inversion during embryogenesis; the volvocacean embryo undergoes inversion after successive divisions to orient flagella toward the outside. The mechanisms of inversion at the molecular and cellular levels in volvocacean algae have been assessed in detail, particularly in Volvox carteri. However, embryogenesis in Astrephomene has not been subjected to such investigations.ResultsThis study relied on light microscopy time-lapse imaging using an actively growing culture of a newly established strain to conduct a developmental analysis of Astrephomene as well as to perform a comparison with the similar spheroidal volvocacean Eudorina. During the successive divisions involved in Astrephomene embryogenesis, gradual rotation of daughter protoplasts resulted in movement of their apical portions toward the embryonic posterior, forming a convex-to-spheroidal cell sheet with the apical ends of protoplasts on the outside. Differentiation of the posterior somatic cells from the embryo periphery was traced based on cell lineages during embryogenesis. In contrast, in Eudorina, the rotation of daughter protoplasts did not occur during successive cell divisions; however, inversion occurred after such divisions, and a spheroidal embryo was formed. Indirect immunofluorescence microscopy of basal bodies and nuclei verified this difference between Astrephomene and Eudorina in the movement of embryonic protoplasts.ConclusionsThese results suggest different tactics for spheroidal colony formation between the two lineages: rotation of daughter protoplasts during successive cell divisions in Astrephomene, and inversion after cell divisions in Eudorina. This study will facilitate further research into the molecular and genetic mechanisms of the parallel evolution of the spheroidal colony in volvocine algae.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0794-x) contains supplementary material, which is available to authorized users.
“…The present TEM observations clearly demonstrate the presence of cytoplasmic bridges between daughter protoplasts that form during the process of multiple fission and persist after the maturation of the colony when they form new flagella ( Figure 5 ). Thus T. socialis -specific cell arrangement in a colony should be determined by means of the cytoplasmic bridges before the formation of new ECM during daughter colony formation as observed in G. pectorale [19] , A. gubernaculifera [36] , Pandorina morum [20] , Eudorina elegans [37] , Platydorina caudata [38] , and V. carteri [21] . Moreover, these results suggest that the evolution of cytoplasmic bridges may be a key structural innovation required to keep colonies together and thus multicellular.…”
Volvocine green algae represent the “evolutionary time machine” model lineage for studying multicellularity, because they encompass the whole range of evolutionary transition of multicellularity from unicellular Chlamydomonas to >500-celled Volvox. Multicellular volvocalean species including Gonium pectorale and Volvox carteri generally have several common morphological features to survive as integrated multicellular organisms such as “rotational asymmetry of cells” so that the cells become components of the individual and “cytoplasmic bridges between protoplasts in developing embryos” to maintain the species-specific form of the multicellular individual before secretion of new extracellular matrix (ECM). However, these morphological features have not been studied in the four-celled colonial volvocine species Tetrabaena socialis that is positioned in the most basal lineage within the colonial or multicellular volvocine greens. Here we established synchronous cultures of T. socialis and carried out immunofluorescence microscopic and ultrastructural observations to elucidate these two morphological attributes. Based on immunofluorescence microscopy, four cells of the mature T. socialis colony were identical in morphology but had rotational asymmetry in arrangement of microtubular rootlets and separation of basal bodies like G. pectorale and V. carteri. Ultrastructural observations clearly confirmed the presence of cytoplasmic bridges between protoplasts in developing embryos of T. socialis even after the formation of new flagella in each daughter protoplast within the parental ECM. Therefore, these two morphological attributes might have evolved in the common four-celled ancestor of the colonial volvocine algae and contributed to the further increase in cell number and complexity of the multicellular individuals of this model lineage. T. socialis is one of the simplest integrated multicellular organisms in which four identical cells constitute the individual.
“…Phylogenetic relationships within the colonial Volvocales have been discussed on the basis of morphological data (Crow 19 18, Shaw 19 19,1922, Pickett-Heaps 1975, Hoops and Floyd 1982a, b, c, 1983, Hoops 1984, Greuel and Floyd 1985, Nozaki 1986, Nozaki and Kuroiwa 1992, Buchheim et al 1994, Hoops et al 1994, Nozaki and Itoh 1994, Nozaki et al 1996, the physiological nature of cell walls or gelatinous matrices (Matsuda et al 1987, Matsuda 1988), or rRNA sequence data (Buchheim and Chapman 1991, Larson et al 1992, Buchheim et al 1994. However, as far as we are aware, phylogenetic relationships within the colonial Volvocales have not been examined by protein-coding gene sequence data.…”
The chloroplast‐encoded large subunit of the ribulose‐1, 5‐bisphosphate carboxylase / oxygenase (rbcL) gene was sequenced from 20 species of the colonial Volvocales (the Volvacaceae, Goniaceae, and Tetrabaenaceae) in order to elucidate phylogenetic relationships within the colonial Volvocales. Eleven hundred twenty‐eight base pairs in the coding regions of the (rbcL) gene were analyzed by the neighbor‐joining (NJ) method using three kinds of distance estimations, as well as by the maximum parsimony (MP) method. A large group comprising all the anisogamous and oogamous volvocacean species was resolved in the MP tree as well as in the NJ trees based on overall and synonymous substitutions. In all the trees constructed, Basichlamys and Tetrabaena (Tetrabaenaceae) constituted a very robust phylogenetic group. Although not supported by high bootstrap values, the MP tree and the NJ tree based on nonsynonymous substitutions indicated that the Tetrabaenaceae is the sister group to the large group comprising the Volvocaceae and the Goniaceae. In addition, the present analysis strongly suggested that Pandorina and Astrephomene are monophyletic genera whereas Eudorina is nonmonophyletic. These results are essentially consistent with the results of the recent cladistic analyses of morphological data. However, the monophyly of the Volvocaceae previously supported by four morphological synapomorphies is found only in the NJ tree based on nonsynonymous substitutions (with very low bootstrap values). The genus Volvox was clearly resolved as a polyphyletic group with V. rousseletii Pocock separated from other species of Volvox in the rbcL gene comparisons, although this genus represents a monophyletic group in the previous morphological analyses. Furthermore, none of the rbcL gene trees supported the monophyly of the Goniaceae; Astrephomene was placed in various phylogenetic positions.
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