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New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy.

ABSTRACT: BACKGROUND:The evolution of oogamy from isogamy, an important biological event, can be summarized as follows: morphologically similar gametes (isogametes) differentiated into small "male" and large "female" motile gametes during anisogamy, from which immotile female gametes (eggs) evolved. The volvocine green algae represent a model lineage to study this type of sex evolution and show two types of gametic unions: conjugation between isogametes outside the parental colonies (external fertilization during isogamy) and fertilization between small motile gametes (sperm) and large gametes (eggs) inside the female colony (internal fertilization during anisogamy and oogamy). Although recent cultural studies on volvocine algae revealed morphological diversity and molecular genetic data of sexual reproduction, an intermediate type of union between these two gametic unions has not been identified. RESULTS:We identified a novel colonial volvocine genus, Colemanosphaera, which produces bundles of spindle-shaped male gametes through successive divisions of colonial cells. Obligately anisogamous conjugation between male and female motile gametes occurred outside the female colony (external fertilization during anisogamy). This new genus contains 16- or 32-celled spheroidal colonies similar to those of the volvocine genera Yamagishiella and Eudorina. However, Colemanosphaera can be clearly distinguished from these two genera based on its sister phylogenetic position to the enigmatic flattened colonial volvocine Platydorina and external fertilization during anisogamy. Two species of Colemanosphaera were found in a Japanese lake; these species are also distributed in European freshwaters based on a published sequence of an Austrian strain and the original description of Pandorina charkowiensis from Ukraine. CONCLUSIONS:Based on phylogeny and morphological data, this novel genus exhibits a missing link between Platydorina and the typical spheroidal colonial volvocine members such as Pandorina or Yamagishiella. Considering the external obligate anisogamy, oogamy evolution may have been preceded by the transition from external to internal fertilization during anisogamy within the volvocine green algae.

SUBMITTER: Nozaki H

PROVIDER: S-EPMC4015742 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy.

Nozaki Hisayoshi H Yamada Toshihiro K TK Takahashi Fumio F Matsuzaki Ryo R Nakada Takashi T

BMC evolutionary biology 20140303 1

<h4>Background</h4>The evolution of oogamy from isogamy, an important biological event, can be summarized as follows: morphologically similar gametes (isogametes) differentiated into small "male" and large "female" motile gametes during anisogamy, from which immotile female gametes (eggs) evolved. The volvocine green algae represent a model lineage to study this type of sex evolution and show two types of gametic unions: conjugation between isogametes outside the parental colonies (external fert ...[more]

PMID: 24589311

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Project description:Colonial Volvocine Algae (CVA) are of great significance for biological evolution study, but little is presently known about their biogeographic distribution. Meanwhile, with the impact of climate change and human activities, their effects on the distribution and structures of CVA communities also remain largely unknown. Herein, the biogeography of CVA was investigated in the Yangtze River basin, 172 sampling sites were set up within a catchment area of 1,800,000 km2, and the distribution and community composition of CVA were studied using single-molecule real-time sequencing and metabarcoding technology based on the full-length 18S sequence. In 76 sampling sites, CVA was discovered in two families, eight genera, and nine species. Eudorina and Colemanosphaera were the main dominant genus. Based on the result of the random forest model and Eta-squared value, the distribution of CVA was significantly influenced by water temperature, altitude, and TP. CVA could be suitably distributed at an average water temperature of 22°C, an average TP concentration of 0.06 mg/L, and an altitude lower than 3,920 m. To assess the effects of anthropogenic pollution on the structures and co-occurrence patterns of CVA communities, we used a stress index calculated by 10 environmental factors to divide the CVA community into low and high pollution group. Network analysis showed that greater pollution levels would have a negative impact on the co-occurrence patterns and diversity of the CVA community. Finally, to study the scientific distribution of CVA under current and future climate change scenarios, we analyzed the climate suitability regionalization of CVA with the maximum entropy model based on 19 climatic factors and four climate scenarios from 2021 to 2040 published by CMIP6. Our results reveal the suitable areas of CVA, and temperature is an important environmental factor affecting the distribution of CVA. With the change of climate in the future, the Three Gorges Reservoir Area, Chaohu Lake, and Taihu Lake are still highly suitable areas for CVA, but the habitat of CVA may be fragmented, and more thorough temporal surveys and sampling of the sediment or mud are needed to investigate the fragmentation of CVA.

Project description:The 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.Here 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.These 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.

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New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy.

Publications

New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy.

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