Arakaki Yoko, Kawai-Toyooka Hiroko, Hamamura Yuki, Higashiyama Tetsuya, Noga Akira, Hirono Masafumi, Olson Bradley J S C, Nozaki Hisayoshi
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo, Japan.
Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Aichi, Japan.
PLoS One. 2013 Dec 11;8(12):e81641. doi: 10.1371/journal.pone.0081641. eCollection 2013.
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.
团藻目绿藻是研究多细胞性的“进化时间机器”模型谱系，因为它们涵盖了从单细胞衣藻到500多个细胞的团藻的多细胞性进化转变的整个范围。包括胸状盘藻和卡特氏团藻在内的多细胞团藻目物种通常具有几个共同的形态特征，以作为整合的多细胞生物生存，例如“细胞的旋转不对称性”，使细胞成为个体的组成部分，以及“发育胚胎中原生质体之间的细胞质桥”，以便在新的细胞外基质（ECM）分泌之前维持多细胞个体的物种特异性形态。然而，在位于群居或多细胞团藻目绿藻最基部谱系中的四细胞群居团藻目物种群居四集藻中，尚未对这些形态特征进行研究。在这里，我们建立了群居四集藻的同步培养物，并进行了免疫荧光显微镜和超微结构观察，以阐明这两个形态特征。基于免疫荧光显微镜观察，成熟的群居四集藻群体的四个细胞在形态上是相同的，但在微管小根的排列和基体的分离上具有旋转不对称性，类似于胸状盘藻和卡特氏团藻。超微结构观察清楚地证实，即使在亲代ECM内每个子原生质体形成新的鞭毛后，群居四集藻发育胚胎的原生质体之间仍存在细胞质桥。因此，这两个形态特征可能在群居团藻目绿藻的共同四细胞祖先中进化，并有助于该模型谱系的多细胞个体的细胞数量进一步增加和复杂性提高。群居四集藻是最简单的整合多细胞生物之一，其中四个相同的细胞构成个体。
