Abstract
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.
Highlights
Organisms on Earth exhibit a wide array of morphological and genetic diversity
Entry into multiple fission occurs during darkness, the C. reinhardtii cell cycle can be highly synchronized to light-dark cycles [13]
The life cycles of the Volvocaceae, V. carteri can be synchronized to light-dark cycles even though its life cycle is 48 h compared to a 24 h cycle for C. reinhardtii [11]
Summary
Organisms on Earth exhibit a wide array of morphological and genetic diversity. This diversity originates from evolution of organisms since the origin of life on the Earth, via evolutionary transitions in individuality (ETIs), in which individuals gathered to become different individuals of higher-level [1]. The volvocine green algae include a complete range of ETIs, from unicellular Chlamydomonas to multicellular Volvox [4,5,6]. The genomes of Chlamydomonas reinhardtii [7] and Volvox carteri [8] have been sequenced, and phylogeny within this group is well resolved [9], [10], and culture and molecular genetic methods have been established [11,12,13]. The volvocine algae offer an excellent opportunity for studying multicellular evolution (Figure 1)
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