Morphogenesis in the Family Volvocaceae: Different Tactics for Turning an Embryo Right-side Out

• Published in: Protist Vol. 157; no. 4; pp. 445 - 461
• Main Author: Hallmann, Armin
• Format: Journal Article
• Language: English
• Published: Germany Elsevier GmbH 01.10.2006
• Subjects: Cell Division; Chlamydomonas; Chlorophyta - growth & development; embryogenesis; Eudorina unicocca; evolution; Evolution, Molecular; Gonium pectorale; inversion; Morphogenesis; Pandorina morum; Volvocaceae; Volvocales; Volvox; Volvox carteri; Volvox globator; Volvox tertius; ECM: extracellular matrix; Volvocales; embryogenesis; Volvox; inversion; evolution; Chlamydomonas
• ISSN: 1434-4610; 1618-0941
• DOI: 10.1016/j.protis.2006.05.010

Green algae of the family Volvocaceae provide an unrivalled opportunity to analyze an evolutionary pathway leading from unicellularity to multicellularity with division of labor. One key step required for achieving multicellularity in this group was the development of a process for turning an embryo inside out: a morphogenetic process that is now known as “inversion,” and that is a diagnostic feature of the group. Inversion is essential because at the end of its embryonic cleavage divisions, each volvocacean embryo contains all of the cells that will be present in an adult, but the flagellar ends of all cells are pointed toward the interior, rather than toward the exterior where they will need to be to function in locomotion. Inversion has been studied in greatest detail in Volvox carteri, but although all other volvocacean species have to struggle with the same awkward situation of being wrong-side out at the end of cleavage, they do it in rather different ways. Here, the inversion processes of six different volvocacean species ( Gonium pectorale, Pandorina morum, Eudorina unicocca, Volvox carteri, Volvox tertius, and Volvox globator) are compared, in order to illustrate the variation in inversion patterns that exists within this family. The simplest inversion process occurs in the plate-shaped alga Gonium pectorale and the most complicated in the spherical alga Volvox globator. Gonium pectorale goes only from a concave-bowl shape to a slightly convex plate. In Volvox globator, the posterior hemisphere inverts completely before the anterior pole opens and the anterior hemisphere slides over the already-inverted posterior hemisphere; during both halves of this inversion process, the regions of maximum cell-sheet curvature move progressively, as radially symmetrical waves, along the posterior–anterior axis.