A Kinesin, InvA, Plays an Essential Role in Volvox Morphogenesis

Abstract

In Volvox carteri adults, reproductive cells called gonidia are enclosed within a spherical monolayer of biflagellate somatic cells. Embryos must "invert" (turn inside out) to achieve this configuration, however, because at the end of cleavage the gonidia are on the outside and the flagellar ends of all somatic cells point inward. Generation of a bend region adequate to turn the embryo inside out involves a dramatic change in cell shape, plus cell movements. Here, we cloned a gene called invA that is essential for inversion and found that it codes for a kinesin localized in the cytoplasmic bridges that link all cells to their neighbors. In invA null mutants, cells change shape normally, but are unable to move relative to the cytoplasmic bridges. A normal bend region cannot be formed and inversion stops. We conclude that the InvA kinesin provides the motile force that normally drives inversion to completion.

Phylogeny and Molecular Evolution of the Green Algae

“…During inversion, cells move relative to the cytoplasmic bridges in order to turn the embryo inside-out, so that the flagella end up on the outer surface (Gerisch, 1959;Marchant, 1977;Fulton, 1978;Green et al, 1981). This process seems to have evolved by co-option of genes already present in the unicellular ancestor of V. carteri: three genes known to be involved in V. carteri inversion (invA, invB, invC) have highly conserved orthologs in C. reinhardtii (Nishii et al, 2003;Ueki & Nishii, 2009;Nishii & Miller, 2010), and an invA ortholog (IAR1) in C. reinhardtii is capable of rescuing V. carteri invA mutants (Nishii et al, 2003).…”

Embryoids, organoids and gastruloids: new approaches to understanding embryogenesis

“…and contraction, provide the mechanical force for complete embryo inversion (Hohn et al, 2015). The transfer of mechanical force across the embryo is achieved by a kinesin motor that is localized at the cytosolic bridges connecting all the cells (Nishii et al, 2003). Another recent study implied that, although the cellular and signaling events in gastrulation can be vastly different among species, it is the mechanics of gastrulation that might be evolutionarily conserved (Brunet et al, 2013).…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…Full inversion of spheroidal colonies has been examined carefully in V. carteri and V. globator (Viamontes and Kirk 1977;Nishii and Ogihara 1999;Nishii 2003;Ueki and Nishii 2009;Höhn and Hallmann 2011), which use different but related mechanisms to invert. In both species, inversion is driven by coordinated cell-shape changes that move through the spheroid along the anteroposterior axis and drive cell sheet bending and involution.…”

“…carteri inversionless mutants have provided insights into the processes governing type A inversion. One such mutant, invA, affects a volvocine algal kinesin that localizes to the cytoplasmic bridge region of cells (Nishii 2003). The function of InvA protein is postulated to involve moving the cytoplasmic bridges relative to the rest of the cell along longitudinal microtubules to effect cell-shape changes and tissue bending.…”