Oogamy: inventing the sexes.

The male-female dichotomy has evolved independently in nearly all lineages of multicellular organisms. Why this should be the case is still uncertain, but recent studies of mating-type genes in green algae open a promising new way to explore molecular-genetic aspects of the evolution of dichotomous sexes.

A twelve-step program for evolving multicellularity and a division of labor.

The volvocine algae provide an unrivalled opportunity to explore details of an evolutionary pathway leading from a unicellular ancestor to multicellular organisms with a division of labor between different cell types. Members of this monophyletic group of green flagellates range in complexity from unicellular Chlamydomonas through a series of extant organisms of intermediate size and complexity to Volvox, a genus of spherical organisms that have thousands of cells and a germ-soma division of labor. It is estimated that these organisms all shared a common ancestor about 50 +/- 20 MYA. Here we outline twelve important ways in which the developmental repertoire of an ancestral unicell similar to modern C. reinhardtii was modified to produce first a small colonial organism like Gonium that was capable of swimming directionally, then a sequence of larger organisms (such as Pandorina, Eudorina and Pleodorina) in which there was an increasing tendency to differentiate two cell types, and eventually Volvox carteri with its complete germ-soma division of labor.

A kinesin, invA, plays an essential role in volvox morphogenesis.

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.

Seeking the ultimate and proximate causes of volvox multicellularity and cellular differentiation.

Volvox and its relatives provide an exceptional model for integrative studies of the evolution of multicellularity and cellular differentiation. The volvocine algae range in complexity from unicellular Chlamydomonas through several colonial genera with a single cell type, to multicellular Volvox with its germ-soma division of labor. Within the monophyletic family Volvocaceae, several species of Volvox have evolved independently in different lineages, the ultimate cause presumably being the advantage that large size and cellular differentiation provide in competing for limiting resources such as phosphorous. The proximate causes of this type of evolutionary transition are being studied in V. carteri. All volvocine algae except Volvox exhibit biphasic development: cells grow during a motile, biflagellate phase, then they lose motility and divide repeatedly during the reproductive phase. In V. carteri three kinds of genes transform this ancestral biphasic program into a dichotomous one that generates non-motile reproductive cells and biflagellate somatic cells with no reproductive potential: first the gls genes act in early embryos to cause asymmetric division and production of large-small sister-cell pairs; then lag genes act in the large cells to repress the biflagellate half of the ancestral program, while regA acts in the small cells to repress the reproductive half of the program. Molecular-genetic analysis of these genes is progressing, as will be illustrated with regA, which encodes a transcription factor that acts in somatic cells to repress nuclear genes encoding chloroplast proteins. Repression of chloroplast biogenesis prevents these obligately photoautotrophic cells from growing, and since they cannot grow, they cannot reproduce.

kangaroo, a mobile element from Volvox carteri, is a member of a newly recognized third class of retrotransposons.

Retrotransposons play an important role in the evolution of genomic structure and function. Here we report on the characterization of a novel retrotransposon called kangaroo from the multicellular green alga, Volvox carteri. kangaroo elements are highly mobile and their expression is developmentally regulated. They probably integrate via double-stranded, closed-circle DNA intermediates through the action of an encoded recombinase related to the lambda-site-specific integrase. Phylogenetic analysis indicates that kangaroo elements are closely related to other unorthodox retrotransposons including PAT (from a nematode), DIRS-1 (from Dictyostelium), and DrDIRS1 (from zebrafish). PAT and kangaroo both contain split direct repeat (SDR) termini, and here we show that DIRS-1 and DrDIRS1 elements contain terminal features structurally related to SDRs. Thus, these mobile elements appear to define a third class of retrotransposons (the DIRS1 group) that are unified by common structural features, genes, and integration mechanisms, all of which differ from those of LTR and conventional non-LTR retrotransposons.