Developmental mechanisms that yield multicellular diversity are proving to be well conserved within lineages, generating interest in their origins in unicellular ancestors. We report that molecular regulation of the haploid-diploid transition in Chlamydomonas, a unicellular green soil alga, shares common ancestry with differentiation pathways in land plants. Two homeoproteins, Gsp1 and Gsm1, contributed by gametes of plus and minus mating types respectively, physically interact and translocate from the cytosol to the nucleus upon gametic fusion, initiating zygote development. Their ectopic expression activates zygote development in vegetative cells and, in a diploid background, the resulting zygotes undergo a normal meiosis. Gsm1/Gsp1 dyads share sequence homology with and are functionally related to KNOX/BELL dyads regulating stem-cell (meristem) specification in land plants. We propose that combinatorial homeoprotein-based transcriptional control, a core feature of the fungal/animal radiation, may have originated in a sexual context and enabled the evolution of land-plant body plans.