Origin of Zygnematophyceae algae from mitotically dividing anydrophyte zygotes

Viktor Zarsky , Vojtech Zarsky, Jakub Dan Zarsky

It is now generally accepted that Zygnematophyceae evolved from the multicellular common ancestor with Embryopyta - Anydrophyta - by reduction to unicellular state. Here we propose and discuss possible scenarios how this reduction might have proceeded - either via stepwise evolutionary reduction or via an abrupt life-cycle reduction, establishing a single cell lineage and rendering a number of developmental genes redundant. Based on phylogenomic, developmental and physiological comparative analyses we argue that Zygnematophyceae are not product of a stepwise loss of multicellularity, but most probably evolved from multicellular into the single-cell organization by the evolutionary “quantum leap”- by mitotic division of Anydrophyta zygotes. We consider an alternative origin from mitotically dividing haploid cells as less probable. According to our hypothesis and in contrast to Embryophyta where anydrophytes dividing zygotes resulted in embryo/sporophyte evolution, these mitotically dividing zygotes have intermittently lost sexual reproduction and initiated a new stable, originally diploid stress-resistant single-cell lineage of Zygnematophyceae algae. Our hypothesis therefore proposes a common origin of sporophyte and Zygnematophyceae based on the propensity of Anydrophyta zygotes for mitotic divisions. This scenario is in concord with short phylogenetic branch leading to Zygnematophyceae indicating an abrupt evolutionary reduction, with multicellular genomic equipment of morphologically simple single-cell algae, with the loss of flagella, loss of oogamy and with de novo conjugative sex evolution. Diploid status of vegetative cells and peculiar life cycle ploidy changes - including reduction of ploidy before gametic cell division - observed during sexual reproduction of several zygnematophyte representatives might be also explained by zygotic diploid origin of Zygnematophyceae.