A New Model and Dating for the Evolution of Complex Plastids of Red Alga Origin

Complex plastids, characterized by more than two bounding membranes, still present an evolutionary puzzle for the traditional endosymbiotic theory. Unlike primary plastids that directly evolved from cyanobacteria, complex plastids originated from green or red algae. The Chromalveolata hypothesis proposes a single red alga endosymbiosis that involved the ancestor of all the Chromalveolata lineages: cryptophytes, haptophytes, stramenopiles, and alveolates. As extensive phylogenetic analyses contradict the monophyly of Chromalveolata, serial plastid endosymbiosis models were proposed, suggesting a single secondary red alga endosymbiosis within Cryptophyta, followed by subsequent plastid transfers to other chromalveolates. Our findings based on 97 plastid-encoded markers, 112 species, and robust phylogenetic methods challenge all the existing models. They reveal two independent secondary endosymbioses, one within Cryptophyta and one within stramenopiles, precisely the phylum Ochrophyta, with two different groups of red algae. Consequently, we propose a new model for the emergence of red alga plastid-containing lineages and, through molecular clock analyses, estimate their ages.