Chlorophyll c–Containing Plastid Relationships Based on Analyses of a Multigene Data Set with All Four Chromalveolate Lineages

Abstract

The chlorophyll c-containing algae comprise four major lineages: dinoflagellates, haptophytes, heterokonts, and cryptophytes. These four lineages have sometimes been grouped together based on their pigmentation, but cytological and rRNA data had suggested that they were not a monophyletic lineage. Some molecular data support monophyly of the plastids, while other plastid and host data suggest different relationships. It is uncontroversial that these groups have all acquired plastids from another eukaryote, probably from the red algal lineage, in a secondary endosymbiotic event, but the number and sequence of such event(s) remain controversial. Understanding chlorophyll c-containing plastid relationships is a first step towards determining the number of endosymbiotic events within the chromalveolates. We report here phylogenetic analyses using 10 plastid genes with representatives of all four chromalveolate lineages. This is the first organellar genomescale analysis to include both haptophytes and dinoflagellates. Concatenated analyses support the monophyly of the chlorophyll c-containing plastids and suggest that cryptophyte plastids are the basal member of the chlorophyll c-containing plastid lineage. The gene psbA, which has at times been used for phylogenetic purposes, was found to differ from the other genes in its placement of the dinoflagellates and the haptophytes, and in its lack of support for monophyly of the green and red plastid lineages. Overall, the concatenated data are consistent with a single origin of chlorophyll c-containing plastids from red algae. However, these data cannot test several key hypothesis concerning chromalveolate host monophyly, and do not preclude the possibility of serial transfer of chlorophyll c-containing plastids among distantly related hosts.

Origin and Distribution of Calvin Cycle Fructose and Sedoheptulose Bisphosphatases in Plantae and Complex Algae: A Single Secondary Origin of Complex Red Plastids and Subsequent Propagation via Tertiary Endosymbioses

“…Instead, we propose that the origin of haptophytes, cryptophytes, diatoms, and peridinin-containing dinoflagellates is best interpreted as the result of a late and unique secondary endosymbiosis with a red alga followed by subsequent tertiary or even quaternary endosymbioses (Bachvaroff et al 2005;Delwiche 1999;Petersen et al 2006). Eukaryote-to-eukaryote endosymbioses with complex algae have already been documented for dinoflagellates that independently reduced either a haptophyte, or a diatom or a cryptophyte to a complex plastid (Chesnick et al 1997;Hackett et al 2003;Tengs et al 2000).…”

“…In contrast, a common ancestry of stramenopiles (oomycetes, heterokont algae), haptophytes, cryptophytes, and alveolates (ciliates, apicomplexa, dinoflagellates) via a single secondary endosymbiosis with a rhodophyte was recently proposed and is known as the "chromalveolate hypothesis" (Cavalier-Smith 1999). This hypothesis is supported by plastid phylogenies in which the "chromalveolate" lineages are monophyletic and nested within red algae (Bachvaroff et al 2005;Yoon et al 2002). At the nuclear level, three genes of the Calvin cycle, i.e.…”

Did the peridinin plastid evolve through tertiary endosymbiosis? A hypothesis

“…This alternative is offered by the mechanism of tertiary endosymbiosis. Gibbs (1978) had been the first to suggest that the peridinin plastid evolved from a haptophyte, and the scenario was recently discussed in more detail by Bodył (2005) and Bachvaroff et al (2005). However, the concatenated tree of plastid proteins generated by Yoon et al (2005) suggests that the ancestor of the peridinin plastid could have been a heterokont rather than a haptophyte (Fig.…”

After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c

“…Chloroplast multi-gene trees support the red algal origin of the chromist plastid, probably from within the more advanced groups of red algae (Bachvaroff et al 2005;Rodriguez-Ezpeleta et al 2005;Khan et al 2007;SanchezPuerta et al 2007;Wang et al 2008;Le Corguillé et al 2009;Janouškovec et al 2010). The monophyly of chromist plastids is also usually supported, but the branching order of the three chromist groups depends on the methods used and the corrections applied to avoid problems due to rapidly evolving sequences and compositional bias (Iida et al 2007;.…”