The endosymbiotic origin, diversification and fate of plastids

Abstract

Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.

How life changes itself: The Read–Write (RW) genome

“…After a symbiogenetic fusion, there is extensive intracellular transfer of DNA from the organelle compartments to the nuclear genome [110,111]. Thus, most of the proteins needed for plastid and mitochondrial function are synthesized from nuclear transcripts in the cytoplasm and have to be reimported into the organelle where they act [112].…”

Oxygenic photosynthesis and the distribution of chloroplasts

“…This idea has become a paradigm that is widely illustrated in text books and continues to have considerable support from phylogenomic analyses (Hackett et al 2007;Keeling 2010). Phylogenetic analyses indeed can be constructed to show that extant cyanobacteria fall into a monophyletic line and suggest that the heterocyst formers diverged when atmospheric O 2 concentrations increased (Tomitani et al 2006) around the time of the great oxidation event.…”

“…In spite of numerous publications, the debate continues (cf. in Green 2010;Baurian et al 2010;Deschamps and Moreira 2009;Janouškovec et al 2010;Keeling 2010;Nozaki et al 2009;Ryes-Prieto et al 2008;Stiller 2007 was one chloroplast origin, and if so, what was the most likely host, i.e., is there only one Cinderella slipper and where is the best fit? Some unambiguous structural signs of symbiotic and/or endosymbiotic events were found some years ago when Gibbs (1981) provided significant examples showing that some chloroplasts had two limiting membranes (green and red algae), others were surrounded by three membranes (euglenids, dinoflagellates), while still others had four chloroplast membranes (browns, diatoms, cryptophytes) usually with an additional set of ribosomes on the ''chloroplast endoplasmic reticulum.''…”

Okadaic acid and microcystin insensitive PPP-family phosphatases may represent novel biotechnology targets

“…Interestingly, these protozoa are also known to possess a vestigial plastid (chloroplast remnant) called an apicoplast as a result of their evolution from early photosynthetic, chloroplast containing eukaryotes. 18,19 Moreover, both protozoa have multiple copies of SLP phosphatases, which may be reflective of different biological roles needed to accommodate the complex life cycles of these organisms. Conversely, SLP phosphatase containing bacteria and fungi were found to possess microcystin, 9,10 okadaic acid 11 and inhibitor-2 protein.…”