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The endosymbiotic origin, diversification and fate of plastids - PubMed

  • ️Fri Jan 01 2010

Review

The endosymbiotic origin, diversification and fate of plastids

Patrick J Keeling. Philos Trans R Soc Lond B Biol Sci. 2010.

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.

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Figures

Figure 1.
Figure 1.

Diversity of phototrophic eukaryotes and their plastids. Primary plastids are found in a subset of photosynthetic eukaryotes, most conspicuously in green algae ((a) Ulva, or sea lettuce) and their close relatives the land plants ((b) Typha, or cattail), and in red algae ((c) Chondracanthus, or Turkish towel). Secondary plastids are known in many other lineages, including some large multicellular algae such as kelps and their relatives ((f) Fucus, a brown alga). In some secondary plastids, the nucleus of the endosymbiotic alga is retained and referred to as a nucleomorph ((d) the nucleomorph from Partenskyella glossopodia). In some dinoflagellates, an additional layer of symbiosis, tertiary symbiosis, has made cells of even greater complexity, for example, (e) Durinskia, where five different genetically distinct compartments have resulted from endosymbiosis: the host nucleus (red), the endosymbiont nucleus (blue), the endosymbiont plastid (yellow) and mitochondria from both host and endosymbiont (purple). (g) Chromera velia is a recently described alga that has shed a great deal of light on the evolution of plastids by secondary endosymbiosis. Image (a) is courtesy of K. Ishida, (e) is courtesy of K. Carpenter and all other images are by the author.

Figure 2.
Figure 2.

Schematic view of plastid evolution in the history of eukaryotes. The various endosymbiotic events that gave rise to the current diversity and distribution of plastids involve divergences and reticulations whose complexity has come to resemble an electronic circuit diagram. Endosymbiosis events are boxed, and the lines are coloured to distinguish lineages with no plastid (grey), plastids from the green algal lineage (green) or the red algal lineage (red). At the bottom is the single primary endosymbiosis leading to three lineages (glaucophytes, red algae and green algae). On the lower right, a discrete secondary endosymbiotic event within the euglenids led to their plastid. On the lower left, a red alga was taken up in the ancestor of chromalveolates. From this ancestor, haptophytes and cryptomonads (as well as their non-photosynthetic relatives like katablepharids and telonemids) first diverged. After the divergence of the rhizarian lineage, the plastid appears to have been lost, but in two subgroups of Rhizaria, photosynthesis was regained: in the chlorarachniophytes by secondary endosymbiosis with a green alga, and in Paulinella by taking up a cyanobacterium (many other rhizarian lineages remain non-photosynthetic). At the top left, the stramenopiles diverged from alveolates, where plastids were lost in ciliates and predominantly became non-photosynthetic in the apicomplexan lineage. At the top right, four different events of plastid replacement are shown in dinoflagellates, involving a diatom, haptophyte, cryptomonad (three cases of tertiary endosymbiosis) and green alga (a serial secondary endosymbiosis). Most of the lineages shown have many members or relatives that are non-photosynthetic, but these have not all been shown for the sake of clarity.

Figure 3.
Figure 3.

Plastid genome structure variation in photosynthetic and non-photosynthetic lineages. Genomes from the green lineage are on the left, the red lineage on the right and the glaucophyte genome is shown in the centre in blue. Inverted repeats encoding rRNA operons are shown as thickened lines. Numbers with names indicate the per cent of the genome that encodes proteins. Where both are available, a genome from a non-photosynthetic species is shown within that of a photosynthetic relative to show the scale of reduction. In general, plastid genomes map as circles and have an inverted repeat that encodes the ribosomal RNA operon. The major exception to this is the plastid genome of dinoflagellates, which has been reduced in coding capacity and broken down to single gene mini-circles. In some rare cases, the repeat and/or operon has been lost (e.g. in Helicosporidium and Chromera), or the rRNA operon is encoded in tandem (e.g. in Euglena). Non-photosynthetic plastids are greatly reduced in size, but tend to retain the overall structure of their photosynthetic counterparts.

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