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CORE Metadata, citation and similar papers at core.ac.uk Provided by University of Queensland eSpace Plastid Origin and Advanced article Evolution Article Contents . Introduction Cheong Xin Chan, Rutgers University, New Brunswick, New Jersey, USA . Primary Plastids and Endosymbiosis . Secondary (and Tertiary) Plastids Debashish Bhattacharya, Rutgers University, New Brunswick, New Jersey, USA . Nonphotosynthetic Plastids . Plastid Theft . Plastid Origin and Eukaryote Evolution . Concluding Remarks Online posting date: 15th November 2011 Plastids (or chloroplasts in plants) are organelles within organisms that emerged ca. 2.8 billion years ago (Olson, which photosynthesis takes place in eukaryotes. The ori- 2006), followed by the evolution of eukaryotic algae ca. 1.5 gin of the widespread plastid traces back to a cyano- billion years ago (Yoon et al., 2004) and finally by the rise of bacterium that was engulfed and retained by a plants ca. 500 million years ago (Taylor, 1988). Photosynthetic reactions occur within the cytosol in heterotrophic protist through a process termed primary prokaryotes. In eukaryotes, however, the reaction takes endosymbiosis. Subsequent (serial) events of endo- place in the organelle, plastid (e.g. chloroplast in plants). symbiosis, involving red and green algae and potentially The plastid also houses many other reactions that are other eukaryotes, yielded the so-called ‘complex’ plastids essential for growth and development in algae and plants; found in photosynthetic taxa such as diatoms, dino- for example, the biosynthesis of fatty acids, biosynthesis of flagellates and euglenids. The field of plastid research also amino acids and carbohydrate storage. See also: Cyano- includes nonphotosynthetic organelles (apicoplasts) bacteria; Evolution of Photosynthesis; Photosynthesis; within the parasitic apicomplexans and the temporary Photosynthesis: The Calvin Cycle; Photosynthetic Carbon sequestration (‘theft’) of plastids by heterotrophic Metabolism; Plant Chloroplasts and Other Plastids organisms (kleptoplasty) such as the sea slug Elysia chlor- Various forms of plastids have been found in eukaryotes, otica. The gain and loss of plastids, and nonlineal gene from the most ‘simple’ two-membrane (primary) plastid, the more ‘complex’ three- and four-membrane-bound transfer (associated with endosymbiosis) are key aspects (secondary and some tertiary) plastids, pigment-lacking of algal evolution that have decisive impacts on inference nonphotosynthetic plastids (e.g. apicoplasts), to the non- of their phylogenetic positions in the tree of life. permanent, ‘stolen’ plastids in a number of heterotrophic Deciphering plastid origin therefore provides general organisms (a phenomenon known as kleptoplasty). These insights into the evolution of eukaryote lineages. diverse forms differ with respect to how the plastid ori- ginated in the ‘host’ cell and in the case of kleptoplasts, their level of genetic integration and dependence on host cell metabolism. Unfortunately, the frequency of complex Introduction plastid transfers between related eukaryote groups such as ‘chromalveolates’ (e.g. diatoms, haptophytes, oomycetes One of the landmark evolutionary events in the history of and dinoflagellates) is difficult if not impossible to divine, life is the origin of oxygenic photosynthesis (photo- resulting in an incomplete understanding of this process. autotrophy), whereby organisms were able to harness light Given that endosymbiosis involves the wholesale transfer energy to produce biochemical energy that is utilised across of genetic material between lineages, plastid evolution is all metabolic processes. Perhaps more importantly, wide- one of the key complicating factors in understanding spread photosynthesis led to oxygenation of the atmos- eukaryote genome evolution. Therefore, deciphering the phere, laying the foundation for the evolution of diverse origin of plastids significantly enhances our understanding and abundant life forms that support extant ecosystems. of the basis of photosynthesis in plants, our primary food Cyanobacteria were the first dominant photosynthetic source on the planet, and its broader impact on eukaryote evolution. eLS subject area: Evolution & Diversity of Life How to cite: Chan, Cheong Xin; and Bhattacharya, Debashish (November 2011) Primary Plastids and Endosymbiosis Plastid Origin and Evolution. In: eLS. John Wiley & Sons, Ltd: Chichester. The simplest forms of plastids, the primary plastids, are DOI: 10.1002/9780470015902.a0023639 found exclusively (except for Paulinella, see below) within eLS & 2011, John Wiley & Sons, Ltd. www.els.net 1 Plastid Origin and Evolution the eukaryote supergroup Plantae (or Archaeplastida) a permanent endosymbiont and ultimately a functional (Rodrı´guez-Ezpeleta et al., 2005) that comprises the glau- organelle that has been vertically transmitted to sub- cophyte algae (Glaucophyta), red algae (Rhodophyta), sequent generations for over a billion years (Figure 1). as well as green algae and plants (collectively known See also: Endosymbionts; Glaucocystophytes; Green as Viridiplantae). The Plantae plastid, bound by two Algae; Plant Biodiversity; Red Algae membranes, originated from a cyanobacterium that was The idea of endosymbiosis was based on the observation engulfed and retained by a free-living, unicellular hetero- of the symbiotic relationship between fungi and algae in trophic protist, in a process termed primary endosymbiosis lichens, made by the Russian biologist, Konstantin Mer- (Margulis, 1970; Kutschera and Niklas, 2005). Rather than eschkowsky (Mereschkowsky, 1905). He championed the being digested, the captured cell in the food vacuole became idea that complex cells are derived from the symbiotic Heterotrophic protist Primary endosymbiosis Cyanobacterium Endosymbiont Paulinella Plantae Plants Green algae Red algae Glaucophyte algae Heterotrophic Heterotrophic protist protist Secondary endosymbiosis Red alga Peridinin dinoflagellates Ancestral dinoflagellate Haptophyte Loss Tertiary endosymbiosis Fucoxanthin dinoflagellates (b) (a) (c) “CHROMALVEOLATA” (SAR + Hacrobia) Figure 1 Current understanding of plastid origins in eukaryotes. Primary cyanobacterial endosymbiosis is thought to have given rise to the plastid shared by all Plantae lineages. An independent primary endosymbiosis gave rise to the plastid in the photosynthetic species of Paulinella (Rhizaria). Subsequent events of endosymbiosis, involving a red algal cell are implicated in the origin of plastids in chromalveolates (lineages that bear the complex chlorophyll a+c plastids). Three proposed evolutionary histories of chromalveolate plastid origin based on current literature are shown: (a) a single secondary red algal endosymbiosis that gave rise to the plastid in most chromalveolate lineages, according to the chromalveolate hypothesis; (b) secondary red algal endosymbiosis giving rise to the plastid in peridinin-type dinoflagellates, with a tertiary haptophyte endosymbiosis giving rise to the plastid in fucoxanthin- type dinoflagellates; (c) secondary red algal endosymbiosis that was potentially preceded by a cryptic green algal endosymbiosis, giving rise to the ancestral chromalveolate plastid but a genome with hundreds of genes of both green and red algal origin. 2 eLS & 2011, John Wiley & Sons, Ltd. www.els.net Plastid Origin and Evolution relationship between more simple forms (i.e. symbiogen- The Paulinella plastid traces its origin to Prochlorococcus esis). The term ‘endosymbiosis’ (Greek origin: endo ‘with- or Synechococcus type cells (Yoon et al., 2006). Also known in’; syn ‘with’; biosis ‘living’) refers to the phenomenon of as cyanelles or chromatophores, these plastids lie free in the an organism living within another, and was extended by cytoplasm, unbounded by a vacuolar membrane (i.e. Ivan Wallin (an American biologist) to explain the origin of characteristics of an organelle), but retain cyanobacterial mitochondria in eukaryotes. In the 1960s, Lynn Margulis features such as peptidoglycan and carboxysomes (John- established the endosymbiotic hypothesis as an explan- son et al., 1988). Interestingly, the closely related, phago- ation for the origin of both mitochondria and plastids in trophic sister lineage, Paulinella ovalis, although lacking a eukaryotes based on evidence from palaeontological, bio- plastid, is an active predator of cyanobacteria that are chemical and cytological sources (Margulis, 1970). commonly localised within food vacuoles (Johnson et al., Whereas her idea was first treated with much scepticism, 1988). A recent analysis of individual P. ovalis cells cap- nowadays endosymbiosis is a widely accepted explanation tured in the wild using single-cell genomics reveals the for the provenance of organelles. presence of genes derived from Prochlorococcus and The hypothesis that algal plastids originated from Synechocococcus lineages in the nuclear genome of P. ovalis cyanobacteria (via endosymbiosis) has been rigorously cells; that is, these cyanobacteria were likely to have been tested in the past two decades, in parallel with the avail- ingested as food and are the source of the transferred ability of molecular data, and the rapid advancement of nuclear genes. These results provide an intriguing and techniques in molecular and computational biology. The apparently direct link between the cyanobacterial diet of cyanobacterial derivation of genes encoded in primary the phagotrophic lineage and the primary plastid in the plastid genomes and clear evidence of
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