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The endosymbiotic origin diversification and fate of plastids

The endosymbiotic origin diversification and fate of

Phil. Trans. R. Soc. B (2010) 365, 729–748 doi:10.1098/rstb.2009.0103 Review The endosymbiotic origin, diversification and fate of plastids Patrick J. Keeling* Botany Department, Canadian Institute for Advanced Research, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, Canada V6T 1Z4 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. Keywords: plastids; endosymbiosis; evolution; algae; protist; phylogeny 1. THE ORIGIN OF PLASTIDS: A SINGLE EVENT OF GLOBAL SIGNIFICANCE Endosymbiosis has played many roles in the evolution of life, but the two most profound effects of this process were undoubtedly the origins of mitochondria and plastids in eukaryotic cells. There are many parallels in how these organelles originated and how their subsequent evolution played out, for example, the reduction of the bacterial symbiont genome and the development of a protein-targeting system (Whatley et al. 1979; Douglas 1998; Gray 1999; Gray et al. 1999; Gould et al. 2008). There are also many differences, however, and one of the more striking is the ultimate fate of the organelle once established: where mitochondria were integrated into the host and the two were seemingly never again separated (Williams & Keeling 2003; van der Giezen et al. 2005), plastid evolution has seen many more twists, turns and dead ends (for other reviews that cover various aspects of this history, see Delwiche 1999; McFadden 1999, *pkeeling@interchange.ubc.ca One contribution of 12 to a Theme Issue ‘Evolution of organellar metabolism in unicellular eukaryotes’. 2001; Archibald & Keeling 2002; Stoebe & Maier 2002; Palmer 2003; Williams & Keeling 2003; Keeling 2004; Archibald 2005; Keeling in press). Ultimately, mitochondria and plastids (with the small but interesting exception detailed in §2) have each been well established to have evolved from a single endosymbiotic event involving an alphaproteobacterium and cyanobacterium, respectively (Gray 1999). This conclusion has not come without considerable debate, which has stemmed from several sources. First, the ancient nature of the event makes reconstructing its history difficult because a great deal of change has taken place since the origin of this system, and all of this change masks ancient history. In addition, however, the complexity of subsequent plastid evolution has made for special and less expected problems. Specifically, plastids were originally established in a subset of eukaryotes by a so-called ‘primary’ endosymbiosis with an ancient cyanobacterial lineage. Once established, primary plastids then spread from that lineage to other eukaryotes by additional rounds of endosymbiosis between two eukaryotes (secondary and tertiary endosymbioses, which are each discussed in detail within their own section below). This led to a very confusing 729 This journal is q 2010 The Royal Society

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