ANRV342-PP59-20 ARI 16 January 2008 15:8 V I E E W R S I E N C N A D V A Plastid Evolution Sven B. Gould, Ross F. Waller, and Geoffrey I. McFadden School of Botany, University of Melbourne, Parkville VIC-3010, Australia; email: [email protected], [email protected], [email protected] Annu. Rev. Plant Biol. 2008. 59:491–517 Key Words The Annual Review of Plant Biology is online at secondary/tertiary endosymbiosis, complex plastids, protein plant.annualreviews.org targeting, genome evolution, intracellular gene transfer, plastid This article’s doi: biochemistry 10.1146/annurev.arplant.59.032607.092915 Copyright c 2008 by Annual Reviews. Abstract ! All rights reserved The ancestors of modern cyanobacteria invented O2-generating 1543-5008/08/0602-0491$20.00 photosynthesis some 3.6 billion years ago. The conversion of wa- ter and CO2 into energy-rich sugars and O2 slowly transformed the planet, eventually creating the biosphere as we know it today. Eukaryotes didn’t invent photosynthesis; they co-opted it from prokaryotes by engulfing and stably integrating a photoautotrophic prokaryote in a process known as primary endosymbiosis. After ap- proximately a billion of years of coevolution, the eukaryotic host and its endosymbiont have achieved an extraordinary level of inte- gration and have spawned a bewildering array of primary producers that now underpin life on land and in the water. No partnership has been more important to life on earth. Secondary endosymbioses have created additional autotrophic eukaryotic lineages that include key organisms in the marine environment. Some of these organisms have subsequently reverted to heterotrophic lifestyles, becoming signifi- cant pathogens, microscopic predators, and consumers. We review the origins, integration, and functions of the different plastid types with special emphasis on their biochemical abilities, transfer of genes to the host, and the back supply of proteins to the endosymbiont. 491 ANRV342-PP59-20 ARI 16 January 2008 15:8 These geological indices testify to an ever- Contents increasing concentration of atmospheric oxy- gen due to photosynthetic activity. Photosyn- INTRODUCTION. 492 thesis was also the evolutionary trigger for the FROM FREEDOM TO SLAVERY: sweeping diversification of O -dependent life. OUTLINING 2 Indeed, oxygen has become critical for most ENDOSYMBIOTIC STEPS . 492 living things, acting as an acceptor for the Primary Endosymbiosis . 493 electrons released from carbon-carbon bonds Eukaryotic Endosymbiosis . 495 that were ultimately created using energy cap- Nature’s Playground: tured by photosynthesis. Thus, a byproduct of The Evolution Continues . 498 photosynthesis (oxygen) became an essential PREPROTEIN TARGETING . 501 component for the burning of the sugars pro- Targeting to Primary Plastids . 501 duced by photosynthesis. The balance of the Targeting Into and Within biosphere was born. Secondary Plastids. 503 Nineteenth century microscopists (Sachs, BIOCHEMICAL PATHWAYS . 505 Altmann, and Schimper) recognized the semi- Starch Synthesis . 505 autonomous nature and bacterial-like staining Isopentenyl Diphosphate properties of chloroplasts (then known as (Isoprenoid Precursor) chlorophyll bodies) and mitochondria (then Synthesis. 506 known as cell granules) (4, 106), but it took Heme Synthesis . 507 another 15 years before Mereschkowsky syn- Aromatic Amino Acid Synthesis . 508 thesized these observations into the theory Fe-S Clusters . 508 that chloroplasts are derived from cyanobac- teria (81, 109). Margulis later formalized the Theory of Endosymbiosis, which posits that INTRODUCTION plastids and mitochondria of eukaryotic cells In nature the counterpart of chaos is not cos- derive from bacterial endosymbionts (71). mos, but evolution. The spark of life was ini- tially a chemical one, leading to the synthesis of the first molecules. Some of these persisted FROM FREEDOM TO SLAVERY: and evolved in a precellular period, perhaps OUTLINING ENDOSYMBIOTIC similar to that described in the model of the STEPS RNA world, leading to the first prokaryotic As far as we know, all eukaryotes have mi- life approximately 3.5 to 4 billion years ago tochondria (or modified, anaerobic forms of (48, 74). The invention of oxygenic photosyn- mitochondria known as hydrogenosomes or thesis by prokaryotic cyanobacteria approxi- mitosomes), and the establishment of this mately 500 million years later was the next partnership is generally regarded as inte- major achievement of biological evolution. It gral to the origin of eukaryotes (123). The had a major impact on the earth by enriching acquisition of plastids by eukaryotes oc- the atmosphere with O2 to a level that trans- curred later, after the establishment of a di- formed the geochemistry of the planet. versity of heterotrophic eukaryotic lineages, The first molecular carbon skeletons typ- one of which adopted a cyanobacterium- ical of cyanobacteria can be identified in like endosymbiont to acquire photosynthe- strata from approximately 2.75 billion years sis and become autotrophic. We refer to an ago (15). At the same time a novel mineral initial plastid-creating endosymbiosis as the known as hematite (Fe2O3), which can form primary endosymbiosis. Secondary (or eu- only in the presence of a minimum critical karyotic) endosymbiosis refers to subsequent concentration of oxygen, began to appear. endosymbiotic events in which the progeny 492 Gould Waller McFadden · · ANRV342-PP59-20 ARI 16 January 2008 15:8 of the primary endosymbiotic partnership diverged from their green algal ancestors become endosymbionts within other het- approximately 400 to 475 mya (36), subse- erotrophic eukaryotes, thus transferring the quently conquered the terrestrial environ- captured cyanobacterial symbiont laterally ment, paving the way for animals to follow among eukaryotes. Subsequently, the progeny them onto land. In accordance with this se- of these secondary endosymbiotic partner- quence, plastids in the glaucophytes (which ships have become endosymbionts in other are sometimes referred to as cyanelles but are eukaryotes, creating tertiary endosymbioses, definitely plastids) most resemble their to weave an extraordinarily complex set of cyanobacterial ancestors in that they re- endosymbiotic relationships of cells within tain a peptidoglycan, wall-like layer between cells within cells within cells (Figure 1). In the inner and outer envelope membranes this review we examine the cell biology of (57). Additionally, the thylakoids inside the these endosymbiotic events and examine how glaucophyte plastid stroma are studded with the various compartments and genomes of phycobilisomes that are identical to those these extraordinary chimeras cooperate as a of cyanobacteria, and the composition of single cell, albeit one made up of parts from the oxygen-evolving enhancer complex is multiple individual cells. also very similar to that of free-living cyanobacteria (117). Rhodophyte plastids also use phycobilins in protein-based light har- Primary Endosymbiosis vesting antenna (phycobilisomes), but their The endosymbiotic integration of a free- plastids have apparently lost the peptido- living, cyanobacterial-like prokaryote into a glycan wall (31). The green algal/plant eukaryotic host produced three major au- lineage plastids are the most derived in the pri- totrophic lineages: the glaucophytes, the mary endosymbiosis lineage. Phycobilisomes green algae (and their descendants, the were replaced by chlorophyll b embedded plants), and the red algae (2, 46) (Figure 1). in thylakoid membranes, and a rich panoply Plastids in these primary endosymbionts are of accessory pigments developed to capture characterized by having two bounding mem- light and protect the photosynthetic appara- branes, which are derived from the two mem- tus from the unfiltered terrestrial light (80). branes (plasma membrane and outer mem- Generally, primary plastids have under- brane) of the Gram-negative cyanobacterium gone major modification during their tenure (17, 20). If a phagocytotic membrane sur- in the eukaryotic host; reduction of their rounded the symbiont when it was first inter- genome’s coding capacity is one of the more nalized by the host, it has disappeared with- conspicuous attenuations. The genome of out a trace (20). The main lines of evidence the cyanobacterium Anabaena sp. PCC 7120 supporting homology between the outer en- has 5366 protein-encoding genes, and other velope membrane and the outer membrane cyanobacteria possess similar numbers of of a cyanobacterium are (a) the presence of genes (53). In contrast, the most gene-rich galactolipids (52), (b) the presence of β-barrel plastid reported to date, that of the red alga proteins in both membranes (110), and (c) the Porphyra purpurea, encodes a paltry 251 genes occurrence of peptidoglycan (or rudiments of (99), and the plastids of the parasitic plant peptidoglycan synthesis machinery) beneath Epifagus virginiana harbor a mere 42 genes these membranes (117). (132). Thus, most of the original genetic ma- Phylogenetic analyses suggest that the terial of the endosymbiont was clearly ei- glaucophytes were the first primary endosym- ther lost or transferred to the host genome biotic lineage to diverge, some 550 mya, during their coevolution. Selection likely fa- and that the red and green algae diverged vored the initial loss of genetic material later (75, 82, 103). Plants, which probably by the endosymbiont because it turned the www.annualreviews.org Plastid Evolution 493 • ANRV342-PP59-20 ARI 16 January 2008 15:8 Rhopalodia