Trends in Genetics
ReviewRecycled plastids: a ‘green movement’ in eukaryotic evolution
Section snippets
Second-hand plastids
Early work on photosynthetic eukaryotes led to the identification of two fundamentally different types of plastid. Primary (or simple) plastids are surrounded by two membranes and are found in red algae, green algae, land plants and glaucocystophytes (Box 2). Primary plastids descend vertically from the original endosymbiosis with a cyanobacterium, and their membranes correspond to the inner and outer membranes of its Gram-negative envelope (Fig. 1a,b). The plastids of glaucocystophytes have
How many secondary endosymbioses?
With the realization that secondary-plastid-containing algae constitute a large proportion of the diversity of photosynthetic eukaryotes comes an important question: how often have these mergers happened? The integration of endosymbiont and host is an immensely complex series of events that has a formidable effect on both host and endosymbiont. It involves massive transfers of DNA between genomes, the development of a sophisticated protein-targeting machinery and a substantial reorganization of
Cryptomonads: the fly in the ointment or the key to the puzzle?
Although available data suggest a single origin of chromalveolate plastids, the cryptomonads are the weakest link in the chain of evidence. Cryptomonads are least often seen to group with other chromalveolates in molecular trees (e.g. Refs 37., 41.). Furthermore, the proposed endosymbiotic replacement of the cryptomonad enolase gene has not affected alveolates [20]. This could be an indication that this enolase came from some other red alga or that cryptomonads actually acquired their secondary
Plastid reduction and loss: an emerging theme
One reason why it has been difficult to determine the evolution of plastids is that we do not understand the process of plastid loss, making it impossible to evaluate different hypotheses of plastid origins. An auxiliary issue is the difficulty of actually proving that a plastid has been lost, as opposed to the loss of photosynthesis. Loss of photosynthesis has been documented in many lineages and, in nearly all cases in which it has been carefully examined, the plastid has been retained.
Future directions
Unambiguously determining the evolutionary history of plastids and their host lineages will require additional corroborating evidence. However, it will certainly be a milestone that not only has a profound effect on our understanding of the major events in eukaryotic evolution but also yields considerable predictive power. An early, common origin of all chromalveolate plastids hints at the possible presence of molecular relicts of plastids, or perhaps even intact organelles, in organisms such
Acknowledgements
We thank B. Leander and N. Fast for helpful discussion, and the Keeling laboratory for critical comments on the manuscript. Our work was supported by a grant from the Canadian Institutes of Health Research (CIHR) to P.J.K. J.M.A. is supported by postdoctoral fellowships from CIHR and the Killam Foundation (University of British Columbia). P.J.K. is a scholar of the Canadian Institute for Advanced Research and the Michael Smith Foundation for Health Research.
References (58)
The chloroplasts of Euglena may have evolved from symbiotic green algae
Can. J. Bot.
(1978)- et al.
Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids
Am. J. Bot.
(2000) Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphidae and the Chlorarachniophyta
J. Eukaryot. Microbiol.
(1995)Molecular chaperones encoded by a reduced nucleus – the cryptomonad nucleomorph
J. Mol. Evol.
(2001)Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids
Mol. Biol. Evol.
(2001)Goniomonas: rRNA sequences indicate that this phagotrophic flagellate is a close relative of the host component of cryptomonads
Eur. J. Phycol.
(1994)Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements
J. Mol. Evol.
(2001)Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae
Plant Cell
(1999)- et al.
The origin of plastids and their spread via secondary endosymbiosis
- et al.
The plastid genome from the cryptomonad alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae
J. Mol. Evol.
(1999)
The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes
Proc. Natl. Acad. Sci. U. S. A.
A kingdom-level phylogeny of eukaryotes based on combined protein data
Science
The origin of red algae and the evolution of chloroplasts
Nature
Plastids and protein targeting
J. Eukaryot. Microbiol.
The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance
Int. Rev. Cytol.
Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree
J. Eukaryot. Microbiol.
Endomembrane structure and the protein targeting pathway in Heterosigma akashiwo (Raphidophyceae, Chromista)
J. Phycol.
The presequence of Euglena LHCPII, a cytoplasmically synthesized chloroplast protein, contains a functional endoplasmic reticulum-targeting domain
Proc. Natl. Acad. Sci. U. S. A.
The origins of plastids
Biol. J. Linn. Soc. London
Myzocytosis’, a kind of endocytosis with implications to compartmentalization in endosymbiosis
Naturwissenschaften
Chloroplasts and cell compartments in Cryptophyceae
Br. Phycol. J.
Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta divisio nova, Chlorarachniophyceae classis nova)
J. Phycol.
Size isn't everything: lessons in genetic miniaturisation from nucleomorphs
Curr. Opin. Genet. Dev.
The highly reduced genome of an enslaved algal nucleus
Nature
The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis
Curr. Genet.
Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase
Proc. Natl. Acad. Sci. U. S. A.
Tracing the thread of plastid diversity through the tapestry of life
Am. Nat.
Complete sequence of Euglena gracilis chloroplast DNA
Nucleic Acids Res.
Molecular phylogeny of chlorarachniophytes based on plastid rRNA and rbcL sequences
Arch. Protistenkd.
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