The origin of plastids

Abstract

It is generally accepted that plastids first arose by acquisition of photosynthetic prokaryotic endosymbionts by non-photosynthetic eukaryotic hosts. It is also accepted that photosynthetic eukaryotes were acquired on several occasions as endosymbionts by non-photosynthetic eukaryote hosts to form secondary plastids. In some lineages, secondary plastids were lost and new symbionts were acquired, to form tertiary plastids. Most recent work has been interpreted to indicate that primary plastids arose only once, referred to as a 'monophyletic' origin. We critically assess the evidence for this. We argue that the combination of Ockham's razor and poor taxon sampling will bias studies in favour of monophyly. We discuss possible concerns in phylogenetic reconstruction from sequence data. We argue that improved understanding of lineage-specific substitution processes is needed to assess the reliability of sequence-based trees. Improved understanding of the timing of the radiation of present-day cyanobacteria is also needed. We suggest that acquisition of plastids is better described as the result of a process rather than something occurring at a discrete time, and describe the 'shopping bag' model of plastid origin. We argue that dinoflagellates and other lineages provide evidence in support of this.

Figure 1

(a) A cyanobacterium breaking up the red/green lineage provides a refutation of monophyly. (b) The hypothesis preferred under Ockham's razor for explaining the origins of characters specific to red and green lineages, i.e. a single endosymbiosis, when no cyanobacteria have been sampled that (a) break up the red/green lineage. R and G indicate the origin of characters specific for the red and green lineages; the star indicates endosymbiosis.

Figure 2

Organization of the electron transfer chain of (a) cyanobacteria and (b) chloroplasts. The figure shows that chloroplasts lack a cytochrome oxidase complex and (at least for green chloroplasts) a cytochrome c₆. Figure courtesy of D. S. Bendall.

Figure 3

The plastid impact hypothesis. Two lineages (A and C) acquire a plastid by endosymbiosis of closely related organisms. The plastid gene subsequently replaces a nuclear counterpart in both lineages (P→N). Thus, phylogenetic trees based on that gene will group A and C to the exclusion of B.

Figure 4

The psbBTNH cluster. This was initially thought to be unique to plastids, indicating a monophyletic origin. However, a similar cluster was then found to exist in the cyanobacterium Gloeobacter.