Trends in Genetics
Volume 18, Issue 11, 1 November 2002, Pages 577-584
Journal home page for Trends in Genetics

Review
Recycled plastids: a ‘green movement’ in eukaryotic evolution

https://doi.org/10.1016/S0168-9525(02)02777-4Get rights and content

Abstract

Secondary endosymbiosis is the process that drives the spread of plastids (chloroplasts) from one eukaryote to another. The number of times that this has occurred and the kinds of cells involved are now becoming clear. Reconstructions of plastid history using molecular data suggest that secondary endosymbiosis is very rare and that perhaps as few as three endosymbioses have resulted in a large proportion of algal diversity. The significance of these events extends beyond photosynthesis, however, because non-photosynthetic organisms such as ciliates appear to have evolved from photosynthetic ancestors and could still harbor plastid-derived genes or relict plastids.

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.

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