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Evolutionary history of plastids.

A major biological event contributing to the biodiversity of present-day organisms was the enslavement of a photosynthetic eubacterium by a primitive eukaryote and its entrapment as an integral part of the cell: the plastid. Since the first acquisition by eukaryotes of photosynthetic capability by primary endosymbiosis, two major lineages (red and green) appear to have arisen. Subsequently, an amazing variety of secondary endosymbioses took place, resulting in a complex assemblage of organisms containing photosynthetic organelles surrounded by multiple membranes. This assemblage includes the extant cryptomonads, chlorarachniophytes, chromophytes, haptophytes, euglenoids, and dinoflagellates. Superimposed upon this scenario were the activities of eukaryotes that were acquiring plastids by tertiary endosymbiosis from the green algal, cryptomonad, chromophyte, and haptophyte lineages (1), and others that were apparently losing the capacity to photosynthesize, while retaining vestigial plastids (e.g., the extant apicomplexans, parasitic plants, colorless cryptomonads, and euglenoids).

Attempts to delineate the events leading to the multicolored array of extant photosynthetic eukaryotes started over one hundred years ago and were initially based on microscopic investigations (2). More recently, biochemical, molecular, and phylogenetic techniques have been employed to dissect the evolutionary history of plastids and their hosts. With the accumulation of molecular data, including the complete plastid sequences from several representative lineages (3) and sequences from nuclear (or nucleus-derived) compartments (4), a clearer picture of some of the events leading to extant photosynthetic eukaryotes is emerging.

The cryptomonad alga Guillardia theta provides a good model organism for tracing the ancestry of plastid-bearing eukaryotes. It is an example of a cell-within-a-cell, being composed of a flagellate host cell, complete with mitochondria and nucleus, surrounding a plastid lying within a reduced cytoplasmic compartment that contains a vestigial nucleus (or nucleomorph). Molecular data from the plastid, nucleomorph, and nucleus (5) are giving clues to the nature of the partners that make up this organism, as well as fascinating insights into the genome reduction that occurred during endosymbiosis.

Plastid genome

The plastid genome of Guillardia theta (121,524 bp) has been completely sequenced and bears striking resemblance to the 191,028 bp plastid genome of the rhodophyte Porphyra purpurea (6). Although much smaller, the cryptomonad plastid genome contains extensive synteny groups that are clearly recognizable and provide excellent evidence for the red algal ancestry of the cryptomonad plastid [ILLUSTRATION FOR FIGURE 1 OMITTED]. Furthermore, a comparison of the Guillardia plastid genome with the 35 kb plastid-like genome of the apicomplexan Plasmodium falciparum shows an almost identical gene order, with only a fraction of the cryptomonad genes present in the apicomplexan. This indicates that the reduced 35 kb circle perhaps had its origins as a cryptomonad plastid genome, which is not unlikely given the propensity for other members of this group (dinoflagellates) to take up cryptomonads as endosymbionts.

The cryptomonad genome contains a short (4.9 kb) inverted repeat containing the rRNA cistrons, 30 tRNA genes, 44 genes encoding proteins for photosynthesis, 44 ribosomal protein genes (26 large subunit and 18 small subunit), 5 genes for biosynthetic function, 19 genes involved in gene expression (including 3 hypothetical chloroplast reading frames or ycfs), 25 additional ycfs, and 9 open reading frames (ORFs) larger than 50 amino acids. Intergenic spacers are very short, no introns have been detected, and several genes overlap, all resulting in a very compact genome. In addition, large clusters of genes (such as the ribosomal protein genes) are organized into single transcriptional units, again resulting in an economically organized genome (7).

Comparisons of plastid gene order and gene sequences support a monophyletic, primary origin of plastids and a subsequent divergence into red and green lineages. Particularly significant are gene clusters that are present in plastid genomes from several lineages, but absent in cyanobacteria (such as the atpA/rpo cluster and the psbBTNH cluster). These clusters most probably evolved post-endosymbiosis, or (less likely) were the product of extreme convergent evolution. Additional evidence for monophyly comes from phylogenetic trees constructed from several genes (such as SSU rRNA, atpB, and tufA).

Nucleomorph genome

One of the first steps in the evolution of a plastid from an endosymbiotic cyanobacteria was the massive loss of redundant genes and/or transfer to the host nucleus of the approximately 900 genes essential for photosynthesis. Since the nucleomorph genome of cryptomonads represents the vestigial nucleus of the host, it was suspected to contain these transferred genes. At an average of 1 kb/gene, this would require a genome of at least 900 kb to encode just the genes for photosynthesis. However, with such a small haploid genome size (520 kb), this scenario seemed less likely. Furthermore, hybridization analysis has shown that all three chromosomes contain repeats of the rRNA cistron (consisting of 18S-5.8S-28S-5S rRNA genes) and several downstream ORFs, each of which occupy about 12 kb. Most of the genes identified in the genome sequencing project are concerned with self-replication and gene expression, rather than with plastid biochemistry. Thus far, ftsZ (which is involved in cell division and may interact with the plastid-encoded ftsH) and a subunit of clpC are probable candidates for plastid-targeted proteins. With the acquisition of more gene sequences from the nucleomorph, it will be possible to determine more precisely the exact role of the nucleomorph in this complex cell.

Phylogenetic analyses performed with nucleomorph genes are thus far confined to the SSU rRNA and hsp70 gene. SSU rRNA phylogenies ally the nucleomorph with red algae (8), and the limited hsp70 data set places cryptomonads between green plants and trypanosomes with a weak bootstrap value (9). Additional evidence for a close relationship between the cryptomonad plastid and red algae is the paucity of introns in the genomes of both organisms.

Nuclear genome

Since the nucleomorph does not seem to encode an abundance of components that function in plastid biochemistry, the nucleus probably does. Although several nuclear genes have been identified and partially sequenced, the only identified gene presumed to code for a plastid component is cpeA, the alpha subunit of phycoerythrin. Analysis of nuclear genes encoding plastid proteins will help to clarify whether these genes were transferred from the nucleomorph during endosymbiosis or originated from a primary endosymbiont present in a photosynthetic host cell that was subsequently lost after acquisition of a eukaryotic endosymbiont, as hypothesized by Hauber et al. (10).

This is NRC publication number NRCC 42291.

Literature Cited

1. Schnepf, E. 1993. From prey via endosymbiont to plastid: comparative studies in dinoflagellates. Pp. 53-72 in Origins of Plastids, R. A. Lewin, ed. Chapman & Hall, New York.

2. Schimper, A. F. W. 1883. Uber die Entwicklung der Chlorophyllkorner und Farbkorner (1 Teil). Bot. Zeit. 41:105-114.

3. Reith, M. E. 1995. Molecular biology of rhodophyte and chromophyte plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 459575.

4. Palmer, J. D., and C. F. Delwiche. 1996. Second-hand chloroplasts and the case of the disappearing nucleus. Proc. Nat. Acad. Sci. USA 93: 7432-7435.

5. McFadden, G.I., P. R. Gilson, S. E. Douglas, T. Cavalier-Smith, C. J. B. Hofmann, and U.-G. Maier. 1997. Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet. 13: 46-49.

6. Reith, M. E., and J. Munholland. 1995. Complete nucleotide sequence of Porphyra purpurea chloroplast genome. Plant Mol. Biol. Rep. 13: 333-335.

7. Wang, S.-L., X.-Q Liu, and S. E. Douglas. 1997. The large ribosomal protein gene cluster of a cryptomonad plastid: gene organization, sequence and evolutionary implications. Biochem. Mol. Biol. Int. 41: 1035-1044.

8. Douglas, S. E., C. A. Murphy, D. F. Spencer, and M. W. Gray. 1991. Cryptomonad algae are evolutionary chimaera of two phylogenetically distinct unicellular eukaryotes. Nature 350:148-151.

9. Rensing, S. A., and U.-G. Maier. 1994. Phylogenetic analysis of the stress-70 protein family. J. Mol. Evol. 39: 80-86.

10. Hauber, M. M., S. B. Muller, V. Speth, and U.-G. Maier. 1994. How to evolve a complex plastid? - A hypothesis. Bot. Acta 107: 383-386.

Discussion

MARGULIS: Are there any nucleosomes in the nucleomorph? Can you tell us about the nucleomorph genes in general with regard to their organization of DNA and histones? What do you mean by chromosomes?

DOUGLAS: We haven't looked at these organisms under the electron microscope. In the plastids there is a histone-like protein that has been identified. We haven't found any histone.

CAVALIER-SMITH: Why do you postulate two separate uptakes of red algae into chromophytes and cryptomonads rather than a single uptake into the ancestor of all three chromist groups?

DOUGLAS: The reason is that the host cells appear to be fairly different both in trees and ultrastructure.

ROTHSCHILD: In your presentation, did you intend to have the origin of the Cryptos coming out before the rest of the Chromista?

DOUGLAS: There was no timing involved there.

ROTHSCHILD: Would you like to hazard a guess on when that symbiosis arose? How long does it take to get through the nucleomorphisms?

DOUGLAS: One possible explanation of why the nucleomorph is there and why it's been lost in some lineages is that the secondary host also harbored an endosymbiont. Genes could have been transferred to lesser or greater degrees from that endosymbiont to that host. If all the genes that were sufficient for running a plastid were transferred, in the secondary endosymbiosis, the nucleomorph could have been lost. If an insufficient number of genes had been transferred to that nucleus of the second host, then it would still need to retain a nucleomorph.
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Title Annotation:includes discussion; Evolution: A Molecular Point of View
Author:Douglas, Susan E.
Publication:The Biological Bulletin
Date:Jun 1, 1999
Words:1554
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