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Single gene circles in dinoflagellate chloroplast genomes

Nature volume 400, pages 155–159 (1999)Cite this article

Abstract

Photosynthetic dinoflagellates are important aquatic primary producers and notorious causes of toxic ‘red tides’. Typical dinoflagellate chloroplasts differ from all other plastids in having a combination of three envelope membranes1 and peridinin-chlorophyll a /c light-harvesting pigments2. Despite evidence of a dinoflagellete satellite DNA containing chloroplast genes3, previous attempts to obtain chloroplast gene sequences have been uniformly unsuccessful. Here we show that the dinoflagellate chloroplast DNA genome structure is unique. Complete sequences of chloroplast ribosomal RNA genes and seven chloroplast protein genes from the dinoflagellate Heterocapsa triquetra reveal that each is located alone on a separate minicircular chromosome: ‘one gene–one circle’. The genes are the most divergent known from chloroplast genomes. Each circle has an unusual tripartite non-coding region (putative replicon origin), which is highly conserved among the nine circles through extensive gene conversion, but is very divergent between species. Several other dinoflagellate species have minicircular chloroplast genes, indicating that this type of genomic organization may have evolved in ancestral peridinean dinoflagellates. Phylogenetic analysis indicates that dinoflagellate chloroplasts are related to chromistan and red algal chloroplasts and supports their origin by secondary symbiogenesis4,5,6.

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Figure 1: Hybridization of dinoflagellate DNA with chloroplast gene probes.
Figure 2: Structure of psbA contig assembled from 17 sequences (circularized on the right).
Figure 3: Consensus sequence of the 9G-9A-9G region.
Figure 4: Alignment of the variable D2 region.
Figure 5: Hybridization of H.
Figure 6: Neighbour-joining tree of seven concatenated protein sequences.

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Acknowledgements

We thank M. Beaton and K. Ishida for valuable discussion and advice; E. Filek for help with plasmid sequencing; X. Wu and E. Chao for advice on PCR; R. G. Hiller for communicating unpublished data; and J. Saldarriaga for H. rotundata and G. grindleyi total DNA. This work was supported by NSERC research grants to B.R.G. and T.C.-S. T.C.-S. thanks the Canadian Institute for Advanced Research for fellowship support.

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  1. Department of Botany, Canadian Institute for Advanced Research Evolutionary Biology Programme, University of British Columbia, Vancouver, V6T 1Z4, British Columbia, Canada

    Zhaoduo Zhang, B. R. Green & T. Cavalier-Smith

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  1. Zhaoduo Zhang
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  3. T. Cavalier-Smith
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Correspondence to B. R. Green.

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Zhang, Z., Green, B. & Cavalier-Smith, T. Single gene circles in dinoflagellate chloroplast genomes. Nature 400, 155–159 (1999). https://doi.org/10.1038/22099

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