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Rate Variation as a Function of Gene Origin in Plastid-Derived Genes of Peridinin-Containing Dinoflagellates

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Abstract

Peridinin-pigmented dinoflagellates contain secondary plastids that seem to have undergone more nearly complete plastid genome reduction than other eukaryotes. Many typically plastid-encoded genes appear to have been transferred to the nucleus, with a few remaining genes found on minicircles. To understand better the evolution of the dinoflagellate plastid, four categories of plastid-associated genes in dinoflagellates were defined based on their history of transfer and evaluated for rate of sequence evolution, including minicircle genes (presumably plastid-encoded), genes probably transferred from the plastid to the nucleus (plastid-transferred), and genes that were likely acquired directly from the nucleus of the previous plastid host (nuclear-transferred). The fourth category, lateral-transferred genes, are plastid-associated genes that do not appear to have a cyanobacterial origin. The evolutionary rates of these gene categories were compared using relative rate tests and likelihood ratio tests. For comparison with other secondary plastid-containing organisms, rates were calculated for the homologous sequences from the haptophyte Emiliania huxleyi. The evolutionary rate of minicircle and plastid-transferred genes in the dinoflagellate was strikingly higher than that of nuclear-transferred and lateral-transferred genes and, also, substantially higher than that of all plastid-associated genes in the haptophyte. Plastid-transferred genes in the dinoflagellate had an accelerated rate of evolution that was variable but, in most cases, not as extreme as the minicircle genes. Furthermore, the nuclear-transferred and lateral-transferred genes showed rates of evolution that are similar to those of other taxa. Thus, nucleus-to-nucleus transferred genes have a more typical rate of sequence evolution, while those whose history was wholly or partially within the dinoflagellate plastid genome have a markedly accelerated rate of evolution.

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Acknowledgments

This work was supported in part by NSF Grant MCB-9984284. We are grateful to E. Gantt, E. Herman, and C. Mitter for helpful suggestions, G. Concepcion and C. Rogers as well as other members of the Delwiche lab for technical support, and the Alfred P. Sloan Foundation for providing seed resources. We also thank anonymous reviewers for useful suggestions.

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  1. Tsvetan R. Bachvaroff

    Present address: Center of Marine Biotechnology, 701 East Pratt Street, Baltimore, MD, 21202, USA

Authors and Affiliations

  1. Department of Cell Biology and Molecular Genetics, University of Maryland College Park, H. J. Patterson Hall, College Park, MD, 20742, USA

    Tsvetan R. Bachvaroff, M. Virginia Sanchez-Puerta & Charles F. Delwiche

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  1. Tsvetan R. Bachvaroff
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  2. M. Virginia Sanchez-Puerta
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  3. Charles F. Delwiche
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Correspondence to Charles F. Delwiche.

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[Reviewing Editor: Dr. Debashish Battacharya]

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Bachvaroff, T.R., Sanchez-Puerta, M.V. & Delwiche, C.F. Rate Variation as a Function of Gene Origin in Plastid-Derived Genes of Peridinin-Containing Dinoflagellates. J Mol Evol 62, 42–52 (2006). https://doi.org/10.1007/s00239-004-0365-4

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