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MBE Advance Access published online on May 12, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl011
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted May 4, 2006

Research Article

Heterotachy Processes in Rhodophyte-Derived Second-Hand Plastid Genes: Implications for Addressing the Origin and Evolution of Dinoflagellate Plastids

Kamran Shalchian-Tabrizi 1, Marianne Skånseng 1, Fredrik Ronquist 2, Dag Klaveness 3, Tsvetan R. Bachvaroff 4, Charles F. Delwiche 5, Andreas Botnen 6, Torstein Tengs 7, and Kjetill S. Jakobsen 1 *

1 Centre for Ecological and Evolutionary Synthesis, Dep. of Biology, University of Oslo, N-0316 Oslo, Norway
2 Evolutionary Biology Centre, Uppsala University, SE-752 36, Uppsala, Sweden; Present addresses: Florida State University, Dep. of Biological Science, Tallahassee, FL 32306, USA
3 Program for Plankton Biology, Dep. of Biology, University of Oslo, N-0316, Oslo, Norway
4 Cell Biology and Molecular Genetics, University of Maryland College Park, College Park, MD 20742 USA; Present addresses: Center of Marine Biotechnology, 701 E Pratt St. Baltimore Maryland 21202, USA
5 Cell Biology and Molecular Genetics, University of Maryland College Park, College Park, MD 20742 USA
6 USIT, University of Oslo, N-0316 Oslo, Norway
7 Centre for Ecological and Evolutionary Synthesis, Dep. of Biology, University of Oslo, N-0316 Oslo, Norway; Present addresses: National Veterinary Institute, Ullevålsveien 68, 0454 Oslo, P.O.Box 8156 Dep., N-0033 Oslo, Norway

* To whom correspondence should be addressed.
Kjetill S. Jakobsen, E-mail: k.s.jakobsen{at}bio.uio.no


  Abstract

Serial transfer of plastids from one eukaryotic host to another is the key process involved in creation of second-hand plastids. Such transfers drastically change the environment of the plastids and hence the selection regimes, presumably leading to changes over time in the characteristics of plastid gene evolution and to misleading phylogenetic inferences. About half of the dinoflagellate protists species are photosynthetic, and unique in harboring a diversity of plastids acquired from a wide range of eukaryotic algae. They are therefore ideal for studying evolutionary processes of plastids gained through secondary and tertiary endosymbiosis. In the light of these processes we have evaluated the origin of two types of dinoflagellate plastids, containing the peridinin or 19'-hexanoyloxyfucoxanthin (19'HNOF) pigments, by inferring the phylogeny using covarion evolutionary models allowing the pattern of among-site rate variation to change over time. Our investigations of genes from secondary and tertiary plastids derived from the rhodophyte plastid lineage clearly reveal heterotachy processes, characterized as stationary covarion substitution patterns and changes in proportion of variable sites across sequences. Failure to accommodate covarion-like substitution patterns can have strong effects on the plastid tree topology. Importantly, multi-gene analyses performed with probabilistic methods using among-site rate and covarion models of evolution conflict with proposed single origin of the peridinin and 19'HNOF containing plastids, suggesting that analysis of second-hand plastids can be hampered by convergence in the evolutionary signature of the plastid DNA sequences. Another type of sequence convergence was detected at protein level involving the psaA gene. Excluding the psaA sequence from a concatenated protein alignment, grouped the peridinin plastid with haptophytes, congruent with all DNA trees. Altogether, taking account of complex processes involved in the evolution of dinoflagellate plastid sequences (both at the DNA and amino acid level), we demonstrate the difficulty of excluding independent, tertiary origin for both the peridinin and 19'HNOF plastids involving engulfment of haptophyte-like algae. In addition, the refined topologies suggest the red algal order, Pophyridales, as the endosymbiont ancestor of the secondary plastids in cryptophytes, haptophytes, and heterokonts.

Keywords: Chromalveolates; chromists; covarion; dinoflagellates; heterotachy; plastid evolution.
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