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Journal of Molecular Evolution

, Volume 62, Issue 2, pp 143–157 | Cite as

A “Green” Phosphoribulokinase in Complex Algae with Red Plastids: Evidence for a Single Secondary Endosymbiosis Leading to Haptophytes, Cryptophytes, Heterokonts, and Dinoflagellates

  • Jörn PetersenEmail author
  • René Teich
  • Henner Brinkmann
  • Rüdiger Cerff
Article

Abstract

Phosphoribulokinase (PRK) is an essential enzyme of photosynthetic eukaryotes which is active in the plastid-located Calvin cycle and regenerates the substrate for ribulose-bisphosphate carboxylase/oxygenase (Rubisco). Rhodophytes and chlorophytes (red and green algae) recruited their nuclear-encoded PRK from the cyanobacterial ancestor of plastids. The plastids of these organisms can be traced back to a single primary endosymbiosis, whereas, for example, haptophytes, dinoflagellates, and euglenophytes obtained their “complex” plastids through secondary endosymbioses, comprising the engulfment of a unicellular red or green alga by a eukaryotic host cell. We have cloned eight new PRK sequences from complex algae as well as a rhodophyte in order to investigate their evolutionary origin. All available PRK sequences were used for phylogenetic analyses and the significance of alternative topologies was estimated by the approximately unbiased test. Our analyses led to several astonishing findings. First, the close relationship of PRK genes of haptophytes, heterokontophytes, cryptophytes, and dinophytes (complex red lineage) supports a monophyletic origin of their sequences and hence their plastids. Second, based on PRK genes the complex red lineage forms a highly supported assemblage together with chlorophytes and land plants, to the exclusion of the rhodophytes. This green affinity is in striking contrast to the expected red algal origin and our analyses suggest that the PRK gene was acquired once via lateral transfer from a green alga. Third, surprisingly the complex green lineages leading to Bigelowiella and Euglena probably also obtained their PRK genes via lateral gene transfers from a red alga and a complex alga with red plastids, respectively.

Keywords

Secondary endosymbiosis Gene transfer Plastid Nuclear genes Calvin cycle Phosphoribulokinase Complex algae Red algae 

Notes

Acknowledgments

We thank Woodland Hastings (Harvard) for the cDNA libraries from Pyrocystis lunula and Lingulodinium polyedrum, William Martin (Düsseldorf) for the cDNA library from Euglena gracilis, Geoff McFadden (Melbourne) for provision of genomic DNA from Bigelowiella natans, Sarina Scharbatke (Hannover) for excellent technical assistance, and Carina Grau-vogel for critical discussions. We are grateful to Naiara Rodriguez-Ezpeleta for helpful comments on an earlier version of the manuscript. The associate editor and four anonymous reviewers provided very helpful suggestions. Major financial support, including a Ph.D. stipend for R.T., was received from the Deutsche Forschungsgemeinschaft (CE 1/27-1).

Supplementary material

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Supplementary material

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Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Jörn Petersen
    • 1
    Email author
  • René Teich
    • 1
  • Henner Brinkmann
    • 2
  • Rüdiger Cerff
    • 1
  1. 1.Institut für GenetikTechnische Universität BraunschweigGermany
  2. 2.Département de BiochimieUniversité de Montréal C.P. 6128MontréalCanada

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