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Cited by 442Protist diversity and phylogenyPhotosynthetic Processes and MechanismsChromosomal and Genetic Variations

A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis

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Yoon, Hwan Su, Hackett, Jeremiah D., Bhattacharya, Debashish·2002·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.172234799PMC PMC129336
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Abstract

The most widely distributed dinoflagellate plastid contains chlorophyll c 2 and peridinin as the major carotenoid. A second plastid type, found in taxa such as Karlodinium micrum and Karenia spp., contains chlorophylls c 1 + c 2 and 19′-hexanoyloxy-fucoxanthin and/or 19′-butanoyloxy-fucoxanthin but lacks peridinin. Because the presence of chlorophylls c 1 + c 2 and fucoxanthin is typical of haptophyte algae, the second plastid type is believed to have originated from a haptophyte tertiary endosymbiosis in an ancestral peridinin-containing dinoflagellate. This hypothesis has, however, never been thoroughly tested in plastid trees that contain genes from both peridinin- and fucoxanthin-containing dinoflagellates. To address this issue, we sequenced the plastid-encoded psa A (photosystem I P700 chlorophyll a apoprotein A1), psb A (photosystem II reaction center protein D1), and “Form I” rbc L (ribulose-1,5-bisphosphate carboxylase/oxygenase) genes from various red and dinoflagellate algae. The combined psa A + psb A tree shows significant support for the monophyly of peridinin- and fucoxanthin-containing dinoflagellates as sister to the haptophytes. The monophyly with haptophytes is robustly recovered in the psb A phylogeny in which we increased the sampling of dinoflagellates to 14 species. As expected from previous analyses, the fucoxanthin-containing dinoflagellates formed a well-supported sister group with haptophytes in the rbc L tree. Based on these analyses, we postulate that the plastid of peridinin- and fucoxanthin-containing dinoflagellates originated from a haptophyte tertiary endosymbiosis that occurred before the split of these lineages. Our findings imply that the presence of chlorophylls c 1 + c 2 and fucoxanthin, and the Form I rbc L gene are in fact the primitive (not derived, as widely believed) condition in dinoflagellates.

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  • Approximately half of the described dinoflagellate species maintain the peridinin-pigmented plastid thought to have been present in their common ancestor.

    “Approximately half of the described dinoflagellate species maintain the peridinin-pigmented plastid thought to have been present in their common ancestor (Yoon et al. 2002).”

    From Genomic Insights into Plastid Evolution (2020) · cites this paper as Yoon et al. 2002

    The Discussion (page not provided) calls fucoxanthin the primitive plastid condition and peridinin a derived state, contrary to the claim that the peridinin-pigmented plastid was present in the common ancestor. The introductory passage says about half of dinoflagellates are photosynthetic; it does not say that half of described species retain a peridinin plastid. (LLM, conf=0.88)

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  1. [2]2. Margulis, L., Corliss, J. O., Melkonian, M. & Chapman, D. J. (Jones and Bartlett, Boston), pp. 419-437.
  2. [7]7. Green, J. C., Leadbeater, B. S. C. & Diver, W. L. (Clarendon, Oxford), Vol. 38, pp. 207-227.
  3. [9]9. Green, J. C., Leadbeater, B. S. C. & Diver, W. L. (Clarendon, Oxford), Vol. 38, pp. 13-36.
  4. [12]12. Palmer, J. D. & Delwiche, C. F. (1996) Proc. Natl. Acad. Sci. USA 93, 7432-7435.
  5. [16]16. Bjørnland, T. & Liaaen-Jensen, S. (1989) in The Chromophyte Algae: Problems and Perspective, eds. Green, J. C., Leadbeater, B. S. C. & Diver, W. L. (Clarendon, Oxford), Vol. 38, pp. 37-60.
  6. [45]45. Lohr, M. & Wilhelm, C. (1999) Proc. Natl. Acad. Sci. USA 96, 8784 -8789.

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Authors
Yoon, H. S., Hackett, J. D., & Bhattacharya, D.
Affiliations
University of Iowa (US)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2002-08-09
Volume
99
Issue
18
Pages
11724-11729
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.172234799
PMC
PMC129336
OpenAlex
W2160201546
Cited by
442
References
42
Citations by year
2026: 20 · 2025: 26 · 2024: 23 · 2023: 20 · 2022: 27 · 2021: 19 · 2020: 26 · 2019: 22 · 2018: 18 · 2017: 9 · 2016: 17 · 2015: 10 · 2014: 20 · 2013: 19 · 2012: 8
FWCI
7.65
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Rutgers University Community Repository (Rutgers University) (submittedVersion)
Funders
National Science Foundation (0110252, 0107754)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
peridinin, fucoxanthin, haptophyte algae, chlorophyll c, plastid phylogeny, PsaA, psbA, rbcL, monophyly, plastid origin, red algae, Karenia
MeSH terms
Rhodophyta, Bacterial Proteins, Carotenoids, Membrane Proteins, Molecular Sequence Data, Phylogeny, Symbiosis, Plastids, Xanthophylls, Photosynthetic Reaction Center Complex Proteins, Photosystem I Protein Complex

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