Cited by 454Protist diversity and phylogenyChromosomal and Genetic VariationsPhotosynthetic Processes and Mechanisms

The highly reduced genome of an enslaved algal nucleus

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Douglas, Susan, Zauner, Stefan, Fraunholz, Martin, Beaton, Margaret, Penny, Susanne, Deng, Lang-Tuo, Wu, Xiaonan, Reith, Michael +2 more·2001·Nature

Abstract

Chromophyte algae differ fundamentally from plants in possessing chloroplasts that contain chlorophyll c and that have a more complex bounding-membrane topology. Although chromophytes are known to be evolutionary chimaeras of a red alga and a non-photosynthetic host, which gave rise to their exceptional membrane complexity, their cell biology is poorly understood. Cryptomonads are the only chromophytes that still retain the enslaved red algal nucleus as a minute nucleomorph. Here we report complete sequences for all three nucleomorph chromosomes from the cryptomonad Guillardia theta. This tiny 551-kilobase eukaryotic genome is the most gene-dense known, with only 17 diminutive spliceosomal introns and 44 overlapping genes. Marked evolutionary compaction hundreds of millions of years ago eliminated nearly all the nucleomorph genes for metabolic functions, but left 30 for chloroplast-located proteins. To allow expression of these proteins, nucleomorphs retain hundreds of genetic-housekeeping genes. Nucleomorph DNA replication and periplastid protein synthesis require the import of many nuclear gene products across endoplasmic reticulum and periplastid membranes. The chromosomes have centromeres, but possibly only one loop domain, offering a means for studying eukaryotic chromosome replication, segregation and evolution.

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  • T1-T8 all indicate independent secondary symbioses each for Euglena, and importantly for Guillardia and Odontella.

    “T1–T8 all indicate independent secondary symbioses (plastid origins from eukaryotic symbionts; refs. 2, 3, and 8) each for Euglena, and importantly for Guillardia and Odontella.”

    From Evolutionary analysis of <i>Arabidopsis</i> , cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus (2002) · cites this paper as [8]

    The Abstract and Figure 1 caption describe independent secondary symbioses involving eukaryotic algal symbionts, and the Abstract identifies Guillardia theta as a cryptomonad. But the paper places the red-algal symbiosis in the common ancestor of cryptomonads and other chromophytes; it does not establish a separate event for each named organism or address T1–T8. Odontella is not identified in the passages found. (LLM, conf=0.83)

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Research works printed but not linked: 9

  1. Loftus, R. T., MacHugh, D. E., Bradley, D. G., Sharp, P. M. & Cunningham, P. Evidence for two independent domestications of cattle. Proc. Natl Acad. Sci. USA 91, 2757±2761 (1994).
  2. Bradley, D. G., MacHugh, D. E., Cunningham, P. & Loftus, R. T. Mitochondrial diversity and the origins of African and European cattle. Proc. Natl Acad. Sci. USA 93, 5131±5135 (1996).
  3. Bailey, J. F. et al. Ancient DNA suggests a recent expansion of European cattle from a diverse wild progenitor species. Proc. R. Soc. Lond. B 263, 1467±1473 (1996).
  4. Excof®er, L. & Schneider, S. Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc. Natl Acad. Sci. USA 96, 10597±10602 (1999).
  5. Cymbron, T., Loftus, R. T., Malheiro, M. I. & Bradley, D. G. Mitochondrial sequence variation suggests an African in¯uence in Portuguese cattle. Proc. R. Soc. Lond. B 266, 597±603 (1999).
  6. Troy, C. S. Mitochondrial DNA Phylogeny and Biogeography of Domestic Cattle. Ph.D Thesis, Univ.- Dublin (1998).
  7. Yang, D. Y., Eng, B., Waye, J. S., Dudar, J. C. & Saunders, S. R. Technical note: improved DNA extraction from ancient bones using silica-based spin columns. Am. J. Phys. Anthropol. 105, 539±543 (1998).
  8. MacHugh, D. E. et al. Early mediaeval cattle remains from a Scandinavian settlement in Dublin: genetic analysis and comparison with extant breeds. Phil. Trans. R. Soc. Lond. B 354, 99±109 (1999).
  9. Macaulay, V. A. CRED: Credible Regions for Coalescence Times. (Univ. Oxford, 1998). Received 5 September 2000; accepted 14 February 2001.

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Authors
Douglas, S., Zauner, S., Fraunholz, M., Beaton, M., Penny, S., Deng, L.-T., Wu, X., Reith, M., Cavalier-Smith, T., & Maier, U.-G.
Affiliations
  • Canadian Institute for Advanced Research (CA)
  • Philipps University of Marburg (DE)
Venue
Nature
Published
2001-04-26
Volume
410
Issue
6832
Pages
1091-1096
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W1582655487
Cited by
454
References
31
Citations by year
2026: 4 · 2025: 2 · 2024: 9 · 2023: 9 · 2022: 5 · 2021: 5 · 2020: 12 · 2019: 10 · 2018: 9 · 2017: 13 · 2016: 12 · 2015: 11 · 2014: 22 · 2013: 23 · 2012: 21
FWCI
12.14
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • Wellcome Trust
  • European Commission
  • Natural Sciences and Engineering Research Council of Canada
  • Natural Environment Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
Keywords
nucleomorph, cryptophytes, Guillardia theta, genome reduction, spliceosomal introns, chloroplast proteins, centromere, chromosome replication, chromosome segregation, endoplasmic reticulum
MeSH terms
Cyanobacteria, Rhodophyta, Base Sequence, Cell Nucleus, Chloroplasts, Chromosome Mapping, Molecular Sequence Data, Symbiosis, Genome, Sequence Analysis, DNA, Eukaryota

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