The highly reduced genome of an enslaved algal nucleus
Open accessAbstract
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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Cites
A revised six-kingdom system of life
Cavalier‐Smith, T. (1998) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s0006323198005167 · Cited by 1,067 · see citing works
Self-citationProgress in Phycological Research
Round, F. E., & Chapman, D. J. (1995) · Bristol Research (University of Bristol) · Cited by 670 · see citing works
Cavalier-Smith, T. (1999) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.1999.tb04614.x · Cited by 629 · see citing works
Self-citationMembrane heredity and early chloroplast evolution
Cavalier-Smith, T. (2000) · Trends in Plant Science · doi:10.1016/s1360-1385(00)01598-3 · Cited by 482 · see citing works
Self-citationA Computational Screen for Methylation Guide snoRNAs in Yeast
Lowe, T. M., & Eddy, S. R. (1999) · Science · doi:10.1126/science.283.5405.1168 · Cited by 467 · see citing works
Meyer, H. H., Shorter, J., Seemann, J., Pappin, D., & Warren, G. (2000) · The EMBO Journal · doi:10.1093/emboj/19.10.2181 · Cited by 446 · see citing works
The origin of red algae and the evolution of chloroplasts
Moreira, D., Guyader, H. L., & Philippe, H. (2000) · Nature · doi:10.1038/35011054 · Cited by 427 · see citing works
Progress in Phycological Research
MOSS, B. L. (1985) · Phycologia · doi:10.2216/i0031-8884-24-3-374a.1 · Cited by 397 · see citing works
Heterogeneity of eukaryotic replicons, replicon clusters, and replication foci
Berezney, R., Dubey, D., & Huberman, J. (2000) · Chromosoma · doi:10.1007/s004120050399 · Cited by 390 · see citing works
Genome-wide bioinformatic and molecular analysis of introns in Saccharomyces cerevisiae
SPINGOLA, M., GRATE, L., HAUSSLER, D., & ARES, M. (1999) · RNA · doi:10.1017/s1355838299981682 · Cited by 316 · see citing works
Douglas, S. E., & Penny, S. L. (1999) · Journal of Molecular Evolution · doi:10.1007/pl00006462 · Cited by 303 · see citing works
Self-citationCryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes
Douglas, S. E., Murphy, C. A., Spencer, D. F., & Gray, M. W. (1991) · Nature · doi:10.1038/350148a0 · Cited by 284 · see citing works
Self-citationFrom extracellular to intracellular: the establishment of mitochondria and chloroplasts
Whatley, J. M., John, P., & Whatley, F. R. (1979) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1979.0020 · Cited by 277 · see citing works
Where is the root of the universal tree of life?
Forterre, P., & Philippe, H. (1999) · BioEssays · doi:10.1002/(sici)1521-1878(199910)21:10 · Cited by 244 · see citing works
The centromere of budding yeast
Hegemann, J. H., & Fleig, U. N. (1993) · BioEssays · doi:10.1002/bies.950150704 · Cited by 152 · see citing works
Centrosomal and Cytoplasmic Cdc2/Cyclin B1 Activation Precedes Nuclear Mitotic Events
Souza, C. P. C. D., Ellem, K. A. O., & Gabrielli, B. G. (2000) · Experimental Cell Research · doi:10.1006/excr.2000.4872 · Cited by 148 · see citing works
Gilson, P. R., & McFadden, G. I. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.7737 · Cited by 128 · see citing works
Lange, B. M. H., Bachi, A., Wilm, M., & González, C. (2000) · The EMBO Journal · doi:10.1093/emboj/19.6.1252 · Cited by 123 · see citing works
Gaasterland, T., & Sensen, C. W. (1996) · Biochimie · doi:10.1016/0300-9084(96)84761-4 · Cited by 114 · see citing works
Eschbach, S., Hofmann, C., Maier, U., Sitte, P., & Hansmann, P. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.8.1779 · Cited by 76 · see citing works
Self-citationZauner, S., Fraunholz, M. J., Wastl, J., Penny, S. L., Beaton, M. J., Cavalier‐Smith, T., Maier, U., & Douglas, S. E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.1.200 · Cited by 75 · see citing works
Self-citationTransport of Proteins into Cryptomonads Complex Plastids
Wastl, J., & Maier, U. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003125200 · Cited by 62 · see citing works
Self-citationPhysical mapping of the plastid genome from the chlorophyll c-containing alga, Cryptomonas Φ
Douglas, S. E. (1988) · Current Genetics · doi:10.1007/bf00434085 · Cited by 56 · see citing works
Self-citationThe skeletal function of non‐genic nuclear DNA: new evidence from ancient cell chimaeras
Cavalier‐Smith, T., & Beaton, M. J. (1999) · Genetica · doi:10.1023/a:1003701925110 · Cited by 52 · see citing works
Self-citationThe Nucleomorph Genomes of Cryptophytes and Chlorarachniophytes
Maier, U., Douglas, S. E., & Cavalier‐Smith, T. (2000) · Protist · doi:10.1078/1434-4610-00011 · Cited by 52 · see citing works
Self-citationLudwig, M. L., & Gibbs, S. P. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb40609.x · Cited by 47 · see citing works
A Nucleomorph-Encoded CbbX and the Phylogeny of RuBisCo Regulators
Maier, U. G., Fraunholz, M. J., Zauner, S., Penny, S. L., & Douglas, S. E. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026337 · Cited by 46 · see citing works
Self-citationKawahara, H., Philipova, R., Yokosawa, H., Patel, R., Tanaka, K., & Whitaker, M. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.15.2659 · Cited by 30 · see citing works
Mergers and acquisitions: malaria and the great chloroplast heist.
McFadden, G. I. (2000) · Genome biology · doi:10.1186/gb-2000-1-4-reviews1026 · Cited by 25 · see citing works
Higher-order chromatin structure: looping long molecules
Paul, A., & Ferl, R. J. (1999) · Plant Molecular Biology · doi:10.1023/a:1006323222693 · Cited by 23 · see citing works
Meyer, S. R. (1987) · South African Journal of Botany · doi:10.1016/s0254-6299(16)31447-8 · Cited by 11 · see citing works
Flagged first, then by citations
Research works printed but not linked: 9
- 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).
- 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).
- 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).
- 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).
- 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).
- Troy, C. S. Mitochondrial DNA Phylogeny and Biogeography of Domestic Cattle. Ph.D Thesis, Univ.- Dublin (1998).
- 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).
- 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).
- Macaulay, V. A. CRED: Credible Regions for Coalescence Times. (Univ. Oxford, 1998). Received 5 September 2000; accepted 14 February 2001.
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Katinka, M., Duprat, S., Cornillot, E., Méténier, G., Thomarat, F., Prensier, G., Barbe, V., Peyretaillade, E., Brottier, P., Wincker, P., et al. (2001) · Nature · doi:10.1038/35106579 · Cited by 1,051 · see citing works
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Malik, H. S., & Henikoff, S. (2003) · Nature Structural & Molecular Biology · doi:10.1038/nsb996 · Cited by 604 · see citing works
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Reyes-Prieto, A., Weber, A. P. M., & Bhattacharya, D. (2007) · Annual Review of Genetics · doi:10.1146/annurev.genet.41.110306.130134 · Cited by 453 · see citing works
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Archibald, J. M. (2009) · Current Biology · doi:10.1016/j.cub.2008.11.067 · Cited by 451 · see citing works
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Hackett, J. D., Anderson, D. M., Erdner, D. L., & Bhattacharya, D. (2004) · American Journal of Botany · doi:10.3732/ajb.91.10.1523 · Cited by 421 · see citing works
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Curtis, B. A., Tanifuji, G., Burki, F., Gruber, A., Irimia, M., Maruyama, S., Arias, M. C., Ball, S. G., Gile, G. H., Hirakawa, Y., et al. (2012) · Nature · doi:10.1038/nature11681 · Cited by 417 · see citing works
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Self-citationNozaki, H., Takano, H., Misumi, O., Terasawa, K., Matsuzaki, M., Maruyama, S., Nishida, K., Yagisawa, F., Yoshida, Y., Fujiwara, T., et al. (2007) · BMC Biology · doi:10.1186/1741-7007-5-28 · Cited by 309 · see citing works
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Sheiner, L., Demerly, J. L., Poulsen, N., Beatty, W. L., Lucas, O., Behnke, M. S., White, M. W., & Striepen, B. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002392 · Cited by 242 · see citing works
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Cavalier‐Smith, T., & Chao, E. E. (2004) · European Journal of Protistology · doi:10.1016/j.ejop.2004.01.002 · Cited by 145 · see citing works
Self-citationMartin, W. F., Rotte, C., Hoffmeister, M., Theißen, U., Gelius‐Dietrich, G., Ahr, S., & Henze, K. (2003) · IUBMB Life · doi:10.1080/1521654031000141231 · Cited by 145 · see citing works
Rivas, J. D. L., Lozano, J. J., & Ortíz, Á. R. (2002) · Genome Research · doi:10.1101/gr.209402 · Cited by 140 · see citing works
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Self-citationShen, G., Zhao, J., Reimer, S. K., Antonkine, M. L., Cai, Q., Weiland, S. M., Golbeck, J. H., & Bryant, D. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m201103200 · Cited by 138 · see citing works
Hoef‐Emden, K., & Melkonian, M. (2003) · Protist · doi:10.1078/143446103322454130 · Cited by 135 · see citing works
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van Dooren, G. G., Schwartzbach, S. D., Osafune, T., & McFadden, G. I. (2001) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(01)00154-9 · Cited by 128 · see citing works
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Dombrovska, O., & Qiu, Y. (2004) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2003.12.013 · Cited by 126 · see citing works
Nozaki, H., Matsuzaki, M., Takahara, M., Misumi, O., Kuroiwa, H., Hasegawa, M., Shin‐I, T., Kohara, Y., Ogasawara, N., & Kuroiwa, T. (2003) · Journal of Molecular Evolution · doi:10.1007/s00239-002-2419-9 · Cited by 124 · see citing works
Petersen, J., Ludewig, A.-K., Michael, V., Bunk, B., Jarek, M., Baurain, D., & Brinkmann, H. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu043 · Cited by 124 · see citing works
Molecular evolution of eukaryotic genomes: hemiascomycetous yeast spliceosomal introns
Bon, E. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg213 · Cited by 125 · see citing works
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Putignani, L., Tait, A., Smith, H. V., Horner, D. S., Tovar, J., Tetley, L., & Wastling, J. M. (2004) · Parasitology · doi:10.1017/s003118200400527x · Cited by 123 · see citing works
Wisecaver, J. H., & Hackett, J. D. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-366 · Cited by 120 · see citing works
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Fraser, C. M. (2005) · Genome Research · doi:10.1101/gr.3724205 · Cited by 119 · see citing works
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Patron, N. J., & Keeling, P. J. (2005) · Journal of Phycology · doi:10.1111/j.1529-8817.2005.00135.x · Cited by 113 · see citing works
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Bowen, N. J., & Jordan, I. K. (2002) · Current Issues in Molecular Biology · doi:10.21775/cimb.004.065 · Cited by 111 · see citing works
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Sanchez-Puerta, M. V., & Delwiche, C. F. (2008) · Journal of Phycology · doi:10.1111/j.1529-8817.2008.00559.x · Cited by 111 · see citing works
Nucleomorph genomes: structure, function, origin and evolution
Archibald, J. M. (2007) · BioEssays · doi:10.1002/bies.20551 · Cited by 108 · see citing works
Hoef‐Emden, K., Marin, B., & Melkonian, M. (2002) · Journal of Molecular Evolution · doi:10.1007/s00239-002-2313-5 · Cited by 109 · see citing works
Hackett, J. D., Maranda, L., Yoon, H. S., & Bhattacharya, D. (2003) · Journal of Phycology · doi:10.1046/j.1529-8817.2003.02100.x · Cited by 108 · see citing works
Mimivirus: the emerging paradox of quasi-autonomous viruses
Claverie, J., & Abergel, C. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.07.003 · Cited by 108 · see citing works
A high frequency of overlapping gene expression in compacted eukaryotic genomes
Williams, B., Slamovits, C. H., Patron, N. J., Fast, N. M., & Keeling, P. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501321102 · Cited by 106 · see citing works
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Shen, G., Saunée, N. A., Williams, S. R., Gallo, E. F., Schluchter, W. M., & Bryant, D. A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602563200 · Cited by 105 · see citing works
Maier, U., Zauner, S., Woehle, C., Bolte, K., Hempel, F., Allen, J. F., & Martin, W. F. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt181 · Cited by 102 · see citing works
Self-citationProtein Targeting into the Complex Plastid of Cryptophytes
Gould, S. B., Sommer, M. S., Hadfi, K., Zauner, S., Kroth, P. G., & Maier, U. (2006) · Journal of Molecular Evolution · doi:10.1007/s00239-005-0099-y · Cited by 101 · see citing works
Self-citationMcFadden, G. I. (2010) · PROTOPLASMA · doi:10.1007/s00709-010-0250-5 · Cited by 100 · see citing works
Misumi, O., Matsuzaki, M., Nozaki, H., Miyagishima, S., Mori, T., Nishida, K., Yagisawa, F., Yoshida, Y., Kuroiwa, H., & Kuroiwa, T. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.053991 · Cited by 100 · see citing works
Khan, H., Parks, N., Kozera, C., Curtis, B. A., Parsons, B. J., Bowman, S., & Archibald, J. M. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm101 · Cited by 107 · see citing works
- 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
- bronze
- doi.org
- 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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