Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes

Nature Reviews Genetics - Tập 5 Số 2 - Trang 123-135 - 2004
Jeremy N. Timmis1, Michael Ayliffe2, Chun Huang1, William Martin3
1School of Molecular and Biomedical Science, The University of Adelaide, South Australia 5005, Australia
2CSIRO Plant Industry, GPO Box 1600, Australian Capital Territory 2601, Australia
3Institute of Botany III, University of Düsseldorf, Düsseldorf, 40225, Germany

Tóm tắt

Từ khóa


Tài liệu tham khảo

Baur, E. Das Wesen und die Erblichkeitsverhältnisse der 'Varietates albomarginatae hort' von Pelargonium zonale. Z. Vererbungsl. 1, 330–351 (1909).

Mereschkowsky, C. Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralbl. 25, 593–604 (1905). [English translation Eur. J. Phycol. 34, 287–295, 1999]. The starting point of endosymbiotic theory. Outlines the reasoning that we still use today to explain the origin of plastids from cyanobacteria, a paper that was many decades ahead of its time.

Margulis, L. Origin of Eukaryotic Cells 349 (Yale Univ. Press, New Haven, 1970). The rediscovery of endosymbiotic theory after Wilson's 1928 condemnation of symbiosis as an evolutionary mechanism (see also reference 2).

Gray, M. W. & Doolittle, W. F. Has the endosymbiont hypothesis been proven? Microbol. Rev. 46, 1–42 (1982).

Bogorad, L. Evolution of organelles and eukaryotic genomes. Science 188, 891–898 (1975).

Ellis, R. J. Chloroplast proteins: synthesis, transport and assembly. Ann. Rev. Pl. Physiol. 32, 111–137 (1981).

Weeden, N. F. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J. Mol. Evol. 17, 133–139 (1981).

Martin, W. & Herrmann, R. G. Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118, 9–17 (1998).

Simpson, C. L. & Stern, D. B. The treasure trove of algal chloroplast genomes. Surprises in architecture and gene content, and their functional implications. Plant Physiol. 129, 957–966 (2002).

Gray, M. W., Burger, G. & Lang, B. F. Mitochondrial evolution. Science 283, 1476–1481 (1999).

Lang, B. F., Gray, M. W. & Burger, G. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33, 351–397 (1999).

Burger, G., Forget, L., Zhu, Y., Gray, M. W. & Lang, B. F. Unique mitochondrial genome architecture in unicellular relatives of animals. Proc. Natl Acad. Sci. USA 100, 892–897 (2003).

Embley, T. M. et al. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55, 387–395 (2003). An incisive and up-to-date review that covers the biology and evolutionary significance of hydrogenosomes, the mitochondria that endosymbiotic theory nearly forgot.

Zhang, Z., Green, B. R. & Cavalier-Smith, T. Single gene circles in dinoflagellate chloroplast genomes. Nature 400, 155–159 (1999).

Hannaert, V. et al. Plant-like traits associated with metabolism of Trypanosoma parasites. Proc. Natl Acad. Sci. USA 100, 1067–1071 (2003).

Cavalier-Smith, T. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5, 174–182 (2000).

Tielens, A. G., Rotte, C., van Hellemond, J. J. & Martin, W. Mitochondria as we don't know them. Trends Biochem. Sci. 27, 564–572 (2002).

Tovar, J. et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172–176 (2003).

Martin, W. et al. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl Acad. Sci. USA 99, 12246–12251 (2002). Shows that approximately 18% of the nuclear genes in Arabidopsis come from the ancestral plastid genome.

Wu, M. et al. The genome sequence and evolution of the reproductive parasite Wolbachia pipientis wMel: a streamlined α-proteobacterium massively infected with mobile genetic elements. PLoS Biology (in the press). Incisive evolutionary insights into endosymbiont genome biology with a genome phylogeny for mitochondrial origin.

Stern, D. B. & Lonsdale, D. M. Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature 299, 698–702 (1982). The paper that initiated progress; showed that DNA was able to migrate between the genetic compartments of eukaryotes.

Jacobs, H. T. et al. Mitochondrial DNA sequences in the nuclear genome of Strongylocentrotus purpuratus. J. Mol. Biol. 165, 609–632 (1983).

Farrely, F. & Butow, R. A. Rearranged mitochondrial genes in the yeast nuclear genome. Nature 301, 296–301 (1983).

Timmis, J. N. & Scott, N. S. Spinach nuclear and chloroplast DNAs have homologous sequences. Nature 305, 65–67 (1983).

Ellis, R. J. Promiscuous DNA — chloroplast genes inside plant mitochondria. Nature 299, 678–679 (1982).

Lopez, J. V., Yuhki, N., Masuda, R., Modi, W. & O'Brien, S. J. Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. J. Mol. Evol. 39, 174–190 (1994).

Bensasson, D., Zhang, D. X. & Hewitt, G. M. Frequent assimilation of mitochondrial DNA by grasshopper nuclear genomes. Mol. Biol. Evol. 17, 406–415 (2000).

Mundy, N. I., Pissinatti, A. & Woodruff, D. S. Multiple nuclear insertions of mitochondrial cytochrome b sequences in callitrichine primates. Mol. Biol. Evol. 17, 1075–1080 (2000).

Lu, X. M., Fu, Y. X. & Zhang, Y. P. Evolution of mitochondrial cytochrome b pseudogene in genus Nycticebus. Mol. Biol. Evol. 19, 2337–2341 (2002).

Williams, S. T. & Knowlton, N. Mitochondrial pseudogenes are pervasive and often insidious in the snapping shrimp genus Alpheus. Mol. Biol. Evol. 18, 1484–1493 (2001).

Olson, L. E. & Yoder, A. D. Using secondary structure to identify ribosomal numts: cautionary examples from the human genome. Mol. Biol. Evol. 19, 93–100 (2002). Together with reference 32, points out that numts are often mistaken for genuine mitochondrial DNA sequences.

Bensasson, D., Zhang, D., Hartl, D. L. & Hewitt, G. M. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends Ecol. Evol. 16, 314–321 (2001).

Ricchetti, M., Fairhead, C. & Dujon, B. Mitochondrial DNA repairs double strand breaks in yeast chromosomes. Nature 402, 96–100 (1999). The initial genome-wide survey for numts; indicates a role for recombination in numt integration.

Mourier, T., Hansen, A. J., Willerslev, E. & Arctander, P. The human genome project reveals a continuous transfer of large mitochondrial fragments to the nucleus. Mol. Biol. Evol. 18, 1833–1837 (2001).

Tourmen, Y. et al. Structure and chromosomal distribution of human mitochondrial pseudogenes. Genomics 80, 71–77 (2002).

Hazkani-Covo, E., Sorek, R. & Graur, D. Evolutionary dynamics of large numts in the human genome: rarity of independent insertions and abundance of post-insertion duplications. J. Mol. Evol. 56, 169–174 (2003). A careful and detailed inspection of numt duplication dynamics during human and primate genome evolution.

Woischnik, M. & Moraes, C. T. Pattern of organisation of human mitochondrial pseudogenes in the nuclear genome. Genome Res. 12, 885–893 (2002).

Richly, E. & Leister, D. Numts in sequenced eukaryotic genomes. Mol. Biol. Evol. (in the press).

Lin, X. Y. et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761–768 (1999). Reports a nearly complete, ∼270-kb copy of the 367-kb Arabidopsis mtDNA near the centromere.

Stupar, R. M. et al. Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc. Natl Acad. Sci. USA 98, 5099–5103 (2001). Shows that the 270-kb copy in reference 39 is really the complete 367-kb circle.

The, Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).

Yuan, Q. et al. Genome sequencing of 239-kb region of rice chromosome 10L reveals a high frequency of gene duplication and a large chloroplast DNA insertion. Mol. Genet. Genom. 267, 713–720 (2002). First hints from genome sequences of large cpDNA chunks (>30 kb) that are integrated in nuclear chromosomes.

The Rice Chromosome 10 Sequencing Consortium. In-depth view of structure, activity, and evolution of rice chromosome 10. Science 300, 1566–1569 (2003). Reports a nearly complete cpDNA genome chunk (130 kb) that is integrated in the nuclear chromosome.

Shahmuradov, I. A., Akbarova, Y. Y., Solovyev, V. V. & Aliyev, J. A. Abundance of plastid DNA insertions in nuclear genomes of rice and Arabidopsis. Plant Mol. Biol. 52, 923–934 (2003).

Ayliffe, M. A. & Timmis, J. N. Tobacco nuclear DNA contains long tracts of homology to chloroplast DNA. Theor. Appl. Genet. 85, 229–238 (1992).

Ayliffe, M. A. & Timmis, J. N. Plastid DNA sequence homologies in the tobacco nuclear genome. Mol. Gen. Genet. 236, 105–112 (1992).

Boore, J. L. Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767–1780 (1999).

Brennicke, A., Grohmann, L., Hiesel, R., Knoop, V. & Schuster, W. The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Lett. 325, 140–145 (1993).

Adams, K. L. & Palmer, J. D. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylog. Evol. 29, 380–395 (2003). A lucid review of flowering plant mitochondrial gene migration to the nucleus.

Adams, K. L., Daley, D. O., Qiu, Y. L., Whelan, J. & Palmer, J. D. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 408, 354–357 (2000).

Adams, K. L, Qiu Y. -L., Stoutemyer, M. & Palmer J. D. Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc. Natl Acad. Sci. USA 99, 9905–9912 (2002). A broad survey of mitochondrial genome reduction that is accompanied by nuclear integration events in flowering plant evolution.

Henze, K. & Martin, W. How are mitochondrial genes transferred to the nucleus? Trends Genet. 17, 383–387 (2001).

Thorsness, P. E. & Weber, E. R. Escape and migration of nucleic acids between chloroplasts, mitochondria, and the nucleus. Int. Rev. Cytol. 165, 207–234 (1996). An excellent review that covers the mechanics of gene transfer from organelles to the nucleus in the pre-genome era.

Blanchard, J. L. & Lynch, M. Organellar genes — why do they end up in the nucleus? Trends Genet. 16, 315–320 (2000).

Figueroa, P., Gomez, I., Holuigue, L., Araya, A. & Jordana, X. Transfer of rps14 from the mitochondrion to the nucleus in maize implied integration within a gene encoding the iron-sulphur subunit of succinate dehydrogenase and expression by alternative splicing. Plant J. 18, 601–609 (1999). Fortuitous recombination in the establishment of active gene transfers.

Kubo, N., Harada, K., Hirai, A. & Kadowaki, K. A single nuclear transcript encoding mitochondrial RPS14 and SSDHB of rice is processed by alternative splicing: common use of the same mitochondrial targeting signal for different proteins. Proc. Natl Acad. Sci. USA 96, 9207–9211 (1999). The establishment of active gene transfers can involve the recruitment of pre-existing transit peptide regions.

Long, M., de Souza, S. J., Rosenberg, C. & Gilbert, W. Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c1 precursor. Proc. Natl Acad. Sci. USA 93, 7727–7731 (1996). Gene transfers can involve conversion of a pre-existing nuclear coding region for a cytosolic enzyme into a transit peptide.

Millen, R. S. et al. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13, 645–658 (2001).

Martin, W. et al. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162–165 (1998).

Lang, B. F. et al. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387, 493–497 (1997). The still unsurpassed mitchondrial genome in terms of gene content and streamlined organization.

Henze, K. et al. A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. Proc. Natl Acad. Sci. USA 92, 9122–9126 (1995).

Stibitz, T. B., Keeling, P. J., & Bhattacharya, D. Symbiotic origin of a novel actin gene in the cryptophyte Pyrenomonas helgolandii. Mol. Biol. Evol. 17, 1731–1738 (2000).

Archibald, J. M., Rogers, M. B., Toop, M., Isheda, K. & Keeling, P. J. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl Acad. Sci. USA 100, 7678–7683 (2003).

Leister, D. Chloroplast research in the genomics age. Trends Genet. 19, 47–56 (2003).

Gabaldón, T. & Huynen, M. A. Reconstruction of the proto-mitochondrial metabolism. Science 301, 609 (2003).

Martin, W. & Schnarrenberger, C. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32, 1–18 (1997).

Gallois, J. L. et al. The Arabidopsis chloroplast ribosomal protein L21 is encoded by a nuclear gene of mitochondrial origin. Gene 274, 179–185 (2001).

Adams, K. L. et al. Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 14, 931–943 (2002).

Brown, J. R. Ancient horizontal gene transfer. Nature Rev. Genet. 4, 121–132 (2003). An incisive review of gene movement across genomes, including the role of endosymbiotic transfers.

Gil, R. et al. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl Acad. Sci. USA 100, 9388–9393 (2003). Underscores how reductive evolution in endosymbiotic bacteria leads to massive gene losses through biochemical parasitism of the host.

Lister, D. L., Bateman, J. M., Purton, S. & Howe, C. J. DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316, 33–38 (2003).

Richly, E., Chinnery, P. F. & Leister, D. Evolutionary diversification of mitochondrial proteomes: implications for human disease. Trends Genet. 19, 356–362 (2003).

Richly, E. & Leister, D. An improved prediction of chloroplast proteins reveals diversities and commonalities in the chloroplast proteomes of Arabidopsis and rice. Gene (in the press).

Huh, W. -K. et al. Global analysis of protein localization in budding yeast. Nature 425, 686–691 (2003).

Lange, B. M., Rujan, T., Martin, W. & Croteau, R. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl Acad. Sci. USA 97, 13172–13177 (2000).

Schnarrenberger, C. & Martin, W. Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants: a case study of endosymbiotic gene transfer. Eur. J. Biochem. 269, 868–883 (2002).

Aravind, L., Anantharaman, V. & Iyer, L. M. Evolutionary connections between bacterial and eukaryotic signaling systems: a genomic perspective. Curr. Opin. Microbiol. 6, 490–497 (2003).

Osteryoung, K. W. & Nunnari, J. The division of endosymbiotic organelles. Science 302, 1698–1704 (2003).

McFadden, G. I. & Ralph, S. A. Dynamin: the endosymbiosis ring of power? Proc. Natl Acad. Sci. USA 100, 3557–3559 (2003).

Thorsness, P. E. & Fox, T. D. Escape of DNA from the mitochondria to the nucleus in the yeast, Saccharomyces cerevisiae. Nature 346, 376–379 (1990). The initial experimental measurement of the frequency of transfer of DNA between genetic compartments.

Thorsness, P. E. & Fox, T. D. Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics 134, 21–28 (1993).

Shafer, K. S., Hanekamp, T., White, K. H. & Thorsness, P. E. Mechanisms of mitochondrial DNA escape to the nucleus in the yeast Saccharomyces cerevisiae. Curr. Genet. 36, 183–194 (1999).

Huang, C. Y., Ayliffe, M. A. & Timmis, J. N. Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422, 72–76 (2003). The initial experimental measurement of the frequency of integrative transfer of DNA between chloroplast and nucleus.

Stegemann, S., Hartmann, S., Ruf, S. & Bock, R. High-frequency gene transfer from the chloroplast genome to the nucleus. Proc. Natl Acad. Sci. USA 100, 8828–8833 (2003).

Campbell, C. L. & Thorsness, P. E. Escape of mitochondrial DNA to the nucleus in yme1 yeast is mediated by vacuolar-dependent turnover of abnormal mitochondrial compartments. J. Cell Sci. 111, 2455–2464 (1998).

Shay, J. W. & Werbin, H. New evidence for the insertion of mitochondrial DNA into the human genome: significance for cancer and aging. Mutat. Res. 275, 227–235 (1992).

Turner, C. et al. Human genetic disease caused by de novo mitochondrial-nuclear DNA transfer. Hum. Genet. 112, 303–309 (2003).

Elo, A. et al. Nuclear genes that encode mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome. Plant Cell 15, 1619–1631 (2003).

Richly, E. et al. Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep. 4, 491–498 (2003).

Allen, J. F. The function of genomes in bioenergetic organelles. Phil. Trans. Roy. Soc. B 358, 19–38 (2003). A comprehensive treatment of competing views on the issue of why some genes remain within organelle genomes.

Pérez-Martínez, X. et al. Subunit II of cytochrome c oxidase in chlamydomonad algae is a heterodimer encoded by two independent nuclear genes. J. Biol. Chem. 276, 11302–11309 (2001)

Daley, D. O. et al. Intracellular gene transfer: reduced hydrophobicity facilitates gene transfer for subunit 2 of cytochrome c oxidase. Proc. Natl Acad. Sci. USA 99, 10510–15015 (2002).

Pfannschmidt, T., Nilsson, A., & Allen, J. F. Photosynthetic control of chloroplast gene expression. Nature 397, 625–628 (1999).

Naithani S., Saracco S. A., Butler C. A. & Fox T. D. Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol. Biol. Cell 14, 324–333 (2003).

Doolittle, W. F. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307–311 (1998).

Race, H. L., Herrmann, R. G. & Martin, W. Why have organelles retained genomes? Trends Genet. 15, 364–370 (1999).

Devos, K. M., Brown, J. K. M. & Bennetzen J. L. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12, 1075–1079 (2002).

Martin, W. Gene transfers from organelles to the nucleus: frequent and in big chunks. Proc. Natl Acad. Sci. USA 100, 8612–8614 (2003).

Maliga, P. Engineering the plastid genome of higher plants. Curr. Opin. Plant Biol. 5, 164–172 (2002).

Daniell, H. & Parkinson, C. L. Jumping genes and containment. Nature Biotechnol. 21, 374–375 (2003). A challenge to the experimental data for gene transfer from chloroplasts by proponents of plastid transgene technology, rebutted head-to-head in reference 101.

Huang, C. Y., Ayliffe, M. A. & Timmis, J. N. Organelle evolution meets biotechnology. Nature Biotechnol. 21, 489–490 (2003).

Martin, W. & Russell, M. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil. Trans. Roy. Soc. Lond. B 358, 59–85 (2003).

Doolittle, W. F. et al. How big is the iceberg of which organellar genes in nuclear genomes are but the tip? Philos. Trans. Roy. Soc. Lond. B 358, 39–57 (2003).

Woese, C., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains archaea, bacteria and eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990). The current higher-level taxonomic model, with eukaryotes as sisters to archaebacteria.

Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239–6244 (1998). A landmark paper that uncovers more eubacterial genes than archaebacterial genes in the yeast genome.

Penny, D., Foulds, L. R. & Hendy, M. D. Testing the theory of evolution by comparing phylogenetic trees constructed from five different protein sequences. Nature 297, 197–200 (1982).

Cummings, M. P., Otto, S. P. & Wakeley, J. Sampling properties of DNA-sequence data in phylogenetic analysis. Mol. Biol. Evol. 12, 814–822 (1995).

Embley, T. M. & Hirt, R. P. Early branching eukaryotes? Curr. Opin. Genet. Dev. 8, 655–661 (1998).

Rokas, A., Williams, B. L., King, N. & Carroll, S. B. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798–804 (2003).

Gogarten P. J., Doolittle W. F. & Lawrence J. G. Prokaryotic evolution in light of lateral gene transfer. Mol. Biol. Evol. 19, 2226–2238 (2002).

Hedges, S. B. et al. A genomic timescale for the origin of eukaryotes. BMC Evol. Biol. 1, 4 (2001).

Hartman, H. & Fedorov, A. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl Acad. Sci. USA 99, 1420–1425 (2002).

Stechmann, A. & Cavalier-Smith, T. Rooting the eukaryote tree by using a derived gene fusion. Science 297, 89–91 (2002). A milestone relating to the issue of which eukaryotes might be the most ancient.

Kondo, N., Nikoh, N., Ijichi, N., Shimada, M. & Fukatsu, T. Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc. Natl Acad. Sci. USA 99, 14280–14285 (2002).

Neupert, W. Protein import into mitochondria. Ann. Rev. Biochem. 66, 683–717 (1997).

Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998).

Soll, J. Protein import into chloroplasts. Curr. Opin. Plant. Biol. 5, 529–535 (2002).

Bendich, A. J. & Drlica, K. Prokaryotic and eukaryotic chromosomes: what's the difference? BioEssays 22, 481–486 (2000). An enlightening survey of chromosome attributes in prokaryotes and eukaryotes.

Birky, C. W. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms and models. Annu. Rev. Genet. 35, 125–148 (2001).

Martin, W., Hoffmeister, M., Rotte, C. & Henze, K. An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol. Chem. 382, 1521–1539 (2001).

Butterfield, N. J. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/ Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386–404 (2000). A fossil red algae of 1. 2 billion years of age anchors plant evolution in the Precambrian age.