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How Did the Eukaryotes Evolve?

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Abstract

The fossil record shows that the stromatolites built by cyanobacteria 2 and 3 billion years ago are virtually identical to those built by their modern descendants, which is just a part of much evidence revealing that bacteria have barely changed in billions of years. They appeared very early in the history of life and have conserved their complexity (in terms of size, shape, and number of components) ever since. The eukaryotes, however, did the opposite. They repeatedly increased the complexity of their cells and eventually broke the cellular barrier and gave origin to all living creatures that we see around us. This gives us one of the major problems in evolution: why have the prokaryotes maintained the same complexity throughout the history of life while the eukaryotes have become increasingly more complex? Here it is shown that a solution does exist, but it is based on experimental data that so far have largely been ignored. It is based on the discovery that, in addition to the genetic code, many other organic codes exist in living systems. The potential to generate organic codes was already present in the common ancestor but was not transmitted indefinitely to all its descendants. After the genetic code and the signal transduction codes that gave origin to the first cells, the prokaryotes evolved no other organic code, whereas the ancestors of the eukaryotes continued to explore the coding space and gave origin to splicing codes, histone code, cytoskeleton codes, tubulin code, compartment codes, and sequence codes. This experimental fact suggests that the prokaryotes did not increase their complexity because they did not evolve new organic codes, whereas the eukaryotes became increasingly more complex because they maintained the potential to bring new codes into existence.

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References

  • Acevedo-Rocha C, Budisa N (2016) Xenomicrobiology: a roadmap for genetic code engineering. Microb Biotechnol 9:666–676

    Article  Google Scholar 

  • Adl SM, Simpson ABG, Farmer MA et al (2005) The new higher-level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451

    Article  Google Scholar 

  • Agalioti T, Chen G, Thanos D (2002) Deciphering the transcriptional histone acetylation code for a human gene. Cell 111(3):381–392

    Article  Google Scholar 

  • Alberts B, Johnson A, Lewis J et al (2007) Molecular biology of the cell, 5th edn. Garland, New York

    Google Scholar 

  • Altaba AR, Nguien V, Palma V (2003) The emergent design of the neural tube: prepattern, SHH morphogen and GLI code. Curr Opin Genet Dev 13:513–521

    Article  Google Scholar 

  • Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706

    Article  Google Scholar 

  • Barash Y, Calarco JA, Gao W et al (2010) Deciphering the splicing code. Nature 465:53–59

    Article  Google Scholar 

  • Barbieri M (2003) The organic codes: an introduction to semantic biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Barbieri M (2015a) Evolution of the genetic code: the ribosome-oriented model. Biol Theory 10:301–310

    Article  Google Scholar 

  • Barbieri M (2015b) Code biology: a new science of life. Springer, Dordrecht

    Book  Google Scholar 

  • Barbieri M (2016) From the common ancestor to the first cells: the code theory. Biol Theory 11:102–112

    Article  Google Scholar 

  • Barghoorn ES, Tyler SM (1965) Microfossils from the Gunflint chert. Science 147:563–577

    Article  Google Scholar 

  • Barisic M, Maiato H (2016) The tubulin code: a navigation system for chromosomes during mitosis. Trends Cell Biol 26(10):766–775

    Article  Google Scholar 

  • Basañez G, Hardwick JM (2008) Unravelling the Bcl-2 apoptosis code with a simple model system. PLoS Biol 6(6):e154. doi:10.137/journal.pbio.0060154

    Article  Google Scholar 

  • Battail G (2007) Information theory and error-correcting codes in genetics and biological evolution. In: Barbieri M (ed) Introduction to biosemiotics. Springer, Dordrecht, pp 299–345

    Google Scholar 

  • Battail G (2014) Information and life. Springer, Dordrecht

    Book  Google Scholar 

  • Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412

    Article  Google Scholar 

  • Berridge M (1985) The molecular basis of communication within the cell. Sci Am 253:142–152

    Article  Google Scholar 

  • Bilwes AM, Alex LA, Crane BR, Simon MI (1999) Structure of CheA, a signal-transducing histidine kinase. Cell 96:131–141

    Article  Google Scholar 

  • Blobel G (1980) Intracellular membrane topogenesis. Proc Natl Acad Sci USA 77:1496–1500

    Article  Google Scholar 

  • Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. J Cell Biol 67:852–862

    Article  Google Scholar 

  • Blumenthal T (2004) Operons in eukaryotes. Brief Funct Genomics Proteomics 3:199–211

    Article  Google Scholar 

  • Brandon MP, Hasselmo ME (2009) Sources of the spatial code within the hippocampus. Biol Rep 1:3–7

    Google Scholar 

  • Brown JR, Doolittle WF (1997) Archaea and the prokaryote–eukaryote transition. Microbiol Rev 61:456–502

    Google Scholar 

  • Buckeridge MS, De Souza AP (2014) Breaking the “glycomic code” of cell wall polysaccharides may improve second-generation bioenergy production from biomass. Bioenerg Res 7:1065–1073. doi:10.1007/s12155-014-9460-6

    Article  Google Scholar 

  • Budisa N (2004) Prolegomena to future efforts on genetic code engineering by expanding its amino acid repertoire. Angew Chem Int Ed 43:3387–3428

    Article  Google Scholar 

  • Budisa N (2014) Xenobiology, new-to-nature synthetic cells and genetic firewall. Curr Org Chem 18:936–943

    Article  Google Scholar 

  • Buratti E, Baralle M, Baralle FE (2006) Defective splicing, disease and therapy: searching for master checkpoints in exon definition. Nucleic Acids Res 34:3494–3510

    Article  Google Scholar 

  • Chakraborti S, Natarajan K, Curiel J et al (2016) The emerging role of the tubulin code: from the tubulin molecule to neuronal function and disease. Cytoskeleton. doi:10.1002/cm.21290

    Google Scholar 

  • Cooper TA, Wan L, Dreyfuss G (2009) RNA and disease. Cell 136:777–793

    Article  Google Scholar 

  • De Beule J (2014) Sketch for a theory of evolution based on coding. Biosemiotics 7(2):181–201

    Article  Google Scholar 

  • De Beule J, Hovig E, Benson M (2011) Introducing dynamics into the field of biosemiotics. Biosemiotics 4(1):5–24

    Article  Google Scholar 

  • Dhir A, Buratti E, van Santen MA et al (2010) The intronic splicing code: multiple factors involved in ATM pseudoexon definition. EMBO J 29:749–760

    Article  Google Scholar 

  • Di Lorenzo PM (2000) The neural code for taste in the brain stem: response profiles. Physiol Behav 69:87–96

    Article  Google Scholar 

  • Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2129

    Article  Google Scholar 

  • Doolittle WF, Bapteste E (2007) Pattern pluralism and the tree of life hypothesis. Proc Natl Acad Sci USA 104:2043–2049

    Article  Google Scholar 

  • Dudai Y (1999) The smell of representations. Neuron 23:633–635

    Article  Google Scholar 

  • Farina A, Pieretti N (2014) Acoustic codes in action in a soundscape context. Biosemiotics 7(2):321–328

    Article  Google Scholar 

  • Farquhar MG (1985) Progress in unravelling pathways of golgi traffic. Ann Rev Cell Biol 1:447–488

    Article  Google Scholar 

  • Fitch WM, Upper K (1987) The phylogeny of tRNA sequences provides evidence for ambiguity reduction in the origin of the genetic code. Cold Spring Harb Symp Quant Biol 52:759–767

    Article  Google Scholar 

  • Flames N, Pla R, Gelman DM et al (2007) Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 27(36):9682–9695

    Article  Google Scholar 

  • Fu XD (2004) Towards a splicing code. Cell 119:736–738

    Article  Google Scholar 

  • Füllgrabe J, Hajji N, Joseph B (2010) Cracking the death code: apoptosis-related histone modifications. Cell Death Differ 17:1238–1243

    Article  Google Scholar 

  • Gabius H-J (2000) Biological information transfer beyond the genetic code: the sugar code. Naturwissenschaften 87:108–121

    Article  Google Scholar 

  • Gabius H-J (2009) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim

    Google Scholar 

  • Gamow G (1954) Possible relation between deoxyribonucleic acid and protein structures. Nature 173:318

    Article  Google Scholar 

  • Gilmore R, Blobel G, Walter P (1982) Protein translocation across the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle. J Cell Biol 95:463–469

    Article  Google Scholar 

  • Gimona M (2008) Protein linguistics and the modular code of the cytoskeleton. In: Barbieri M (ed) The codes of life: the rules of macroevolution. Springer, Dordrecht, pp 189–206

    Chapter  Google Scholar 

  • Görlich D, Artmann S, Dittrich P (2011) Cells as semantic systems. Biochem Biophys Acta 1810(10):914–923

    Article  Google Scholar 

  • Görlich D, Dittrich P (2013) Molecular codes in biological and chemical reaction networks. PLoS ONE 8(1):e54694. doi:10.1371/journal.pone.0054694

    Article  Google Scholar 

  • Gräff J, Mansuy IM (2008) Epigenetic codes in cognition and behavior. Behav Brain Res 192:70–87

    Article  Google Scholar 

  • Haeckel E (1866) Generalle Morphologie der Organismen. Georg Reimer, Berlin

    Book  Google Scholar 

  • Hafting T, Fyhn M, Molden S et al (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806

    Article  Google Scholar 

  • Hallock RM, Di Lorenzo PM (2006) Temporal coding in the gustatory system. Neurosci Behav Rev 30:1145–1160

    Article  Google Scholar 

  • Hansen JC, Tse C, Wolfe AP (1998) Structure and function of the core histone N-termini: more than meets the eye. Biochemistry 37:17637–17641

    Article  Google Scholar 

  • Harold FM (2014) In search of cell history: the evolution of life’s building blocks. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Hart AC, Sims S, Kaplan JM (1995) Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378:82–85

    Article  Google Scholar 

  • Hartman MCT, Josephson K, Lin C-W, Szostak JW (2007) An expanded set of amino acid analogs for the ribosomal translation of unnatural peptides. PLoS One 2(10):e972. doi:10.1371/journal.pone.0000972

    Article  Google Scholar 

  • Hou Y-M, Schimmel P (1988) A simple structural feature is a major determinant of the identity of a transfer RNA. Nature 333:140–145

    Article  Google Scholar 

  • Hunt P, Whiting J, Nonchev S et al (1991) The branchial Hox code and its implications for gene regulation, patterning of the nervous system and head evolution. Development 2:63–77

    Google Scholar 

  • Janke C (2014) The tubulin code: molecular components, readout mechanisms, and functions. J Cell Biol 206(4):461–472

    Article  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  Google Scholar 

  • Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Genet 1:20–29

    Article  Google Scholar 

  • Jun S-R, Sims GE, Wu GA, Kim SH (2010) Whole genome phylogeny of prokaryotes by feature frequency profiles: an alignment-free method with optimal resolution. Proc Natl Acad Sci USA 107:133–138

    Article  Google Scholar 

  • Keeling PJ, Burger G, Durnford DG et al (2005) The tree of the eukaryotes. Trends Ecol Evol 20:670–676

    Article  Google Scholar 

  • Kelly RB (1985) Pathways of protein secretion in eukaryotes. Science 230:25–31

    Article  Google Scholar 

  • Kessel M, Gruss P (1991) Homeotic transformation of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:89–104

    Article  Google Scholar 

  • Kim J, Daniel J, Espejo A et al (2006) Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep 7(4):397–403

    Google Scholar 

  • Kindler S, Wang H, Richter D, Tiedge H (2005) RNA transport and local control of translation. Annu Rev Cell Dev Biol 21:223–245

    Article  Google Scholar 

  • Knoll AH (2003) Life on a young planet. The first three billion years of evolution on Earth. Princeton University Press, Princeton

    Google Scholar 

  • Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81:203–229

    Article  Google Scholar 

  • Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1:127–136

    Article  Google Scholar 

  • Koonin EV (2007) The biological big bang model for the major transitions in evolution. Biol Direct 1:22

    Article  Google Scholar 

  • Koonin EV (2012) The logic of chance. The nature and origin of biological evolution. Pearson Education, Upper Saddle River

    Google Scholar 

  • Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–294

    Article  Google Scholar 

  • Kühn S, Hofmeyr J-HS (2014) Is the “histone code” an organic code? Biosemiotics 7(2):203–222

    Article  Google Scholar 

  • Kurland CG, Collins LJ, Penny D (2006) Genomics and the irreducible nature of eukaryotic cells. Science 312:1011–1014

    Article  Google Scholar 

  • Lane N (2011) Energetics and genetics across the prokaryote–eukaryote divide. Biol Direct 6:35

    Article  Google Scholar 

  • Lane N (2015) The vital question. Energy, evolution and the origins of complex life. Norton, New York

    Google Scholar 

  • Lane N, Martin W (2010) The energetic of genome complexity. Nature 467:929–934

    Article  Google Scholar 

  • Levin M (2014) Endogenous bioelectrical networks store non-genetic patterning information during development and regeneration. J Physiol 592(11):2295–2305

    Article  Google Scholar 

  • Ling J, O’Donoghue P, Söll D (2015) Genetic code flexibility in microorganisms: novel mechanisms and impact on bacterial physiology. Nat Rev Microbiol 13:707–721

    Article  Google Scholar 

  • Lòpez-Garcia P, Moreira D (1999) Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci 24:88–93

    Article  Google Scholar 

  • Maraldi NM (2008) A lipid-based code in nuclear signalling. In: Barbieri M (ed) The codes of life: the rules of macroevolution. Springer, Dordrecht, pp 207–221

    Chapter  Google Scholar 

  • Margulis L (1970) Origin of eucaryotic cells. Yale University Press, New Haven

    Google Scholar 

  • Margulis L (1981) Symbiosis in cell evolution. Freeman, San Francisco

    Google Scholar 

  • Marijuán PC, Navarro J, del Moral R (2015) How the living is in the world: an inquiry into the informational choreographies of life. Prog Biophys Mol Biol 119:469–480

    Article  Google Scholar 

  • Marquard T, Pfaff SL (2001) Cracking the transcriptional code for cell specification in the neural tube. Cell 106:651–654

    Article  Google Scholar 

  • Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 342:37–41

    Article  Google Scholar 

  • Maruta H, Greer K, Rosenbaum JL (1986) The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J Cell Biol 103:571–579

    Article  Google Scholar 

  • Matlin A, Clark F, Smith C (2005) Understanding alternative splicing: towards a cellular code. Nat Rev Mol Cell Biol 6:386–398

    Article  Google Scholar 

  • Maurer-Stroh S, Dickens NJ, Hughes-Davies L et al (2003) The tudor domain “royal family”: tudor, plant agenet, chromo, PWWP and MBT domains. Trends Biochem Sci 28(2):69–74

    Article  Google Scholar 

  • Mereschowsky C (1910) Theorie der Zwei Pflanzenarten als Grundlage der Symbiogenesis, einer neuen Lehre der Entstehung der Organismen. Biologisches Zentralblatt 30:278–303, 321–347, 353–367

  • Miller RV (1998) Bacterial gene-swapping in nature. Sci Am 278:67–71

    Article  Google Scholar 

  • Mujtaba S, Zeng L, Zhou MM (2007) Structure and acetyl-lysine recognition of the bromodomain. Oncogene 26(37):5521–5527

    Article  Google Scholar 

  • Nicolelis M (2011) Beyond boundaries: the new neuroscience of connecting brains with machines and how it will change our lives. Times Books, New York

    Google Scholar 

  • Nicolelis M, Ribeiro S (2006) Seeking the neural code. Sci Am 295:70–77

    Article  Google Scholar 

  • Nudler E, Mironov AS (2004) The riboswitch control of bacterial metabolism. Trends Biochem Sci 29(1):11–17

    Article  Google Scholar 

  • O’Keefe J, Burgess N (2005) Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15:853–866

    Article  Google Scholar 

  • O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428

    Article  Google Scholar 

  • Osawa S (1995) Evolution of the genetic code. Oxford University Press, New York

    Google Scholar 

  • Owen DJ, Ornaghi P, Yang J-C et al (2000) The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase Gcn5p. EMBO J 19(22):6141–6149

    Article  Google Scholar 

  • Papoutsi M, de Zwart JA, Jansma JM et al (2009) From phonemes to articulatory codes: an fMRI study of the role of Broca’s area in speech production. Cereb Cortex 19:2156–2165

    Article  Google Scholar 

  • Pertea M, Mount SM, Salzberg SL (2007) A computational survey of candidate exonic splicing enhancer motifs in the model plant Arabidopsis thaliana. BMC Bioinform 8:159

    Article  Google Scholar 

  • Peterson CL, Laniel M-A (2004) Histones and histone modifications. Curr Biol 14:546–551

    Article  Google Scholar 

  • Pfeffer SR, Rothman JE (1987) Biosynthetic protein transport and sorting by the endoplasmic reticulum and golgi. Annu Rev Biochem 56:829–852

    Article  Google Scholar 

  • Portier P (1918) Les symbiotes. Masson et Cie, New York

    Google Scholar 

  • Raunser S, Gatsoiannis C (2015) Deciphering the tubulin code. Cell 161(5):960–961

    Article  Google Scholar 

  • Ray A, Naters WVDG, Shiraiwa T, Carlson JR (2006) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53:353–369

    Article  Google Scholar 

  • Redies C, Takeichi M (1996) Cadherine in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev Biol 180:413–423

    Article  Google Scholar 

  • Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152–155

    Article  Google Scholar 

  • Robinson A, Austen B (1987) The role of topogenic sequences in the movement of proteins through membranes. Biochem J 246:249–261

    Article  Google Scholar 

  • Salgado H, Moreno-Hagelsieb G, Smith TF, Collado-Vides J (2000) Operons in Escherichia coli: genomic analyses and predictions. Proc Natl Acad Sci USA 97(12):6652–6657

    Article  Google Scholar 

  • Schimmel P (1987) Aminoacyl tRNA synthetases: general scheme of structure-function relationship in the polypeptides and recognition of tRNAs. Ann Rev Biochem 56:125–158

    Article  Google Scholar 

  • Schimmel P, Giegé R, Moras D, Yokoyama S (1993) An operational RNA code for amino acids and possible relationship to genetic code. Proc Natl Acad Sci USA 90:8763–8768

    Article  Google Scholar 

  • Schimper AFW (1883) Uber die Entwickelung der Chlorophyllkörner und Farbkorper. Bot Ztg 41:105–114

    Google Scholar 

  • Schopf JW (1999) Cradle of life. The discovery of Earth’s earliest fossils. Princeton University Press, Princeton

    Google Scholar 

  • Schreiber SL, Bernstein BE (2002) Signaling network model of chromatin. Cell 111:771–778

    Article  Google Scholar 

  • Shannon CE (1948) A mathematical theory of communication. Bell Labs Tech J 27(3):379–423

    Article  Google Scholar 

  • Shapiro L, Colman DR (1999) The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron 23:427–430

    Article  Google Scholar 

  • Simonson AB, Servin JA, Skophammer RG et al (2005) Decoding the genomic tree of life. Proc Natl Acad Sci USA 102:6608–6613

    Article  Google Scholar 

  • Snel B, Huynen MA, Dulith BA (2005) Genome trees and the nature of genome evolution. Ann Rev Microbiol 59:191–209

    Article  Google Scholar 

  • Solis AS, Shariat N, Patton JG (2008) Splicing fidelity, enhancers, and disease. Front Biosci 13:1926–1942

    Article  Google Scholar 

  • Stergachis AB, Haugen E, Shafer A et al (2013) Exonic transcription factor binding directs codon choice and affects protein evolution. Science 342:1367–1372

    Article  Google Scholar 

  • Strahl BD, Allis D (2000) The language of covalent histone modifications. Nature 403:41–45

    Article  Google Scholar 

  • Szabo GG, Soltesz I (2015) Pass-through code of synaptic integration. Neuron 87:1124–1126

    Article  Google Scholar 

  • Tavares EQP, Buckeridge MS (2015) Do plant cells have a code? Plant Sci 241:286–294

    Article  Google Scholar 

  • Tazi J, Bakkour N, Stamm S (2009) Alternative splicing and disease. Biochim Biophys Acta 1792:14–26

    Article  Google Scholar 

  • Trifonov EN (1989) The multiple codes of nucleotide sequences. Bull Math Biol 51:417–432

    Article  Google Scholar 

  • Trifonov EN (1996) Interfering contexts of regulatory sequence elements. Cabios 12:423–429

    Google Scholar 

  • Trifonov EN (1999) Elucidating sequence codes: three codes for evolution. Ann N Y Acad Sci 870:330–338

    Article  Google Scholar 

  • Tseng AS, Levin M (2013) Cracking the bioelectric code. Probing endogenous ionic controls of pattern formation. Commun Integr Biol 6(1):1–8

    Article  Google Scholar 

  • Tucker BJ, Breaker RR (2005) Riboswitches as versatile gene control elements. Curr Opin Struct Biol 15(3):342–348

    Article  Google Scholar 

  • Turner BM (2000) Histone acetylation and an epigenetic code. BioEssays 22:836–845

    Article  Google Scholar 

  • Turner BM (2002) Cellular memory and the histone code. Cell 111:285–291

    Article  Google Scholar 

  • Turner BM (2007) Defining an epigenetic code. Nat Cell Biol 9:2–6

    Article  Google Scholar 

  • Verhey KJ, Gaertig J (2007) The tubulin vode. Cell Cycle 6(17):2152–2160

    Article  Google Scholar 

  • Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2004) Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet 20(1):44–50

    Article  Google Scholar 

  • Wallin JE (1927) Symbionticism and the origin of species. Williams and Wilkins, Baltimore

    Book  Google Scholar 

  • Wang Z, Burge C (2008) Splicing regulation: from a part list of regulatory elements to an integrated splicing code. RNA 14:802–813

    Article  Google Scholar 

  • Wang GS, Cooper TA (2007) Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 8:749–761

    Article  Google Scholar 

  • Weatheritt RJ, Babu MM (2013) The hidden codes that shape protein evolution. Science 342:1325–1326

    Article  Google Scholar 

  • Webster DR, Wehland J, Weber K, Borisy GG (1990) Detyrosination of alpha tubulin does not stabilize microtubules in vivo. J Cell Biol 111:113–122

    Article  Google Scholar 

  • Woese CR (1965) Order in the genetic code. Proc Natl Acad Sci USA 54:71–75

    Article  Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Google Scholar 

  • Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97:8392–8396

    Article  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Article  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eukarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  Google Scholar 

  • Wolfe AP, Hayes JJ (1999) Chromatin disruption and modification. Nucleic Acid Res 27:711–720

    Article  Google Scholar 

  • Wu J, Grunstein M (2000) 25 years after the nucleosome model: chromatin modifications. Trends Biochem Sci 25(12):619–623

    Article  Google Scholar 

  • Yang D, Oyaizu Y, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:443–447

    Google Scholar 

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I am grateful to Salthe and to two anonymous reviewers whose suggestions greatly improved the first version of this manuscript.

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Barbieri, M. How Did the Eukaryotes Evolve?. Biol Theory 12, 13–26 (2017). https://doi.org/10.1007/s13752-016-0253-3

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