Skip to main content
Log in

The Promise and Peril of Continuous In Vitro Evolution

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Experimental evolution methods can be used to address and illuminate issues central to the understanding of evolutionary theory. One of the most powerful of these methods involves the in vitro evolution of nucleic acid enzymes, taking advantage of the direct relationship between the genotype of a nucleic acid sequence and the phenotype of its associated catalytic function. This review and commentary focuses on the past, present, and future potential of systems for the continuous in vitro evolution of nucleic acid enzymes as tools for modeling evolutionary processes in biology. It offers a candid appraisal of both the strengths and the limitations of these systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • DP Bartel JW Szostak (1993) ArticleTitleIsolation of new ribozymes from a large pool of random sequences Science 261 1411–1418 Occurrence Handle7690155

    PubMed  Google Scholar 

  • AA Beaudry GF Joyce (1992) ArticleTitleDirected evolution of an RNA enzyme Science 257 635–641 Occurrence Handle1496376

    PubMed  Google Scholar 

  • NH Bergman WK Johnston DP Bartel (2000) ArticleTitleKinetic framework for ligation by an efficient RNA ligase ribozyme Biochemistry 39 3115–3123 Occurrence Handle10.1021/bi992654u Occurrence Handle10715133

    Article  PubMed  Google Scholar 

  • RR Breaker GF Joyce (1994) ArticleTitleEmergence of a replicating species from an in vitro RNA evolution reaction Proc Natl Acad Sci USA 91 6093–6097 Occurrence Handle7517040

    PubMed  Google Scholar 

  • JJ Bull CM Pease (1995) ArticleTitleWhy is the polymerase chain reaction resistant to in vitro evolution J Mol Evol 41 1160–1164 Occurrence Handle10.1007/BF00173197

    Article  Google Scholar 

  • J Compton (1991) ArticleTitleNucleic acid sequence-based amplification Nature 350 91–92 Occurrence Handle10.1038/350091a0 Occurrence Handle1706072

    Article  PubMed  Google Scholar 

  • M Eigen (1971) ArticleTitleSelforganization of matter and the evolution of biological macromolecules Naturwissenschaften 58 465–523 Occurrence Handle10.1007/BF00623322 Occurrence Handle4942363

    Article  PubMed  Google Scholar 

  • EH Ekland JW Szostak DP Bartel (1995) ArticleTitleStructurally complex and highly active RNA ligases derived from random RNA sequences Science 269 364–370 Occurrence Handle7618102

    PubMed  Google Scholar 

  • T Ellinger R Ehricht JS McCaskill (1998) ArticleTitleIn vitro evolution of molecular cooperation in CATCH, a cooperatively coupled amplification system Chem Biol 5 729–741 Occurrence Handle10.1016/S1074-5521(98)90665-2 Occurrence Handle9862794

    Article  PubMed  Google Scholar 

  • SJ Gould ES Vrba (1982) ArticleTitleExaptation—A missing term in the science of form Paleobiology 8 4–15

    Google Scholar 

  • JC Guatelli KM Whitfield DY Kwoh KJ Barringer DD Richman TR Gingeras (1990) ArticleTitleIsothermal, in vitro amplification of nucleic acids by a multienzyme reaction modeled after retroviral replication Proc Natl Acad Sci USA 87 1874–1878 Occurrence Handle2308948

    PubMed  Google Scholar 

  • MM Hanczyc RL Dorit (2000) ArticleTitleReplicability and recurrence in the experimental evolution of a group I ribozyme Mol Biol Evol 17 1050–1060 Occurrence Handle10889218

    PubMed  Google Scholar 

  • Hill CS (1996) Gen-Probe transcription mediated amplification: system principles. Gen-Probe Inc. technical document. Available at: http://www.gen-probe.com/pdfs/tma_whiteppr.pdf

  • D Imburgio M Rong K Ma WT McAllister (2000) ArticleTitleStudies of promoter recognition and start site selection by T7 RNA polymerase using a comprehensive collection of promoter variants Biochemistry 39 10419–10430 Occurrence Handle10.1021/bi000365w Occurrence Handle10956032

    Article  PubMed  Google Scholar 

  • GF Joyce (2004) ArticleTitleDirected evolution of nucleic acid enzymes Annu Rev Biochem 73 791–836 Occurrence Handle10.1146/annurev.biochem.73.011303.073717 Occurrence Handle15189159

    Article  PubMed  Google Scholar 

  • H Kühne GF Joyce (2003) ArticleTitleContinuous in vitro evolution of ribozymes that operate under conditions of extreme pH J Mol Evol 57 1–7 Occurrence Handle10.1007/s00239-002-2434-x Occurrence Handle12962301

    Article  PubMed  Google Scholar 

  • N Lehman (2004) ArticleTitleAssessing the likelihood of recurrence during RNA evolution in vitro Artif Life 10 1–22 Occurrence Handle10.1162/106454604322875887 Occurrence Handle15035860

    Article  PubMed  Google Scholar 

  • R Levisohn S Spiegelman (1969) ArticleTitleFurther extracellular Darwinian experiments with replicating RNA molecules; diverse variants isolated under different selective conditions Proc Natl Acad Sci USA 63 805–811 Occurrence Handle5259764

    PubMed  Google Scholar 

  • KE McGinness MC Wright GF Joyce (2002) ArticleTitleContinuous in vitro evolution of a ribozyme that catalyzes three successive nucleotidyl addition reactions Chem Biol 9 585–596 Occurrence Handle10.1016/S1074-5521(02)00136-9 Occurrence Handle12031665

    Article  PubMed  Google Scholar 

  • DR Mills RL Peterson S Spiegelman (1967) ArticleTitleAn extracellular Darwinian experiment with a self-duplicating nucleic acid molecule Proc Natl Acad Sci USA 58 217–224 Occurrence Handle5231602

    PubMed  Google Scholar 

  • M Mörl I Niemer C Schmeizer (1992) ArticleTitleNew reactions catalyzed by a group II intron ribozyme with RNA and DNA substrates Cell 70 803–810 Occurrence Handle10.1016/0092-8674(92)90313-2 Occurrence Handle1381286

    Article  PubMed  Google Scholar 

  • KB Mullis FA Faloona (1987) ArticleTitleSpecific synthesis of DNA in vitro via a polymerase catalyzed chain reaction Methods Enzymol 155 335–350 Occurrence Handle3431465

    PubMed  Google Scholar 

  • P Ordoukhanian OF Joyce (1999) ArticleTitleA molecular description of the evolution of resistance Chem Biol 6 881–889 Occurrence Handle10.1016/S1074-5521(00)80007-1 Occurrence Handle10631516

    Article  PubMed  Google Scholar 

  • R Saffhill H Schneider-Bernloehr LE Orgel (1970) ArticleTitleIn vitro selection of bacteriophage Qβ ribonucleic acid variants resistant to ethidium bromide J Mol Biol 51 531–539 Occurrence Handle10.1016/0022-2836(70)90006-9 Occurrence Handle5492605

    Article  PubMed  Google Scholar 

  • RK Saiki S Scharf F Faloona KB Mullis GT Horn HA Erlich N Arnheim (1985) ArticleTitleEnzymatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia Science 230 1350––1354

    Google Scholar 

  • T Schmitt N Lehman (1999) ArticleTitleNon-unity in molecular heritability demonstrated by continuous evolution in vitro Chem Biol 6 857–869 Occurrence Handle10.1016/S1074-5521(00)80005-8 Occurrence Handle10631514

    Article  PubMed  Google Scholar 

  • DS Tawfik AD Griffiths (1998) ArticleTitleMan-made cell-like compartments for molecular evolution Nature Biotechnol 16 652–656 Occurrence Handle10.1038/nbt0798-652

    Article  Google Scholar 

  • B Wlotzka JS McCaskill (1997) ArticleTitleA molecular predator and its prey: coupled isothermal amplification of nucleic acids Chem Biol 4 25–33 Occurrence Handle10.1016/S1074-5521(97)90234-9 Occurrence Handle9070425

    Article  PubMed  Google Scholar 

  • MC Wright GF Joyce (1997) ArticleTitleContinuous in vitro evolution of catalytic function Science 276 614–617 Occurrence Handle10.1126/science.276.5312.614 Occurrence Handle9110984

    Article  PubMed  Google Scholar 

  • S Wright (1931) ArticleTitleEvolution in Mendelian populations Genetics 16 97–159

    Google Scholar 

  • S Wright (1932) ArticleTitleThe roles of mutation, inbreeding, crossbreeding, and selection in evolution Proc 6th Int Congr Genet 1 356–366

    Google Scholar 

  • S Wright (1982) ArticleTitleThe shifting balance theory and macroevolution Annu Rev Genet 16 1–19 Occurrence Handle10.1146/annurev.ge.16.120182.000245 Occurrence Handle6760797

    Article  PubMed  Google Scholar 

Download references

Acknowledgment

This work was supported by Grant NAG5-9386 from the National Aeronautics and Space Administration and The Skaggs Institute for Chemical Biology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerald F. Joyce.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johns, G.C., Joyce, G.F. The Promise and Peril of Continuous In Vitro Evolution. J Mol Evol 61, 253–263 (2005). https://doi.org/10.1007/s00239-004-0307-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-0307-1

Keywords

Navigation