1932

Abstract

DNA synthesis technology has progressed to the point that it is now practical to synthesize entire genomes. Quite a variety of methods have been developed, first to synthesize single genes but ultimately to massively edit or write from scratch entire genomes. Synthetic genomes can essentially be clones of native sequences, but this approach does not teach us much new biology. The ability to endow genomes with novel properties offers special promise for addressing questions not easily approachable with conventional gene-at-a-time methods. These include questions about evolution and about how genomes are fundamentally wired informationally, metabolically, and genetically. The techniques and technologies relating to how to design, build, and deliver big DNA at the genome scale are reviewed here. A fuller understanding of these principles may someday lead to the ability to truly design genomes from scratch.

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2020-06-20
2024-12-05
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Literature Cited

  1. 1. 
    Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J et al. 2018. Earth BioGenome Project: sequencing life for the future of life. PNAS 115:174325–33
    [Google Scholar]
  2. 2. 
    Agarwal KL, Büchi H, Caruthers MH, Gupta N, Khorana HG et al. 1970. Total synthesis of the gene for an alanine transfer ribonucleic acid from yeast. Nature 227:525327–34
    [Google Scholar]
  3. 3. 
    Cello J, Paul AV, Wimmer E 2002. Chemical synthesis of poliovirus cDNA: generation of infectious virus in the absence of natural template. Science 297:55831016–18
    [Google Scholar]
  4. 4. 
    Gibson DG, Benders GA, Andrews-Pfannkoch C, Denisova EA, Baden-Tillson H et al. 2008. Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science 319:58671215–20
    [Google Scholar]
  5. 5. 
    Smith HO, Hutchison CA, Pfannkoch C, Venter JC 2003. Generating a synthetic genome by whole genome assembly: φX174 bacteriophage from synthetic oligonucleotides. PNAS 100:2615440–45
    [Google Scholar]
  6. 6. 
    Sanger F, Coulson AR, Friedmann T, Air GM, Barrell BG et al. 1978. The nucleotide sequence of bacteriophage φX174. J. Mol. Biol. 125:2225–46
    [Google Scholar]
  7. 7. 
    Chan LY, Kosuri S, Endy D 2005. Refactoring bacteriophage T7. Mol. Syst. Biol. 1:2005.0018
    [Google Scholar]
  8. 8. 
    Temme K, Zhao D, Voigt CA 2012. Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. PNAS 109:187085–90
    [Google Scholar]
  9. 9. 
    Ren H, Biswas S, Ho S, van der Donk WA, Zhao H 2018. Rapid discovery of glycocins through pathway refactoring in Escherichia coli. ACS Chem. Biol 13:102966–72
    [Google Scholar]
  10. 10. 
    Chao L, Vargas C, Spear BB, Cox EC 1983. Transposable elements as mutator genes in evolution. Nature 303:5918633–35
    [Google Scholar]
  11. 11. 
    Yu BJ, Sung BH, Koob MD, Lee CH, Lee JH et al. 2002. Minimization of the Escherichia coli genome using a Tn5-targeted Cre/loxP excision system. Nat. Biotechnol. 20:1018–23
    [Google Scholar]
  12. 12. 
    Kolisnychenko V, Plunkett G, Herring CD, Fehér T, Pósfai J et al. 2002. Engineering a reduced Escherichia coli genome. Genome Res 12:4640–47
    [Google Scholar]
  13. 13. 
    Pósfai G, Plunkett G, Fehér T, Frisch D, Keil GM et al. 2006. Emergent properties of reduced-genome Escherichia coli. Science 312:57761044–46
    [Google Scholar]
  14. 14. 
    Hashimoto M, Ichimura T, Mizoguchi H, Tanaka K, Fujimitsu K et al. 2005. Cell size and nucleoid organization of engineered Escherichia coli cells with a reduced genome. Mol. Microbiol. 55:1137–49
    [Google Scholar]
  15. 15. 
    Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V et al. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:53311453–62
    [Google Scholar]
  16. 16. 
    Richardson SM, Mitchell LA, Stracquadanio G, Yang K, Dymond JS et al. 2017. Design of a synthetic yeast genome. Science 355:63291040–44
    [Google Scholar]
  17. 17. 
    Dymond J, Boeke J. 2012. The Saccharomyces cerevisiae SCRaMbLE system and genome minimization. Bioengineered 3:3168–71
    [Google Scholar]
  18. 18. 
    Hutchison CA, Peterson SN, Gill SR, Cline RT, White O et al. 1999. Global transposon mutagenesis and a minimal mycoplasma genome. Science 286:54472165–69
    [Google Scholar]
  19. 19. 
    Ross-Macdonald P, Coelho PSR, Roemer T, Agarwal S, Kumar A et al. 1999. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402:6760413–18
    [Google Scholar]
  20. 20. 
    Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008
    [Google Scholar]
  21. 21. 
    Giaever G, Chu AM, Ni L, Connelly C, Riles L et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:6896387–91
    [Google Scholar]
  22. 22. 
    Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E et al. 2003. Comprehensive transposon mutant library of Pseudomonas aeruginosa. PNAS 100:2414339–44
    [Google Scholar]
  23. 23. 
    Christen B, Abeliuk E, Collier JM, Kalogeraki VS, Passarelli B et al. 2011. The essential genome of a bacterium. Mol. Syst. Biol. 7:528
    [Google Scholar]
  24. 24. 
    Mitchell LA, Wang A, Stracquadanio G, Kuang Z, Wang X et al. 2017. Synthesis, debugging, and effects of synthetic chromosome consolidation: synVI and beyond. Science 355:6329eaaf4831
    [Google Scholar]
  25. 25. 
    Lajoie MJ, Kosuri S, Mosberg JA, Gregg CJ, Zhang D, Church GM 2013. Probing the limits of genetic recoding in essential genes. Science 342:6156361–63
    [Google Scholar]
  26. 26. 
    Wu Y, Li B-Z, Zhao M, Mitchell LA, Xie Z-X et al. 2017. Bug mapping and fitness testing of chemically synthesized chromosome X. Science 355:6329eaaf4706
    [Google Scholar]
  27. 27. 
    Plotkin JB, Kudla G. 2011. Synonymous but not the same: the causes and consequences of codon bias. Nat. Rev. Genet. 12:132–42
    [Google Scholar]
  28. 28. 
    Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y et al. 2010. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141:2344–54
    [Google Scholar]
  29. 29. 
    Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:5924218–23
    [Google Scholar]
  30. 30. 
    Hoshika S, Leal NA, Kim M-J, Kim M-S, Karalkar NB et al. 2019. Hachimoji DNA and RNA: a genetic system with eight building blocks. Science 363:6429884–87
    [Google Scholar]
  31. 31. 
    Biondi E, Benner SA. 2018. Artificially expanded genetic information systems for new aptamer technologies. Biomedicines 6:253
    [Google Scholar]
  32. 32. 
    Yaren O, Alto BW, Gangodkar PV, Ranade SR, Patil KN et al. 2017. Point of sampling detection of Zika virus within a multiplexed kit capable of detecting dengue and chikungunya. BMC Infect. Dis. 17:1293
    [Google Scholar]
  33. 33. 
    Zhang Y, Ptacin JL, Fischer EC, Aerni HR, Caffaro CE et al. 2017. A semi-synthetic organism that stores and retrieves increased genetic information. Nature 551:7682644–47
    [Google Scholar]
  34. 34. 
    Michelson AM, Todd AR. 1955. Nucleotides part XXXII. Synthesis of a dithymidine dinucleotide containing a 3′:5′-internucleotidic linkage. J. Chem. Soc. Resumed 1955:2632–38
    [Google Scholar]
  35. 35. 
    Beaucage SL, Caruthers MH. 1981. Deoxynucleoside phosphoramidites—a new class of key intermediates for deoxypolynucleotide synthesis. Tetrahedron Lett 22:201859–62
    [Google Scholar]
  36. 36. 
    Fodor SP, Read JL, Pirrung MC, Stryer L, Lu AT, Solas D 1991. Light-directed, spatially addressable parallel chemical synthesis. Science 251:4995767–73
    [Google Scholar]
  37. 37. 
    LeProust EM, Peck BJ, Spirin K, McCuen HB, Moore B et al. 2010. Synthesis of high-quality libraries of long (150mer) oligonucleotides by a novel depurination controlled process. Nucleic Acids Res 38:82522–40
    [Google Scholar]
  38. 38. 
    Kosuri S, Church GM. 2014. Large-scale de novo DNA synthesis: technologies and applications. Nat. Methods 11:5499–507
    [Google Scholar]
  39. 39. 
    Hughes RA, Ellington AD. 2017. Synthetic DNA synthesis and assembly: putting the synthetic in synthetic biology. Cold Spring Harb. Perspect. Biol. 9:1a023812
    [Google Scholar]
  40. 40. 
    Motea EA, Berdis AJ. 2010. Terminal deoxynucleotidyl transferase: the story of a misguided DNA polymerase. Biochim. Biophys. Acta Proteins Proteom. 1804:51151–66
    [Google Scholar]
  41. 41. 
    Bollum FJ. 1960. Calf thymus polymerase. J. Biol. Chem. 235:82399–403
    [Google Scholar]
  42. 42. 
    Bollum FJ. 1962. Oligodeoxyribonucleotide-primed reactions catalyzed by calf thymus polymerase. J. Biol. Chem. 237:1945–49
    [Google Scholar]
  43. 43. 
    Tjong V, Yu H, Hucknall A, Rangarajan S, Chilkoti A 2011. Amplified on-chip fluorescence detection of DNA hybridization by surface-initiated enzymatic polymerization. Anal. Chem. 83:135153–59
    [Google Scholar]
  44. 44. 
    Tauraitė D, Jakubovska J, Dabužinskaitė J, Bratchikov M, Meškys R 2017. Modified nucleotides as substrates of terminal deoxynucleotidyl transferase. Molecules 22:4672
    [Google Scholar]
  45. 45. 
    Kuwahara M, Obika S, Takeshima H, Hagiwara Y, Nagashima J et al. 2009. Smart conferring of nuclease resistance to DNA by 3′-end protection using 2′,4′-bridged nucleoside-5′-triphosphates. Bioorg. Med. Chem. Lett. 19:112941–43
    [Google Scholar]
  46. 46. 
    Stemmer WPC, Crameri A, Ha KD, Brennan TM, Heyneker HL 1995. Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides. Gene 164:149–53
    [Google Scholar]
  47. 47. 
    Xiong A-S, Peng R-H, Zhuang J, Liu J-G, Gao F et al. 2008. Non-polymerase-cycling-assembly-based chemical gene synthesis: strategies, methods, and progress. Biotechnol. Adv. 26:2121–34
    [Google Scholar]
  48. 48. 
    Gibson DG. 2009. Synthesis of DNA fragments in yeast by one-step assembly of overlapping oligonucleotides. Nucleic Acids Res 37:206984–90
    [Google Scholar]
  49. 49. 
    Dymond JS, Scheifele LZ, Richardson S, Lee P, Chandrasegaran S et al. 2009. Teaching synthetic biology, bioinformatics and engineering to undergraduates: the interdisciplinary Build-a-Genome course. Genetics 181:113–21
    [Google Scholar]
  50. 50. 
    Xie Z-X, Li B-Z, Mitchell LA, Wu Y, Qi X et al. 2017. “Perfect” designer chromosome V and behavior of a ring derivative. Science 355:6329eaaf4704
    [Google Scholar]
  51. 51. 
    Knight T. 2003. Idempotent vector design for standard assembly of biobricks Rep., MIT Synth. Biol. Work. Group Cambridge, MA: http://hdl.handle.net/1721.1/21168
    [Google Scholar]
  52. 52. 
    Shetty RP, Endy D, Knight TF 2008. Engineering BioBrick vectors from BioBrick parts. J. Biol. Eng. 2:5
    [Google Scholar]
  53. 53. 
    Anderson JC, Dueber JE, Leguia M, Wu GC, Goler JA et al. 2010. BglBricks: a flexible standard for biological part assembly. J. Biol. Eng. 4:1
    [Google Scholar]
  54. 54. 
    Engler C, Kandzia R, Marillonnet S 2008. A one pot, one step, precision cloning method with high throughput capability. PLOS ONE 3:11e3647
    [Google Scholar]
  55. 55. 
    Engler C, Gruetzner R, Kandzia R, Marillonnet S 2009. Golden Gate shuffling: a one-pot DNA shuffling method based on type IIs restriction enzymes. PLOS ONE 4:5e5553
    [Google Scholar]
  56. 56. 
    Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S 2011. A modular cloning system for standardized assembly of multigene constructs. PLOS ONE 6:2e16765
    [Google Scholar]
  57. 57. 
    Agmon N, Mitchell LA, Cai Y, Ikushima S, Chuang J et al. 2015. Yeast Golden Gate (yGG) for the efficient assembly of S. cerevisiae transcription units. ACS Synth. Biol. 4:7853–59
    [Google Scholar]
  58. 58. 
    Guo Y, Dong J, Zhou T, Auxillos J, Li T et al. 2015. YeastFab: the design and construction of standard biological parts for metabolic engineering in Saccharomyces cerevisiae. Nucleic Acids Res 43:13e88
    [Google Scholar]
  59. 59. 
    Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6:5343–45
    [Google Scholar]
  60. 60. 
    Mitchell LA, Cai Y, Taylor M, Noronha AM, Chuang J et al. 2013. Multichange isothermal mutagenesis: a new strategy for multiple site-directed mutations in plasmid DNA. ACS Synth. Biol. 2:8473–77
    [Google Scholar]
  61. 61. 
    Hinnen A, Hicks JB, Fink GR 1978. Transformation of yeast. PNAS 75:41929–33
    [Google Scholar]
  62. 62. 
    Winston F, Chumley F, Fink GR 1983. Eviction and transplacement of mutant genes in yeast. Methods Enzymol 101:211–28
    [Google Scholar]
  63. 63. 
    Orr-Weaver TL, Szostak JW, Rothstein RJ 1981. Yeast transformation: a model system for the study of recombination. PNAS 78:106354–58
    [Google Scholar]
  64. 64. 
    Larionov V, Kouprina N, Graves J, Chen XN, Korenberg JR, Resnick MA 1996. Specific cloning of human DNA as yeast artificial chromosomes by transformation-associated recombination. PNAS 93:1491–96
    [Google Scholar]
  65. 65. 
    Larionov V, Kouprina N, Solomon G, Barrett JC, Resnick MA 1997. Direct isolation of human BRCA2 gene by transformation-associated recombination in yeast. PNAS 94:147384–87
    [Google Scholar]
  66. 66. 
    Kouprina N, Annab L, Graves J, Afshari C, Barrett JC et al. 1998. Functional copies of a human gene can be directly isolated by transformation-associated recombination cloning with a small 3′ end target sequence. PNAS 95:84469–74
    [Google Scholar]
  67. 67. 
    Gibson DG, Benders GA, Axelrod KC, Zaveri J, Algire MA et al. 2008. One-step assembly in yeast of 25 overlapping DNA fragments to form a complete synthetic Mycoplasma genitalium genome. PNAS 105:5120404–9
    [Google Scholar]
  68. 68. 
    Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang R-Y et al. 2010. Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329:598752–56
    [Google Scholar]
  69. 69. 
    Mitchell LA, Chuang J, Agmon N, Khunsriraksakul C, Phillips NA et al. 2015. Versatile genetic assembly system (VEGAS) to assemble pathways for expression in S. cerevisiae. Nucleic Acids Res 43:136620–30
    [Google Scholar]
  70. 70. 
    Lin Q, Jia B, Mitchell LA, Luo J, Yang K et al. 2015. RADOM, an efficient in vivo method for assembling designed DNA fragments up to 10 kb long in Saccharomyces cerevisiae. ACS Synth. Biol 4:3213–20
    [Google Scholar]
  71. 71. 
    Annaluru N, Muller H, Mitchell LA, Ramalingam S, Stracquadanio G et al. 2014. Total synthesis of a functional designer eukaryotic chromosome. Science 344:617955–58
    [Google Scholar]
  72. 72. 
    Muller H, Annaluru N, Schwerzmann JW, Richardson SM, Dymond JS et al. 2012. Assembling large DNA segments in yeast. Methods Mol. Biol. 852:133–50
    [Google Scholar]
  73. 73. 
    Itaya M, Tsuge K, Koizumi M, Fujita K 2005. Combining two genomes in one cell: stable cloning of the Synechocystis PCC6803 genome in the Bacillus subtilis 168 genome. PNAS 102:4415971–76
    [Google Scholar]
  74. 74. 
    Itaya M, Fujita K, Kuroki A, Tsuge K 2008. Bottom-up genome assembly using the Bacillus subtilis genome vector. Nat. Methods 5:141–43
    [Google Scholar]
  75. 75. 
    Benders GA, Noskov VN, Denisova EA, Lartigue C, Gibson DG et al. 2010. Cloning whole bacterial genomes in yeast. Nucleic Acids Res 38:82558–69
    [Google Scholar]
  76. 76. 
    Venetz JE, Medico LD, Wölfle A, Schächle P, Bucher Y et al. 2019. Chemical synthesis rewriting of a bacterial genome to achieve design flexibility and biological functionality. PNAS 116:168070–79
    [Google Scholar]
  77. 77. 
    Fredens J, Wang K, de la Torre D, Funke LFH, Robertson WE et al. 2019. Total synthesis of Escherichia coli with a recoded genome. Nature 569:7757514–18
    [Google Scholar]
  78. 78. 
    Shen Y, Wang Y, Chen T, Gao F, Gong J et al. 2017. Deep functional analysis of synII, a 770-kilobase synthetic yeast chromosome. Science 355:6329eaaf4791
    [Google Scholar]
  79. 79. 
    Zhang W, Zhao G, Luo Z, Lin Y, Wang L et al. 2017. Engineering the ribosomal DNA in a megabase synthetic chromosome. Science 355:6329eaaf3981
    [Google Scholar]
  80. 80. 
    Karas BJ, Molparia B, Jablanovic J, Hermann WJ, Lin Y-C et al. 2013. Assembly of eukaryotic algal chromosomes in yeast. J. Biol. Eng. 7:30
    [Google Scholar]
  81. 81. 
    Lartigue C, Glass JI, Alperovich N, Pieper R, Parmar PP et al. 2007. Genome transplantation in bacteria: changing one species to another. Science 317:5838632–38
    [Google Scholar]
  82. 82. 
    Labroussaa F, Lebaudy A, Baby V, Gourgues G, Matteau D et al. 2016. Impact of donor-recipient phylogenetic distance on bacterial genome transplantation. Nucleic Acids Res 44:178501–11
    [Google Scholar]
  83. 83. 
    Baby V, Labroussaa F, Brodeur J, Matteau D, Gourgues G et al. 2018. Cloning and transplantation of the Mesoplasma florum genome. ACS Synth. Biol. 7:1209–17
    [Google Scholar]
  84. 84. 
    Lartigue C, Vashee S, Algire MA, Chuang R-Y, Benders GA et al. 2009. Creating bacterial strains from genomes that have been cloned and engineered in yeast. Science 325:59481693–96
    [Google Scholar]
  85. 85. 
    Karas BJ, Jablanovic J, Sun L, Ma L, Goldgof GM et al. 2013. Direct transfer of whole genomes from bacteria to yeast. Nat. Methods 10:5410–12
    [Google Scholar]
  86. 86. 
    Brown DM, Chan YA, Desai PJ, Grzesik P, Oldfield LM et al. 2017. Efficient size-independent chromosome delivery from yeast to cultured cell lines. Nucleic Acids Res 45:7e50
    [Google Scholar]
  87. 87. 
    Kazuki Y, Oshimura M. 2011. Human artificial chromosomes for gene delivery and the development of animal models. Mol. Ther. 19:91591–601
    [Google Scholar]
  88. 88. 
    Takiguchi M, Kazuki Y, Hiramatsu K, Abe S, Iida Y et al. 2014. A novel and stable mouse artificial chromosome vector. ACS Synth. Biol. 3:12903–14
    [Google Scholar]
  89. 89. 
    Shizuya H, Kouros-Mehr H. 2001. The development and applications of the bacterial artificial chromosome cloning system. Keio J. Med. 50:126–30
    [Google Scholar]
  90. 90. 
    Fournier RE, Ruddle FH. 1977. Microcell-mediated transfer of murine chromosomes into mouse, Chinese hamster, and human somatic cells. PNAS 74:1319–23
    [Google Scholar]
  91. 91. 
    Iida Y, Kim J-H, Kazuki Y, Hoshiya H, Takiguchi M et al. 2010. Human artificial chromosome with a conditional centromere for gene delivery and gene expression. DNA Res 17:5293–301
    [Google Scholar]
  92. 92. 
    Oshimura M, Uno N, Kazuki Y, Katoh M, Inoue T 2015. A pathway from chromosome transfer to engineering resulting in human and mouse artificial chromosomes for a variety of applications to bio-medical challenges. Chromosome Res 23:1111–33
    [Google Scholar]
  93. 93. 
    Lau YH, Stirling F, Kuo J, Karrenbelt MAP, Chan YA et al. 2017. Large-scale recoding of a bacterial genome by iterative recombineering of synthetic DNA. Nucleic Acids Res 45:116971–80
    [Google Scholar]
  94. 94. 
    Wang K, Fredens J, Brunner SF, Kim SH, Chia T, Chin JW 2016. Defining synonymous codon compression schemes by genome recoding. Nature 539:762759–64
    [Google Scholar]
  95. 95. 
    Hutchison CA, Chuang R-Y, Noskov VN, Assad-Garcia N, Deerinck TJ et al. 2016. Design and synthesis of a minimal bacterial genome. Science 351:6280aad6253
    [Google Scholar]
  96. 96. 
    Rouet P, Smih F, Jasin M 1994. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. PNAS 91:136064–68
    [Google Scholar]
  97. 97. 
    Smih F, Rouet P, Romanienko PJ, Jasin M 1995. Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res 23:245012–19
    [Google Scholar]
  98. 98. 
    Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J et al. 2001. Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol. Cell. Biol. 21:1289–97
    [Google Scholar]
  99. 99. 
    Bibikova M, Golic M, Golic KG, Carroll D 2002. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics 161:31169–75
    [Google Scholar]
  100. 100. 
    Carroll D. 2014. Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83:409–39
    [Google Scholar]
  101. 101. 
    Chari R, Church GM. 2017. Beyond editing to writing large genomes. Nat. Rev. Genet. 18:12749–60
    [Google Scholar]
  102. 102. 
    Shao Y, Lu N, Wu Z, Cai C, Wang S et al. 2018. Creating a functional single-chromosome yeast. Nature 560:7718331–35
    [Google Scholar]
  103. 103. 
    Luo J, Sun X, Cormack BP, Boeke JD 2018. Karyotype engineering by chromosome fusion leads to reproductive isolation in yeast. Nature 560:7718392–96
    [Google Scholar]
  104. 104. 
    Wang T, Wei JJ, Sabatini DM, Lander ES 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343:616680–84
    [Google Scholar]
  105. 105. 
    Joung J, Engreitz JM, Konermann S, Abudayyeh OO, Verdine VK et al. 2017. Genome-scale activation screen identifies a lncRNA locus regulating a gene neighbourhood. Nature 548:7667343–46
    [Google Scholar]
  106. 106. 
    Fulco CP, Munschauer M, Anyoha R, Munson G, Grossman SR et al. 2016. Systematic mapping of functional enhancer-promoter connections with CRISPR interference. Science 354:6313769–73
    [Google Scholar]
  107. 107. 
    Yang L, Güell M, Niu D, George H, Lesha E et al. 2015. Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350:62641101–4
    [Google Scholar]
  108. 108. 
    Ellis HM, Yu D, DiTizio T, Court DL 2001. High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. PNAS 98:126742–46
    [Google Scholar]
  109. 109. 
    Wang HH, Isaacs FJ, Carr PA, Sun ZZ, Xu G et al. 2009. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:7257894–98
    [Google Scholar]
  110. 110. 
    Wang HH, Kim H, Cong L, Jeong J, Bang D, Church GM 2012. Genome-scale promoter engineering by co-selection MAGE. Nat. Methods 9:6591–93
    [Google Scholar]
  111. 111. 
    Carr PA, Wang HH, Sterling B, Isaacs FJ, Lajoie MJ et al. 2012. Enhanced multiplex genome engineering through co-operative oligonucleotide co-selection. Nucleic Acids Res 40:17e132
    [Google Scholar]
  112. 112. 
    Gregg CJ, Lajoie MJ, Napolitano MG, Mosberg JA, Goodman DB et al. 2014. Rational optimization of tolC as a powerful dual selectable marker for genome engineering. Nucleic Acids Res 42:74779–90
    [Google Scholar]
  113. 113. 
    Napolitano MG, Landon M, Gregg CJ, Lajoie MJ, Govindarajan L et al. 2016. Emergent rules for codon choice elucidated by editing rare arginine codons in Escherichia coli. PNAS 113:38E5588–97
    [Google Scholar]
  114. 114. 
    DiCarlo JE, Conley AJ, Penttilä M, Jäntti J, Wang HH, Church GM 2013. Yeast oligo-mediated genome engineering (YOGE). ACS Synth. Biol. 2:12741–49
    [Google Scholar]
  115. 115. 
    Barbieri EM, Muir P, Akhuetie-Oni BO, Yellman CM, Isaacs FJ 2017. Precise editing at DNA replication forks enables multiplex genome engineering in eukaryotes. Cell 171:61453–67
    [Google Scholar]
  116. 116. 
    Isaacs FJ, Carr PA, Wang HH, Lajoie MJ, Sterling B et al. 2011. Precise manipulation of chromosomes in vivo enables genome-wide codon replacement. Science 333:6040348–53
    [Google Scholar]
  117. 117. 
    Wannier TM, Kunjapur AM, Rice DP, McDonald MJ, Desai MM, Church GM 2018. Adaptive evolution of genomically recoded Escherichia coli. PNAS 115:123090–95
    [Google Scholar]
  118. 118. 
    Lajoie MJ, Rovner AJ, Goodman DB, Aerni H-R, Haimovich AD et al. 2013. Genomically recoded organisms expand biological functions. Science 342:6156357–60
    [Google Scholar]
  119. 119. 
    Lajoie MJ, Söll D, Church GM 2016. Overcoming challenges in engineering the genetic code. J. Mol. Biol. 428:5, Pt. B1004–21
    [Google Scholar]
  120. 120. 
    Mukai T, Lajoie MJ, Englert M, Söll D 2017. Rewriting the genetic code. Annu. Rev. Microbiol. 71:557–77
    [Google Scholar]
  121. 121. 
    Mitchell LA, Phillips NA, Lafont A, Martin JA, Cutting R, Boeke JD 2015. qPCRTag analysis—a high throughput, real time PCR assay for Sc2.0 genotyping. J. Vis. Exp. 99:e52941
    [Google Scholar]
  122. 122. 
    Scior A, Preissler S, Koch M, Deuerling E 2011. Directed PCR-free engineering of highly repetitive DNA sequences. BMC Biotechnol 11:187
    [Google Scholar]
  123. 123. 
    Blacketer MJ, Gannon MK, Young IA, Shogren-Knaak MA 2017. Solid-phase synthesis of highly repetitive chromatin assembly templates. Anal. Biochem. 531:12–15
    [Google Scholar]
  124. 124. 
    Ran FA, Hsu PD, Lin C-Y, Gootenberg JS, Konermann S et al. 2013. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:61380–89
    [Google Scholar]
  125. 125. 
    Trevino AE, Zhang F. 2014. Genome editing using Cas9 nickases. Methods Enzymol 546:161–74
    [Google Scholar]
  126. 126. 
    Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR 2016. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:7603420–24
    [Google Scholar]
  127. 127. 
    Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH et al. 2017. Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage. Nature 551:7681464–71
    [Google Scholar]
  128. 128. 
    Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M et al. 2016. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353:6305aaf8729
    [Google Scholar]
  129. 129. 
    Yang L, Briggs AW, Chew WL, Mali P, Guell M et al. 2016. Engineering and optimising deaminase fusions for genome editing. Nat. Commun. 7:13330
    [Google Scholar]
  130. 130. 
    Ostrov N, Landon M, Guell M, Kuznetsov G, Teramoto J et al. 2016. Design, synthesis, and testing toward a 57-codon genome. Science 353:6301819–22
    [Google Scholar]
  131. 131. 
    Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S 2008. Virus attenuation by genome-scale changes in codon pair bias. Science 320:58841784–87
    [Google Scholar]
  132. 132. 
    Mueller S, Coleman JR, Papamichail D, Ward CB, Nimnual A et al. 2010. Live attenuated influenza virus vaccines by computer-aided rational design. Nat. Biotechnol. 28:7723–26
    [Google Scholar]
  133. 133. 
    Dormitzer PR, Suphaphiphat P, Gibson DG, Wentworth DE, Stockwell TB et al. 2013. Synthetic generation of influenza vaccine viruses for rapid response to pandemics. Sci. Transl. Med. 5:185185ra68
    [Google Scholar]
  134. 134. 
    Dymond JS, Richardson SM, Coombes CE, Babatz T, Muller H et al. 2011. Synthetic chromosome arms function in yeast and generate phenotypic diversity by design. Nature 477:7365471–76
    [Google Scholar]
  135. 135. 
    Shen Y, Stracquadanio G, Wang Y, Yang K, Mitchell LA et al. 2016. SCRaMbLE generates designed combinatorial stochastic diversity in synthetic chromosomes. Genome Res 26:136–49
    [Google Scholar]
  136. 136. 
    Hochrein L, Mitchell LA, Schulz K, Messerschmidt K, Mueller-Roeber B 2018. L-SCRaMbLE as a tool for light-controlled Cre-mediated recombination in yeast. Nat. Commun. 9:1931
    [Google Scholar]
  137. 137. 
    Jia B, Wu Y, Li B-Z, Mitchell LA, Liu H et al. 2018. Precise control of SCRaMbLE in synthetic haploid and diploid yeast. Nat. Commun. 9:1933
    [Google Scholar]
  138. 138. 
    Luo Z, Wang L, Wang Y, Zhang W, Guo Y et al. 2018. Identifying and characterizing SCRaMbLEd synthetic yeast using ReSCuES. Nat. Commun. 9:1930
    [Google Scholar]
  139. 139. 
    Shen MJ, Wu Y, Yang K, Li Y, Xu H et al. 2018. Heterozygous diploid and interspecies SCRaMbLEing. Nat. Commun. 9:1934
    [Google Scholar]
  140. 140. 
    Blount BA, Gowers G-OF, Ho JCH, Ledesma-Amaro R, Jovicevic D et al. 2018. Rapid host strain improvement by in vivo rearrangement of a synthetic yeast chromosome. Nat. Commun. 9:1932
    [Google Scholar]
  141. 141. 
    Liu W, Luo Z, Wang Y, Pham NT, Tuck L et al. 2018. Rapid pathway prototyping and engineering using in vitro and in vivo synthetic genome SCRaMbLE-in methods. Nat. Commun. 9:1936
    [Google Scholar]
  142. 142. 
    Wu Y, Zhu R-Y, Mitchell LA, Ma L, Liu R et al. 2018. In vitro DNA SCRaMbLE. Nat. Commun. 9:1935
    [Google Scholar]
  143. 143. 
    Court Justice EU. 2018. Organisms obtained by mutagenesis are GMOs and are, in principle, subject to the obligations laid down by the GME Directive Press Release 111/18, July 28. https://curia.europa.eu/jcms/upload/docs/application/pdf/2018-07/cp180111en.pdf
    [Google Scholar]
  144. 144. 
    US Dep. Agric 2018. Secretary Perdue issues USDA statement on plant breeding innovation Bulletin, Mar. 28. https://content.govdelivery.com/accounts/USDAAPHIS/bulletins/1e599ff
    [Google Scholar]
  145. 145. 
    Oye KA, Esvelt K, Appleton E, Catteruccia F, Church G et al. 2014. Regulating gene drives. Science 345:6197626–28
    [Google Scholar]
  146. 146. 
    Scudellari M. 2019. Self-destructing mosquitoes and sterilized rodents: the promise of gene drives. Nature 571:7764160–62
    [Google Scholar]
  147. 147. 
    Natl. Acad. Sci. Eng. Med 2017. Human Genome Editing: Science, Ethics, and Governance Washington, DC: Natl. Acad. Press
    [Google Scholar]
  148. 148. 
    Boeke JD, Church G, Hessel A, Kelley NJ, Arkin A et al. 2016. The Genome Project-Write. Science 353:6295126–27
    [Google Scholar]
  149. 149. 
    Miga KH. 2019. Centromeric satellite DNAs: hidden sequence variation in the human population. Genes 10:5352
    [Google Scholar]
  150. 150. 
    Mitchell LA, McCulloch LH, Pinglay S, Berger H, Bosco N et al. 2019. De novo assembly, delivery and expression of a 101 kb human gene in mouse cells. bioRxiv 423426. https://doi.org/10.1101/423426
    [Crossref]
  151. 151. 
    Laurent JM, Fu X, German S, Maurano MT, Zhang K, Boeke JD 2019. Big DNA as a tool to dissect an age-related macular degeneration-associated haplotype. Precis. Clin. Med. 2:11–7
    [Google Scholar]
  152. 152. 
    Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:7307720–26
    [Google Scholar]
  153. 153. 
    Zarrella I, Herten K, Maes GE, Tai S, Yang M et al. 2019. The survey and reference assisted assembly of the Octopus vulgaris genome. Sci. Data 6:113
    [Google Scholar]
  154. 154. 
    Johnson DBF, Wang C, Xu J, Schultz MD, Schmitz RJ et al. 2012. Release factor one is nonessential in Escherichia coli. ACS Chem. Biol 7:81337–44
    [Google Scholar]
  155. 155. 
    Rovner AJ, Haimovich AD, Katz SR, Li Z, Grome MW et al. 2015. Recoded organisms engineered to depend on synthetic amino acids. Nature 518:753789–93
    [Google Scholar]
  156. 156. 
    Mandell DJ, Lajoie MJ, Mee MT, Takeuchi R, Kuznetsov G et al. 2015. Biocontainment of genetically modified organisms by synthetic protein design. Nature 518:753755–60
    [Google Scholar]
  157. 157. 
    Naito T, Matsuura A, Ishikawa F 1998. Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat. Genet. 20:2203
    [Google Scholar]
  158. 158. 
    Haber JE, Rogers DT, McCusker JH 1980. Homothallic conversions of yeast mating-type genes occur by intrachromosomal recombination. Cell 22:1, Pt. 1277–89
    [Google Scholar]
  159. 159. 
    Ueda Y, Ikushima S, Sugiyama M, Matoba R, Kaneko Y et al. 2012. Large-scale genome reorganization in Saccharomyces cerevisiae through combinatorial loss of mini-chromosomes. J. Biosci. Bioeng. 113:6675–82
    [Google Scholar]
  160. 160. 
    Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N et al. 2015. Polyploidy can drive rapid adaptation in yeast. Nature 519:7543349–52
    [Google Scholar]
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