Skip to main content
SpringerLink
Log in
Book cover

Functional Genomics and Biotechnology in Solanaceae and Cucurbitaceae Crops pp 239–250Cite as

Genome-Editing Technologies and Their Use in Tomato

  • Chapter
  • First Online:

  • 1374 Accesses

Part of the book series: Biotechnology in Agriculture and Forestry ((AGRICULTURE,volume 70))

Abstract

Genome-editing technology using artificial nucleases has enormous potential as a plant-breeding tool that can be used to create mutations at only the targeted sites in genes of interest. Indeed, successful gene modification in a variety of plant species using artificial nucleases, including ZFNs, TALENs and CRISPER/Cas9s, has been reported. TALEN and CRISPER/Cas9 technologies have been successfully applied in tomato, which is an economically important and useful model crop for studying fleshy fruit development. Tomatoes with the TALEN-modified PROCERA gene, a negative regulator of gibberellin signalling, showed the expected tall and slender phenotypes. Modifications in SlAGO7 using CRISPER/Cas9s influenced the leaf morphology. Although genome editing using artificial nucleases still possesses potential problems, such as low efficiency or off-target binding, this technology exhibits sufficient potential to consider it to be an efficient tool for manipulating the tomato genome and generating better materials for tomato breeding. In this chapter, genome-editing technologies in plants and the application of these methods for genome modification in tomato plants are summarized.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Azadi H, Ho P (2010) Genetically modified and organic crops in developing countries: a review of options for food security. Biotechnol Adv 28(1):160–168

    Article  PubMed  Google Scholar 

  • Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG 2nd, Tan W, Penheiter SG, Ma AC, Leung AY, Fahrenkrug SC, Carlson DF, Voytas DF, Clark KJ, Essner JJ, Ekker SC (2012) In vivo genome editing using a high-efficiency TALEN system. Nature 491(7422):114–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beumer k, Bhattacharyya G, Bibikova M, Trautman JK, Carroll D (2006) Efficient gene targeting in Drosophila with zinc-finger nucleases. Genetics 172:2391–2403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bibikova M, Carroll D, Segal DJ, Trautman JK, Smith J, Kim YG, Chandrasegaran S (2001) Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol 21(1):289–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bitinaite J, Wah DA, Aggarwal AK, Schildkraut I (1998) FokI dimerization is required for DNA cleavage. Proc Natl Acad Sci U S A 95(18):10570–10575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326(1509):1509–1512

    Article  CAS  PubMed  Google Scholar 

  • Briggs AW, Rios X, Chari R, Yang L, Zhang F, Mali P, Church GM (2012) Iterative capped assembly: rapid and scalable synthesis of repeat-module DNA such as TAL effectors from individual monomers. Nucleic Acids Res 40(15):e117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Britt AB, May GD (2003) Re-engineering plant gene targeting. Trends Plant Sci 8(2):90–95

    Article  CAS  PubMed  Google Scholar 

  • Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166(3):1292–1297

    Article  PubMed  PubMed Central  Google Scholar 

  • Carroll D (2011) Genome engineering with zinc-finger nucleases. Genetics 188:773–782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cermak T, Doyle E, Christian M, Wang L, Zhang Y, Schmidt C, Baller J, Somia NV, Bogdanove AJ, Voytas D (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39(17):7879

    Article  CAS  PubMed Central  Google Scholar 

  • Chen K, Gao C (2013) TALENs: customizable molecular DNA scissors for genome engineering of plants. J Genet Genomics 40(6):271–279

    Article  PubMed  Google Scholar 

  • Chen S, Oikonomou G, Chiu CN, Niles BJ, Liu J, Lee DA, Antoshechkin I, Prober DA (2013) A large-scale in vivo analysis reveals that TALENs are significantly more mutagenic than ZFNs generated using context-dependent assembly. Nucleic Acids Res 41(4):2769–2778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christian ML, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186(2):757–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christian ML, Demorest ZL, Starker CG, Osborn MJ, Nyquist MD, Zhang Y, Carlson DF, Bradley P, Bogdanove AJ, Voytas DF (2012) Targeting G with TAL effectors: a comparison of activities of TALENs constructed with NN and NK repeat variable di-residues. PLoS One 7(9):e45383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cradick TJ, Fine EJ, Antico CJ, Bao G (2013) CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 41(20):9584–9592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Pater S, Neuteboom LW, Pinas JE, Hooykaas PJ, van der Zaal BJ (2009) ZFN-induced mutagenesis and gene-targeting in Arabidopsis through Agrobacterium-mediated floral dip transformation. Plant Biotechnol J 7(8):821–835

    Article  PubMed  Google Scholar 

  • Deng D, Yan C, Pan X, Mahfouz M, Wang J, Zhu JK, Shi Y, Yan N (2012) Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335(6069):720–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle EL, Booher NJ, Standage DS, Voytas DF, Brendel VP, Vandyk JK, Bogdanove AJ (2012) TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res 40(Web Server issue):W117–W122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng Z, Mao Y, Xu N, Zhang B, Wei P, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci U S A 111(12):4632–4637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao J, Wang G, Ma S, Xie X, Wu X, Zhang X, Wu Y, Zhao P, Xia Q (2015) CRISPR/Cas9 mediated targeted mutagenesis in Nicotiana tabacum. Plant Mol Biol 87(1–2):99–110

    Article  CAS  PubMed  Google Scholar 

  • Gürlbeck D, Thieme F, Bonas U (2006) Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J Plant Physiol 163(3):233–255

    Article  Google Scholar 

  • Gurushidze M, Hensel G, Hiekel S, Schedel S, Valkov V, Kumlehn J (2014) True-breeding targeted gene knock-out in Barley using designer TALE-Nuclease in haploid cells. PLoS One 9(3):e92046

    Article  PubMed  PubMed Central  Google Scholar 

  • Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12(7):934–940

    Article  CAS  PubMed  Google Scholar 

  • Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29(8):699–700

    Article  PubMed  Google Scholar 

  • Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3):233–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318(5850):648–651

    Article  CAS  PubMed  Google Scholar 

  • Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93(3):1156–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Huang S, Zhao X, Wright DA, Carpenter C, Spalding MH, Weeks DP, Yang B (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 39(14):6315–6325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat biotechnol 30(5):390–392

    Article  CAS  PubMed  Google Scholar 

  • Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31(8):688–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang Z, Zhang K, Chen K, Gao C (2014) Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J Genet Genomics 41(2):63–68

    Article  CAS  PubMed  Google Scholar 

  • Lioyd A, Plaisier CL, Carroll D, Drews GN (2005) Targeted mutagenesis using zinc-finger nucleases in Arabidopsis. Proc Natl Acad Sci U S A 102(6):2232–2237

    Article  Google Scholar 

  • Liu Q, Xia Z, Zhong X, Case CC (2002) Validated zinc finger protein designs for all 16 GNN DNA triplet targets. J Biol Chem 277(6):3850–3856

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Li C, Yu Z, Huang P, Wu H, Wei C, Zhu N, Shen Y, Chen Y, Zhang B, Deng WM, Jiao R (2012) Efficient and specific modifications of the Drosophila genome by means of an easy TALEN strategy. J Genet Genomics 39(5):209–215

    Article  CAS  PubMed  Google Scholar 

  • Lor VS, Starker CG, Voytas DF, Weiss D, Olszewski NE (2014) Targeted mutagenesis of the tomato PROCERA gene using transcription activator-like effector nucleases. Plant Physiol 166(3):1288–1291

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahfouz MM, Li L (2011) TALE nucleases and next generation GM crops. GM Crops 2(2):99–103

    Article  PubMed  Google Scholar 

  • Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK (2011) De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci U S A 108(6):2623–2628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marois E, Van den Ackerveken G, Bonas U (2002) The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant Microbe Interact 15(7):637–646

    Article  CAS  PubMed  Google Scholar 

  • Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, Wan J, Gu H, Qu LJ (2013) Targeted mutagenesis in rice using CRISPR-Cas system. Cell Res 23(10):1233–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, Dulay GP, Hua KL, Ankoudinova I, Cost GJ, Urnov FD, Zhang S, Holmes MC, Zhang L, Gregory PD, Rebar EJ (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29(2):143–148

    Article  CAS  PubMed  Google Scholar 

  • Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 356(5959):1501

    Article  Google Scholar 

  • Mussolino C, Morbitzer R, Lütge F, Dannemann N, Lahaye T, Cathomen T (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39(21):9283–9293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31(8):691–693

    Article  CAS  PubMed  Google Scholar 

  • Osakabe K, Osakabe Y, Toki S (2010) Site-directed mutagenesis in Arabidopsis using custom-designed zinc finger nucleases. Proc Natl Acad Sci U S A 107(26):12034–12039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramirez CL, Foley JE, Wright DA, Müller-Lerch F, Rahman SH, Cornu TI, Winfrey RJ, Sander JD, Fu F, Townsend JA, Cathomen T, Voytas DF, Joung JK (2008) Unexpected failure rates for modular assembly of engineered zinc fingers. Nat Methods 5(5):374–375

    Article  CAS  PubMed  Google Scholar 

  • Ray A, Langer M (2002) Homologous recombination: ends as the means. Trends Plant Sci 7(10):435–440

    Article  CAS  PubMed  Google Scholar 

  • Roderick H, Tripatihi L, Babirye A, Wang D, Tripathi J, Urwin PE, Atkinson HJ (2012) Generation of transgenic plantain (Musa spp.) with resistance to plant pathogenic nematodes. Mol Plant Pathol 13(8):842–851

    Article  CAS  PubMed  Google Scholar 

  • Römer P, Recht S, Lahaye T (2009) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc Natl Acad Sci U S A 106(48):20526–20531

    Article  PubMed  PubMed Central  Google Scholar 

  • Saito T, Ariizumi T, Okabe Y, Asamizu E, Hiwasa-tanase K, Fukuda N, Mizoguchi T, Yamazaki Y, Aoki K, Ezura H (2011) TOMATOMA: a novel tomato mutant database distributing Micro-Tom mutant collections. Plant Cell Physiol 52(2):283–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, Yeh JR (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29(8):697–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Segal DJ (2002) The use of zinc finger peptides to study the role of specific factor binding sites in the chromatin environment. Methods 26(1):76–83

    Article  CAS  PubMed  Google Scholar 

  • Segal DJ, Dreier B, Beerli RR, Barbas CF 3rd (1999) Toward controlling gene expression at will: selection and design of zinc finger domains recognizing each of the 5′-GNN-3′ DNA target sequences. Proc Natl Acad Sci U S A 96(6):2758–2763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan Q, Wang Y, Chen K, Liang Z, Li J, Zhang Y, Zhang K, Liu J, Voytas DF, Zheng X, Zhang Y, Gao C (2013a) Rapid and efficient gene modification in rice and Brachypodium using TALENs. Mol Plant 6(4):1365–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013b) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31(8):686–688

    Article  CAS  PubMed  Google Scholar 

  • Shan Q, Wang Y, Li J, Gao C (2014) Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc 9(10):2395–2410

    Article  CAS  PubMed  Google Scholar 

  • Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD, Urnov FD (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459(7245):437–441

    Article  CAS  PubMed  Google Scholar 

  • Sripaoraya S, Keawsompong S, Insupa P, Power JB, Davey MR, Srinives P (2006) Genetically manipulated pineapple: trans-gene stability, gene expression and herbicide tolerance under field conditions. Plant Breed 125(4):411–413

    Article  CAS  Google Scholar 

  • Streubel J, Blücher C, Landgraf A, Boch J (2012) TAL effector RVD specificities and efficiencies. Nat Biotechnol 30(7):593–595

    Article  CAS  PubMed  Google Scholar 

  • The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635-641

    Google Scholar 

  • Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459(7245):442–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyay SK, Kumar J, Alok A, Tuli R (2013) RNA-guided genome editing for target gene mutations in wheat. G3 (Bethesda) 3(12):2233–2238

    Article  CAS  Google Scholar 

  • Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32(9):947–951

    Article  CAS  PubMed  Google Scholar 

  • Weber E, Gruetzner R, Werner S, Engler C, Marillonnet S (2011) Assembly of designer TAL effectors by golden gate cloning. PLoS One 6(5):e19722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendt T, Holm PB, Starker CG, Christian M, Voytas DF, Brinch-Pedersen H, Holme IB (2013) TAL effector nucleases induce mutations at a pre-selected location in the genome of primary barley transformants. Plant Mol Biol 83(3):279–285

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Zhu W, Johnson LB, White FF (2000) The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway dependent nuclear-localized double-stranded DNA-binding protein. Proc Natl Acad Sci U S A 97(17):9807–9812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D, Peterson T, Joung JK, Voytas DF (2009) High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci U S A 107(26):12028–12033

    Article  Google Scholar 

  • Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG, Bogdanove AJ, Voytas DF (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161(1):20–27

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan

    Jeong-Eun Lee & Hiroshi Ezura

Authors
  1. Jeong-Eun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroshi Ezura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroshi Ezura .

Editor information

Editors and Affiliations

  1. University of Tsukuba Faculty of Life and Environmental Sc., Tsukuba, Japan

    Hiroshi Ezura

  2. University of Tsukuba, Faculty of Life and Environmental Sciences, Tsukuba, Japan

    Tohru Ariizumi

  3. IRTA, Center for Research in Agricultural Genomics CSIC-IRTA-UAB-UB, Barcelona, Spain

    Jordi Garcia-Mas

  4. Cornell University, Plant Biology Section, School of Integrated Plant Science, Ithaca, New York, USA

    Jocelyn Rose

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lee, JE., Ezura, H. (2016). Genome-Editing Technologies and Their Use in Tomato. In: Ezura, H., Ariizumi, T., Garcia-Mas, J., Rose, J. (eds) Functional Genomics and Biotechnology in Solanaceae and Cucurbitaceae Crops. Biotechnology in Agriculture and Forestry, vol 70. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-48535-4_14

Download citation

Publish with us

Policies and ethics

Search

Navigation