Skip to main content

Applications of CPPs in Genome Editing of Plants

  • Protocol
  • First Online:
Cell Penetrating Peptides

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2383))

Abstract

Cell penetrating peptides (CPPs) are short peptides that are able to translocate themselves and their cargo into cells. The progressive and continuous application of CPPs in various fields of basic and applied research shows that they are efficient delivery vectors for an assortment of biomolecules, including nucleic acids and proteins. This feature makes CPPs an excellent tool for modification of plant genomes through transgenesis and genome editing. In this review, we present the progress during the last three decades in application of CPPs for delivery of DNA, RNA, and proteins into plant cells and tissues. Moreover, we highlight the exploiting of CPPs as advantageous and beneficial tool for plant genome editing via delivery of nuclease proteins, and provide a practical example of genome alternation through CPP-delivered nucleases. Finally, the current exploitation of peptides in organelle-specific DNA delivery and modification of organellar genomes is discussed.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
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

Institutional subscriptions

References

  1. McCarty DR, Latshaw S, Wu S, Suzuki M, Hunter CT, Avigne WT, Koch KE (2013) Mu-seq: sequence-based mapping and identification of transposon induced mutations. PLoS One 8:e77172. https://doi.org/10.1371/journal.pone.0077172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hirochika H, Guiderdoni E, An G, Hsing YI, Eun MY et al (2004) Rice mutant resources for gene discovery. Plant Mol Biol 54:325–334. https://doi.org/10.1023/B:PLAN.0000036368.74758.66

    Article  CAS  PubMed  Google Scholar 

  3. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA et al (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36:283–287. https://doi.org/10.1038/ng1314

    Article  CAS  PubMed  Google Scholar 

  4. Smyth SJ (2020) The human health benefits from GM crops. Plant Biotechnol J 18(4):887–888. https://doi.org/10.1111/pbi.13261

    Article  PubMed  Google Scholar 

  5. Bak RO, Gomez-Ospina N, Porteus MH (2018) Gene editing on center stage. Trends Genet 34(8):600–611. https://doi.org/10.1016/j.tig.2018.05.004

    Article  CAS  PubMed  Google Scholar 

  6. Zhang Y, Massel K, Godwin ID, Gao C (2018) Applications and potential of genome editing in crop improvement. Genome Biol 19:210. https://doi.org/10.1186/s13059-018-1586-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Huang YW, Lee HJ, Tolliver LM, Aronstam RS (2015) Delivery of nucleic acids and nanomaterials by cell-penetrating peptides: opportunities and challenges. Biomed Res Int 2015:834079. https://doi.org/10.1155/2015/834079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Frankel AD, Pabo CO (1988) Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55(6):1189–1193. https://doi.org/10.1016/0092-8674(88)90263-2

    Article  CAS  PubMed  Google Scholar 

  9. Vives E, Brodin P, Lebleu B (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272(25):16010–16017. https://doi.org/10.1074/jbc.272.25.16010

    Article  CAS  PubMed  Google Scholar 

  10. Zorko M, Langel U (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 57(4):529–545. https://doi.org/10.1016/j.addr.2004.10.010

    Article  CAS  PubMed  Google Scholar 

  11. Chugh A, Eudes F, Shim YS (2010) Cell-penetrating peptides: nanocarrier for macromolecule delivery in living cells. IUBMB Life 62(3):183–193. https://doi.org/10.1002/iub.297

    Article  CAS  PubMed  Google Scholar 

  12. Eiriksdottir E, Konate K, Langel U, Divita G, Deshayes S (2010) Secondary structure of cell-penetrating peptides controls membrane interaction and insertion. Biochim Biophys Acta 1798(6):1119–1128. https://doi.org/10.1016/j.bbamem.2010.03.005

    Article  CAS  PubMed  Google Scholar 

  13. Madani F, Lindberg S, Langel U, Futaki S, Graslund A (2011) Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys 2011:414729. https://doi.org/10.1155/2011/414729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ziegler A (2008) Thermodynamic studies and binding mechanisms of cell-penetrating peptides with lipids and glycosaminoglycans. Adv Drug Deliv Rev 60(4–5):580–597. https://doi.org/10.1016/j.addr.2007.10.005

    Article  CAS  PubMed  Google Scholar 

  15. Soomets U, Lindgren M, Gallet X, Hallbrink M, Elmquist A, Balaspiri L et al (2000) Deletion analogues of transportan. Biochim Biophys Acta 1467(1):165–176. https://doi.org/10.1016/s0005-2736(00)00216-9

    Article  CAS  PubMed  Google Scholar 

  16. El-Andaloussi S, Johansson HJ, Holm T, Langel U (2007) A novel cell-penetrating peptide, M918, for efficient delivery of proteins and peptide nucleic acids. Mol Ther 15(10):1820–1826. https://doi.org/10.1038/sj.mt.6300255

    Article  CAS  PubMed  Google Scholar 

  17. Elmquist A, Lindgren M, Bartfai T, Langel U (2001) VE-cadherin-derived cell-penetrating peptide, pVEC, with carrier functions. Exp Cell Res 269(2):237–244. https://doi.org/10.1006/excr.2001.5316

    Article  CAS  PubMed  Google Scholar 

  18. Futaki S, Suzuki T, Ohashi W, Yagami T, Tanaka S, Ueda K et al (2001) Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J Biol Chem 276(8):5836–5840. https://doi.org/10.1074/jbc.M007540200

    Article  CAS  PubMed  Google Scholar 

  19. Rusiecka I, Ruczynski J, Alenowicz M, Rekowski P, Kocic I (2016) Transportan 10 improves the anticancer activity of cisplatin. Naunyn Schmiedeberg’s Arch Pharmacol 389(5):485–497. https://doi.org/10.1007/s00210-016-1219-5

    Article  CAS  Google Scholar 

  20. Khalil IA, Kogure K, Akita H, Harashima H (2006) Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol Rev 58(1):32–45. https://doi.org/10.1124/pr.58.1.8

    Article  CAS  PubMed  Google Scholar 

  21. Mae M, Langel U (2006) Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery. Curr Opin Pharmacol 6(5):509–514. https://doi.org/10.1016/j.coph.2006.04.004

    Article  CAS  PubMed  Google Scholar 

  22. Mano M, Teodosio C, Paiva A, Simoes S, Pedroso de Lima MC (2005) On the mechanisms of the internalization of S4(13)-PV cell-penetrating peptide. Biochem J 390(Pt 2):603–612. https://doi.org/10.1042/BJ20050577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nakase I, Tadokoro A, Kawabata N, Takeuchi T, Katoh H, Hiramoto K et al (2007) Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 46(2):492–501. https://doi.org/10.1021/bi0612824

    Article  CAS  PubMed  Google Scholar 

  24. Lindgren M, Langel U (2011) Classes and prediction of cell-penetrating peptides. Methods Mol Biol 683:3–19. https://doi.org/10.1007/978-1-60761-919-2_1

    Article  CAS  PubMed  Google Scholar 

  25. Fretz MM, Penning NA, Al-Taei S, Futaki S, Takeuchi T, Nakase I et al (2007) Temperature-, concentration- and cholesterol-dependent translocation of L- and D-octa-arginine across the plasma and nuclear membrane of CD34+ leukaemia cells. Biochem J 403(2):335–342. https://doi.org/10.1042/BJ20061808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Takeuchi T, Futaki S (2016) Current understanding of direct translocation of arginine-rich cell-penetrating peptides and its internalization mechanisms. Chem Pharma Bull 64(10):1431–1437. https://doi.org/10.1248/cpb.c16-00505

    Article  CAS  Google Scholar 

  27. Mae M, Myrberg H, Jiang Y, Paves H, Valkna A, Langel U (2005) Internalisation of cell-penetrating peptides into tobacco protoplasts. Biochim Biophys Acta 1669(2):101–107. https://doi.org/10.1016/j.bbamem.2005.01.006

    Article  CAS  PubMed  Google Scholar 

  28. Chugh A, Eudes F (2008) Cellular uptake of cell-penetrating peptides pVEC and transportan in plants. J Pept Sci 14(4):477–481. https://doi.org/10.1002/psc.937

    Article  CAS  PubMed  Google Scholar 

  29. Chugh A, Eudes F (2008) Study of uptake of cell penetrating peptides and their cargoes in permeabilized wheat immature embryos. FEBS J 275(10):2403–2414. https://doi.org/10.1111/j.1742-4658.2008.06384.x

    Article  CAS  PubMed  Google Scholar 

  30. Numata K, Horii Y, Oikawa K, Miyagi Y, Demura T, Ohtani M (2018) Library screening of cell-penetrating peptide for BY-2 cells, leaves of Arabidopsis, tobacco, tomato, poplar, and rice callus. Sci Rep 8(1):10966. https://doi.org/10.1038/s41598-018-29298-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Jarver P, Langel U (. (2006) Cell-penetrating peptides—a brief introduction. Biochim Biophys Acta 1758(3):260–263. https://doi.org/10.1016/j.bbamem.2006.02.012

    Article  CAS  PubMed  Google Scholar 

  32. Cartier R, Reszka R (2002) Utilization of synthetic peptides containing nuclear localization signals for nonviral gene transfer systems. Gene Ther 9(3):157–167. https://doi.org/10.1038/sj.gt.3301635

    Article  CAS  PubMed  Google Scholar 

  33. Morris MC, Vidal P, Chaloin L, Heitz F, Divita G (1997) A new peptide vector for efficient delivery of oligonucleotides into mammalian cells. Nucleic Acids Res 25(14):2730–2736. https://doi.org/10.1093/nar/25.14.2730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen CP, Chou JC, Liu BR, Chang M, Lee HJ (2007) Transfection and expression of plasmid DNA in plant cells by an arginine-rich intracellular delivery peptide without protoplast preparation. FEBS Lett 581(9):1891–1897. https://doi.org/10.1016/j.febslet.2007.03.076

    Article  CAS  PubMed  Google Scholar 

  35. Liu W, Yuan JS, Stewart CN Jr (2013) Advanced genetic tools for plant biotechnology. Nat Rev Genet 14(11):781–793. https://doi.org/10.1038/nrg3583

    Article  CAS  PubMed  Google Scholar 

  36. Chugh A, Amundsen E, Eudes F (2009) Translocation of cell-penetrating peptides and delivery of their cargoes in triticale microspores. Plant Cell Rep 28(5):801–810. https://doi.org/10.1007/s00299-009-0692-4

    Article  CAS  PubMed  Google Scholar 

  37. Lakshmanan M, Kodama Y, Yoshizumi T, Sudesh K, Numata K (2013) Rapid and efficient gene delivery into plant cells using designed peptide carriers. Biomacromolecules 14(1):10–16. https://doi.org/10.1021/bm301275g

    Article  CAS  PubMed  Google Scholar 

  38. Silva S, Almeida AJ, Vale N (2019) Combination of cell-penetrating peptides with nanoparticles for therapeutic application: a review. Biomol Ther 9(1):22. https://doi.org/10.3390/biom9010022

    Article  CAS  Google Scholar 

  39. Zonin E, Moscatiello R, Miuzzo M, Cavallarin N, Di Paolo ML, Sandona D et al (2011) TAT-mediated aequorin transduction: an alternative approach for effective calcium measurements in plant cells. Plant Cell Physiol 52(12):2225–2235. https://doi.org/10.1093/pcp/pcr145

    Article  CAS  PubMed  Google Scholar 

  40. Miyamoto T, Tsuchiya K, Numata K (2019) Block copolymer/plasmid DNA micelles postmodified with functional peptides via thiol-maleimide conjugation for efficient gene delivery into plants. Biomacromolecules 20(2):653–661. https://doi.org/10.1021/acs.biomac.8b01304

    Article  CAS  PubMed  Google Scholar 

  41. Chang M, Chou JC, Chen CP, Liu BR, Lee HJ (2007) Noncovalent protein transduction in plant cells by macropinocytosis. New Phytol 174(1):46–56. https://doi.org/10.1111/j.469-8137.2007.01977.x

    Article  CAS  PubMed  Google Scholar 

  42. Chang M, Huang YW, Aronstam RS, Lee HJ (2014) Cellular delivery of noncovalently-associated macromolecules by cell-penetrating peptides. Curr Pharm Biotechnol 15(3):267–275. https://doi.org/10.2174/1389201015666140617095415

    Article  CAS  PubMed  Google Scholar 

  43. Jain A, Yadav BK, Chugh A (2015) Marine antimicrobial peptide tachyplesin as an efficient nanocarrier for macromolecule delivery in plant and mammalian cells. FEBS J 282(4):732–745. https://doi.org/10.1111/febs.13178

    Article  CAS  PubMed  Google Scholar 

  44. Qi X, Droste T, Kao CC (2011) Cell-penetrating peptides derived from viral capsid proteins. Mol Plant-Microbe Interact 24(1):25–36. https://doi.org/10.1094/MPMI-07-10-0147

    Article  CAS  PubMed  Google Scholar 

  45. Bilichak A, Luu J, Eudes F (2015) Intracellular delivery of fluorescent protein into viable wheat microspores using cationic peptides. Front Plant Sci 6:666. https://doi.org/10.3389/fpls.2015.00666

    Article  PubMed  PubMed Central  Google Scholar 

  46. Chang M, Chou JC, Lee HJ (2005) Cellular internalization of fluorescent proteins via arginine-rich intracellular delivery peptide in plant cells. Plant Cell Physiol 46(3):482–488. https://doi.org/10.1093/pcp/pci046

    Article  CAS  PubMed  Google Scholar 

  47. Lu SW, Hu JW, Liu BR, Lee CY, Li JF, Chou JC et al (2010) Arginine-rich intracellular delivery peptides synchronously deliver covalently and noncovalently linked proteins into plant cells. J Agric Food Chem 58(4):2288–2294. https://doi.org/10.1021/jf903039j

    Article  CAS  PubMed  Google Scholar 

  48. Ng KK, Motoda Y, Watanabe S, Sofiman Othman A, Kigawa T, Kodama Y, Numata K (2016) Intracellular delivery of proteins via fusion peptides in intact plants. PLoS One 11(4):e0154081. https://doi.org/10.1371/journal.pone.0154081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Eggenberger K, Mink C, Wadhwani P, Ulrich AS, Nick P (2011) Using the peptide BP100 as a cell-penetrating tool for the chemical engineering of actin filaments within living plant cells. Chembiochem 12(1):132–137. https://doi.org/10.1002/cbic.201000402

    Article  CAS  PubMed  Google Scholar 

  50. Zhang Y, Zhang F, Li X, Baller JA, Qi Y, Starker CG et al (2013) Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol 161(1):20–27. https://doi.org/10.1104/pp.112.205179

    Article  CAS  PubMed  Google Scholar 

  51. Bilichak A, Sastry-Dent L, Sriram S, Simpson M, Samuel P, Webb S et al (2020) Genome editing in wheat microspores and haploid embryos mediated by delivery of ZFN proteins and cell-penetrating peptide complexes. Plant Biotechnol J 18(5):1307–1316. https://doi.org/10.1111/pbi.13296

    Article  CAS  PubMed  Google Scholar 

  52. Bilichak A, Gaudet D, Laurie J (2072) Emerging genome engineering tools in crop research and breeding. Methods Mol Biol 2020:165–181. https://doi.org/10.1007/978-1-4939-9865-4_14

    Article  CAS  Google Scholar 

  53. Ziemienowicz A, Shim YS, Matsuoka A, Eudes F, Kovalchuk I (2012) A novel method of transgene delivery into triticale plants using the Agrobacterium transferred DNA-derived nano-complex. Plant Physiol 158(4):1503–1513. https://doi.org/10.1104/pp.111.192856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Shim YS, Eudes F, Kovalchuk I (2013) dsDNA and protein co-delivery in triticale microspores. In Vitro Cell Dev Biol Plant 49(2):156–165. https://doi.org/10.1007/s11627-012-9471-y

    Article  CAS  Google Scholar 

  55. Pepper JT, Maheshwari P, Ziemienowicz A, Hazendonk P, Kovalchuk I, Eudes F (2017) Tetrabutylphosphonium bromide reduces size and polydispersity index of Tat2:siRNA nano-complexes for triticale RNAi. Front Mol Biosci 4:30. https://doi.org/10.3389/fmolb.2017.00030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Numata K, Ohtani M, Yoshizumi T, Demura T, Kodama Y (2014) Local gene silencing in plants via synthetic dsRNA and carrier peptide. Plant Biotechnol J 12(8):1027–1034. https://doi.org/10.1111/pbi.12208

    Article  CAS  PubMed  Google Scholar 

  57. Barton KA, Binns AN, Matzke AJM, Chilton M-D (1983) Regeneration of intact tobacco plants containing full length copies of genetically engineered T-DNA, and transmission of T-DNA to R1 progeny. Cell 32:1033–1043. https://doi.org/10.1016/0092-8674(83)90288-X

    Article  CAS  PubMed  Google Scholar 

  58. Sanford JC (1990) Biolistic plant transformation. Physiol Plant 79(1):206–209. https://doi.org/10.1111/j.1399-3054.1990.tb05888.x

    Article  CAS  Google Scholar 

  59. Liu J, Nannas NJ, Fu FF, Shi J, Aspinwall B, Parrott WA, Dawe RK (2019) Genome-scale sequence disruption following biolistic transformation in rice and maize. Plant Cell 31(2):368–383. https://doi.org/10.1105/tpc.18.00613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Svitashev SK, Pawlowski WP, Makarevitch I, Plank DW, Somers DA (2002) Complex transgene locus structures implicate multiple mechanisms for plant transgene rearrangement. Plant J 32(4):433–445. https://doi.org/10.1046/j.1365-313X.2002.01433.x

    Article  CAS  PubMed  Google Scholar 

  61. Hamada H, Liu Y, Nagira Y, Miki R, Taoka N, Imai R (2018) Biolistic-delivery-based transient CRISPR/Cas9 expression enables in planta genome editing in wheat. Sci Rep 8:14422. https://doi.org/10.1038/s41598-018-32714-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Maher MF, Nasti RA, Vollbrecht M, Starker CG, Clark MD, Voytas DF (2020) Plant gene editing through de novo induction of meristems. Nat Biotechnol 38(1):84–89. https://doi.org/10.1038/s41587-019-0337-2

    Article  CAS  PubMed  Google Scholar 

  63. Ellison EE, Nagalakshmi U, Gamo ME, Huang PJ, Dinesh-Kumar S, Voytas DF (2020) Multiplexed heritable gene editing using RNA viruses and mobile single guide RNAs. Nat Plants 6(6):620–624. https://doi.org/10.1038/s41477-020-0670-y

    Article  CAS  PubMed  Google Scholar 

  64. Ghoshal B, Vong B, Picard CL, Feng S, Tam JM, Jacobsen SE (2020) A viral guide RNA delivery system for CRISPR-based transcriptional activation and heritable targeted DNA demethylation in Arabidopsis thaliana. PLoS Genet 16(12):e1008983. https://doi.org/10.1371/journal.pgen.1008983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Martin F, Sanchez-Hernandez S, Gutierrez-Guerrero A, Pinedo-Gomez J, Benabdellah K (2016) Biased and unbiased methods for the detection of off-target cleavage by CRISPR/Cas9: an overview. Int J Mol Sci 17(9):1507. https://doi.org/10.3390/ijms17091507

    Article  CAS  PubMed Central  Google Scholar 

  66. Okonechnikov K, Golosova O, Fursov M, the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28(8):1166–1167. https://doi.org/10.1093/bioinformatics/bts091

    Article  CAS  PubMed  Google Scholar 

  67. Svitashev S, Schwartz C, Lenderts B, Young JK, Cigan AM (2016) Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nat Commun 7(1):13274. https://doi.org/10.1038/ncomms13274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Liang Z, Chen K, Zhang Y, Liu J, Yin K, Qiu J-L, Gao C (2018) Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nat Protoc 13(3):413–430. https://doi.org/10.1038/nprot.2017.145

    Article  CAS  PubMed  Google Scholar 

  69. Murovec J, Gucek K, Bohanec B, Avbelj M, Jerala R (2018) DNA-free genome editing of Brassica oleracea and B. rapa protoplasts using CRISPR-Cas9 ribonucleoprotein complexes. Front Plant Sci 9:1594. https://doi.org/10.3389/fpls.2018.01594

    Article  PubMed  PubMed Central  Google Scholar 

  70. Park J, Choi S, Park S, Yoon J, Park AY, Choe S (2019) DNA-free genome editing via ribonucleoprotein (RNP) delivery of CRISPR/Cas in lettuce. Methods Mol Biol 1917:337–354. https://doi.org/10.1007/978-1-4939-8991-1_25

    Article  CAS  PubMed  Google Scholar 

  71. Banakar R, Schubert M, Collingwood M, Vakulskas C, Eggenberger AL, Wang K (2020) Comparison of CRISPR-Cas9/Cas12a ribonucleoprotein complexes for genome editing efficiency in the rice phytoene desaturase (OsPDS) gene. Rice 13(1):4. https://doi.org/10.1186/s12284-019-0365-z

    Article  PubMed  PubMed Central  Google Scholar 

  72. Bhattacharya A, Kumar A, Desai N, Parikh S (2012) Organelle transformation. Methods Mol Biol 877:401–406. https://doi.org/10.1007/978-1-61779-818-4_29

    Article  CAS  PubMed  Google Scholar 

  73. Maliga P, Bock R (2011) Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol 155(4):1501–1510. https://doi.org/10.1104/pp.110.170969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Bolsover SR, Hyams JS, Shephard EA, White HA, Wiederman CG (2003) Intracellular protein trafficking. Cell biology: a short course, 2nd edn. Wiley, pp 213–235. https://doi.org/10.1002/047146158X.ch1

    Book  Google Scholar 

  75. Wani SH, Haider N, Kumar H, Sigh N (2010) Plant plastid engineering. Curr Genomics 11(7):500–512. https://doi.org/10.2174/138920210793175912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Kanevski I, Maliga P (1994) Relocation of the plastid rbcL gene to the nucleus yields functional ribulose-1,5-bisphosphate carboxylase in tobacco chloroplasts. Proc Natl Acad Sci U S A 91(5):1969–1973. https://doi.org/10.1073/pnas.91.5.1969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gnanasambandam A, Polkinghorne IG, Birch RG (2007) Heterologous signals allow efficient targeting of a nuclear-encoded fusion protein to plastids and endoplasmic reticulum in diverse plant species. Plant Biotechnol J 5(2):290–296. https://doi.org/10.1111/j.467-7652.2007.00241.x

    Article  PubMed  Google Scholar 

  78. Lee DW, Kim JK, Lee S, Choi S, Kim S, Hwang I (2008) Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20(6):1603–1622. https://doi.org/10.1105/tpc.108.060541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Primavesi LF, Wu H, Mudd EA, Day A, Jones HD (2008) Visualisation of plastids in endosperm, pollen and roots of transgenic wheat expressing modified GFP fused to transit peptides from wheat SSU RubisCO, rice FtsZ and maize ferredoxin III proteins. Transgenic Res 17(4):529–543. https://doi.org/10.1007/s11248-007-9126-7

    Article  CAS  PubMed  Google Scholar 

  80. MacMillan T (2013) Plant organelle targeting cell penetrating peptides. Ph.D. thesis, University of Lethbridge, Canada

    Google Scholar 

  81. Yoshizumi T, Oikawa K, Chuah JA, Kodama Y, Numata K (2018) Selective gene delivery for integrating exogenous DNA into plastid and mitochondrial genomes using peptide-DNA complexes. Biomacromolecules 19(5):1582–1591. https://doi.org/10.1021/acs.biomac.8b00323

    Article  CAS  PubMed  Google Scholar 

  82. Thagun C, Chuah JA, Numata K (2019) Targeted gene delivery into various plastids mediated by clustered cell-penetrating and chloroplast-targeting peptides. Adv Sci 6(23):1902064. https://doi.org/10.1002/advs.201902064

    Article  CAS  Google Scholar 

  83. Moller IM (2016) What is hot in plant mitochondria? Physiol Plant 157(3):256–263. https://doi.org/10.1111/ppl.12456

    Article  CAS  PubMed  Google Scholar 

  84. Farre JC, Araya A (2001) Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles. Nucleic Acids Res 29(12):2484–2491. https://doi.org/10.1093/nar/29.12.2484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Koulintchenko M, Konstantinov Y, Dietrich A (2003) Plant mitochondria actively import DNA via the permeability transition pore complex. EMBO J 22(6):1245–1254. https://doi.org/10.1093/emboj/cdg128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Tarasenko TA, Tarasenko VI, Koulintchenko MV, Klimenko ES, Konstantinov YM (2019) DNA import into plant mitochondria: complex approach for in organello and in vivo studies. Biochemistry 84(7):817–828. https://doi.org/10.1134/S0006297919070113

    Article  CAS  PubMed  Google Scholar 

  87. Fox TD, Sanford JC, McMullin TW (1988) Plasmids can stably transform yeast mitochondria lacking endogenous mtDNA. Proc Natl Acad Sci U S A 85:7288–7292. https://doi.org/10.1073/pnas.85.19.7288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Johnston S, Anziano P, Shark K, Sanford J, Butow R (1988) Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240:1538–1541. https://doi.org/10.1126/science.2836954

    Article  CAS  PubMed  Google Scholar 

  89. Randolph-Anderson BL, Boynton JE, Gillham NW, Harris EH, Johnson AM, Dorthu M-P, Matagne RF (1993) Further characterization of the respiratory deficient dum-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Mol Gen Genet 236:235–244. https://doi.org/10.1007/BF00277118

    Article  CAS  PubMed  Google Scholar 

  90. Remacle C, Cardol P, Coosemans N, Gaisne M, Bonnefoy N (2006) High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc Natl Acad Sci U S A 103(12):4771–4776. https://doi.org/10.1073/pnas.0509501103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Chuah JA, Yoshizumi T, Kodama Y, Numata K (2015) Gene introduction into the mitochondria of Arabidopsis thaliana via peptide-based carriers. Sci Rep 5:7751. https://doi.org/10.1038/srep07751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. MacMillan T, Ziemienowicz A, Jiang F, Eudes F, Kovalchuk I (2019) Gene delivery into the plant mitochondria via organelle-specific peptides. Plant Biotechnol Rep 13(1):11–23. https://doi.org/10.1007/s11816-018-0502-y

    Article  Google Scholar 

Download references

Acknowledgments

The A.S., J.L., and A.Z. authors thank Agriculture and Agri-Food Canada and Agriculture Funding Consortium (Alberta Innovates/Biosolutions, Alberta Wheat Commission and Saskatchewan Wheat Development Commission) for their financial support. A.B. thanks to Agriculture and Agri-Food Canada for New scientists support fund.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alicja Ziemienowicz .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Soliman, A., Laurie, J., Bilichak, A., Ziemienowicz, A. (2022). Applications of CPPs in Genome Editing of Plants. In: Langel, Ü. (eds) Cell Penetrating Peptides. Methods in Molecular Biology, vol 2383. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1752-6_39

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-1752-6_39

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-1751-9

  • Online ISBN: 978-1-0716-1752-6

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics