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Gene transfer to plants by electroporation: methods and applications

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Abstract

Developing gene transfer technologies enables the genetic manipulation of the living organisms more efficiently. The methods used for gene transfer fall into two main categories; natural and artificial transformation. The natural methods include the conjugation, transposition, bacterial transformation as well as phage and retroviral transductions, contain the physical methods whereas the artificial methods can physically alter and transfer genes from one to another organisms’ cell using, for instance, biolistic transformation, micro- and macroinjection, and protoplast fusion etc. The artificial gene transformation can also be conducted through chemical methods which include calcium phosphate-mediated, polyethylene glycol-mediated, DEAE-Dextran, and liposome-mediated transfers. Electrical methods are also artificial ways to transfer genes that can be done by electroporation and electrofusion. Comparatively, among all the above-mentioned methods, electroporation is being widely used owing to its high efficiency and broader applicability. Electroporation is an electrical transformation method by which transient electropores are produced in the cell membranes. Based on the applications, process can be either reversible where electropores in membrane are resealable and cells preserve the vitality or irreversible where membrane is not able to reseal, and cell eventually dies. This problem can be minimized by developing numerical models to iteratively optimize the field homogeneity considering the cell size, shape, number, and electrode positions supplemented by real-time measurements. In modern biotechnology, numerical methods have been used in electrotransformation, electroporation-based inactivation, electroextraction, and electroporative biomass drying. Moreover, current applications of electroporation also point to some other uncovered potentials for various exploitations in future.

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References

  1. Low LY, Yang SK, Kok DXA, Ong-Abdullah J, Tan NP, Lai KS (2018) Transgenic plants: gene constructs, vector and transformation method. New visions in plant science. IntechOpen, London, pp 43–62. https://doi.org/10.5772/intechopen.79369

    Book  Google Scholar 

  2. Saxena G, Kishor R, Saratale GD, Bharagava RN (2020) Genetically modified organisms (GMOs) and their potential in environmental management: constraints, prospects, and challenges. In: Bharagava R, Saxena G (eds) Bioremediation of industrial waste for environmental safety, Biological agents and methods for industrial waste management. Vol 2. Springer, Singapore, pp 1–19. https://doi.org/10.1007/978-981-13-3426-9_12

    Chapter  Google Scholar 

  3. Ahmad MM, Ali A, Siddiqui S, Kamaluddin M, Abdin MZ (2017) Methods in transgenic technology. In: Abdin MZ, Kiran U, Kamaluddin M, Ali A (eds) Plant biotechnology: principles and applications. Springer, Singapore, pp 93–115. https://doi.org/10.1007/978-981-10-2961-5_4

    Chapter  Google Scholar 

  4. Kaul T, Raman NM, Eswaran M, Thangaraj A, Sathelly KM, Kaul R, Yadava P, Agrawal PK (2019) Data mining by pluralistic approach on CRISPR gene editing in plants. Front Plant Sci 10:801. https://doi.org/10.3389/fpls.2019.00801

    Article  PubMed  PubMed Central  Google Scholar 

  5. Parray JA, Mir MY, Shameem N (2019) Plant genetic engineering and GM crops: merits and demerits. In: Parray JA, Mir MY, Shameem N (eds) Sustainable agriculture: biotechniques in plant biology. Springer, Singapore, pp 155–229. https://doi.org/10.1007/978-981-13-8840-8_4

    Chapter  Google Scholar 

  6. Yang Z, Wafula EK, Kim G, Shahid S, McNeal JR, Ralph PE, Timilsena PR, Yu W, Kelly EA, Zhang H, Person TN, Altman NS, Axtell MJ, Westwood JH, dePamphilis CW (2019) Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants. Nat Plants 5(9):991–1001. https://doi.org/10.1038/s41477-019-0458-0

    Article  CAS  PubMed  Google Scholar 

  7. Nishimura A (2020) Agrobacterium transformation in the rice genome. In: Vaschetto LM (ed) Cereal genomics. Humana, New York, pp 207–216. https://doi.org/10.1007/978-1-4939-9865-4

    Chapter  Google Scholar 

  8. Bhatia S, Dahiya R (2015) Concepts and techniques of plant tissue culture science. In: Bhatia S, Sharma K, Dahiya R, Bera T (eds) Modern applications of plant biotechnology in pharmaceutical sciences. Academic Press, Boston, pp 121–156. https://doi.org/10.1016/B978-0-12-802221-4.00004-2

    Chapter  Google Scholar 

  9. Cabezón E, Ripoll-Rozada J, Peña A, De La Cruz F, Arechaga I (2014) Towards an integrated model of bacterial conjugation. FEMS Microbiol Rev 39(1):81–95. https://doi.org/10.1111/1574-6976.12085

    Article  CAS  PubMed  Google Scholar 

  10. Bourgeois Y, Boissinot S (2019) On the population dynamics of junk: a review on the population genomics of transposable elements. Genes Basel 10(6):419. https://doi.org/10.3390/genes10060419

    Article  CAS  PubMed Central  Google Scholar 

  11. Ozyigit II (2012) Agrobacterium tumefaciens and its use in plant biotechnology. In: Ashraf M, Ozturk M, Ahmad MSA, Aksoy A (eds) Crop Production for agricultural improvement. Springer, Dordrecht, pp 317–361. https://doi.org/10.1007/978-94-007-4116-4

    Chapter  Google Scholar 

  12. Ozyigit II, Dogan I, Artam Tarhan E (2013) Agrobacterium rhizogenes-mediated transformation and its biotechnological applications in crops. In: Hakeem K, Ahmad P, Ozturk M (eds) Crop improvement. Springer, Boston, pp 1–48. https://doi.org/10.1007/978-1-4614-7028-1_1

    Chapter  Google Scholar 

  13. Johnston C, Martin B, Fichant G, Polard P, Claverys JP (2014) Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol 12:181–196. https://doi.org/10.1038/nrmicro3199

    Article  CAS  PubMed  Google Scholar 

  14. Goh S (2016) Phage transduction. In: Roberts A, Mullany P (eds) Clostridium difficile, Methods in molecular biology, vol 1476. Humana Press, New York, pp 177–185. https://doi.org/10.1007/978-1-4939-6361-4_131476

    Chapter  Google Scholar 

  15. Kaya Y, Yilmaz S, Gozukirmizi N, Huyop F (2013) Evaluation of transgenic Nicotiana tabacum with dehE gene using transposon based IRAP markers. Am J Plant Sci 48(8A):41–44. https://doi.org/10.4236/ajps.2013.48A005

    Article  CAS  Google Scholar 

  16. Cakmak Guner B, Karlik E, Marakli S, Gozukirmizi N (2018) Detection of HERV-K6 and HERV-K11 transpositions in the human genome. Biomed Rep 9(1):53–59. https://doi.org/10.3892/br.2018.1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ragupathi NKD, Sethuvel DPM, Gajendran R, Anandan S, Walia K, Veeraraghavan B (2019) Horizontal transfer of antimicrobial resistance determinants among enteric pathogens through bacterial conjugation. Curr Microbiol 76(6):666–672. https://doi.org/10.1007/s00284-019-01676-x

    Article  CAS  Google Scholar 

  18. Marakli S, Calis A, Gozukirmizi N (2019) Determination of barley-specific retrotransposons’ movements in Pinus nigra ssp. pallasiana varieties: Pyramidata and Seneriana. Russ J Genet 55(1):71–78. https://doi.org/10.1134/S1022795419010101

    Article  CAS  Google Scholar 

  19. Suh A (2019) Genome size evolution: small transposons with large consequences. Curr Biol 29(7):R241–R243. https://doi.org/10.1016/j.cub.2019.02.032

    Article  CAS  PubMed  Google Scholar 

  20. Borges RC, Rossato M, Albuquerque GMR, Ferreira MA, Brasileiro AC, Fonseca MEN, Boiteux LS (2019) Crown gall caused by Agrobacterium tumefaciens species complex: a novel nursery disease of Tectona grandis in Brazil. J Plant Pathol 101(2):445–445. https://doi.org/10.1007/s42161-018-00211-4

    Article  Google Scholar 

  21. Xu R, Li H, Qin R, Wang L, Li L, Wei P, Yang J (2014) Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice 7(1):5. https://doi.org/10.1186/s12284-014-0005-6

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hwang HH, Gelvin SB, Lai EM (2015) Editorial: “Agrobacterium biology and its application to transgenic plant production”. Front Plant Sci 6:265. https://doi.org/10.3389/fpls.2015.00265

    Article  PubMed  PubMed Central  Google Scholar 

  23. Brown-Jaque M, Calero-Cáceres W, Muniesa M (2015) Transfer of antibiotic-resistance genes via phage-related mobile elements. Plasmid 79:1–7. https://doi.org/10.1016/j.plasmid.2015.01.001

    Article  CAS  PubMed  Google Scholar 

  24. Gómez-Gómez C, Blanco-Picazo P, Brown-Jaque M, Quirós P, Rodríguez-Rubio L, Cerdà-Cuellar M, Muniesa M (2019) Infectious phage particles packaging antibiotic resistance genes found in meat products and chicken feces. Sci Rep 9(1):1–11. https://doi.org/10.1038/s41598-019-49898-0

    Article  CAS  Google Scholar 

  25. Smith TW, Nishimura MI (2020) Targeting cancer with genetically engineered TCR T cells. In: Theobald M (ed) Current immunotherapeutic strategies in cancer. Springer, Cham, pp 129–151. https://doi.org/10.1007/978-3-030-23765-3

    Chapter  Google Scholar 

  26. Davies KM, Deroles SC, Boase MR, Hunter DA, Schwinn KE (2013) Biolistics-based gene silencing in plants using a modified particle inflow gun. In: Sudowe S, Reske-Kunz A (eds) Biolistic DNA delivery. Humana Press, Totowa, pp 63–74. https://doi.org/10.1007/978-1-62703-110-3_6

    Chapter  Google Scholar 

  27. Wang H, Wang W, Zhan J, Huang W, Xu H (2015) An efficient PEG-mediated transient gene expression system in grape protoplasts and its application in subcellular localization studies of flavonoids biosynthesis enzymes. Sci Hortic 191:82–89. https://doi.org/10.1016/j.scienta.2015.04.039

    Article  CAS  Google Scholar 

  28. Rolong A, Davalos RV, Rubinsky B (2018) History of electroporation. In: Meijerink M, Scheffer HJ, Narayanan G (eds) Irreversible electroporation in clinical practice. Springer, Cham, pp 13–37. https://doi.org/10.1007/978-3-319-55113-5

    Chapter  Google Scholar 

  29. Montanari A, Bolotin-Fukuhara M, D’Orsi MF, De Luca C, Bianchi MM, Francisci S (2015) Biolistic transformation for delivering DNA into the mitochondria. In: van den Berg M, Maruthachalam K (eds) Genetic transformation systems in fungi, vol 1. Springer, Cham, pp 101–117. https://doi.org/10.1007/978-3-319-10142-2_101

    Chapter  Google Scholar 

  30. De la Pena A, Lörz H, Schell J (1987) Transgenic rye plants obtained by injecting DNA into young floral tillers. Nature 325(6101):274–276. https://doi.org/10.1038/325274a0

    Article  Google Scholar 

  31. Khan FA (2018) Biotechnology fundamentals, 2nd edn. CRC Press, Boca Raton FL, pp 1–696. ISBN 9780815370048

  32. Xu W (2019) Microinjection and micromanipulation: a historical perspective. In: Liu C, Du Y (eds) Microinjection, methods in molecular biology, vol 1874. Humana Press, New York, pp 1–16. https://doi.org/10.1007/978-1-4939-8831-0_11874

    Chapter  Google Scholar 

  33. Wang J, Jiang J, Wang Y (2013) Protoplast fusion for crop improvement and breeding in China. Plant Cell, Tissue Organ Cult 112:131–142. https://doi.org/10.1007/s11240-012-0221-y

    Article  Google Scholar 

  34. Klein TM, Arentzen R, Lewis PA, Fitzpatrick-McElligott S (1992) Transformation of microbes, plants and animals by particle bombardment. Nat Biotechnol 10:286–291. https://doi.org/10.1038/nbt0392-286

    Article  CAS  Google Scholar 

  35. Johnston SA, Tang D (1994) Gene gun transfection of animal cells and genetic immunization. In: Roth MG (ed) Methods in cell biology, vol 43. pp 353–365. https://doi.org/10.1016/s0091-679x(08)60612-3

  36. Lee JE, Yin Y, Lim SY, Kim ES, Jung J, Kim D, Park JW, Lee MS, Jeong JH (2019) Enhanced transfection of human mesenchymal stem cells using a hyaluronic acid/calcium phosphate hybrid gene delivery system. Polymers 11(5):798. https://doi.org/10.3390/polym11050798

    Article  CAS  PubMed Central  Google Scholar 

  37. Uchiumi F, Ohi H, Tanuma S (2014) Application of DEAE-dextran method to an efficient gene transfer system. Seikagaku 86(4):532–537

    PubMed  Google Scholar 

  38. Allen TM, Cullis PR (2013) Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev 65:36–48. https://doi.org/10.1016/j.addr.2012.09.037

    Article  CAS  PubMed  Google Scholar 

  39. Jin L, Zeng X, Liu M, Deng Y, He N (2014) Current progress in gene delivery technology based on chemical methods and nano-carriers. Theranostics 4:240–255. https://doi.org/10.7150/thno.6914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yu D, Wang A, Huang H, Chen Y (2008) PEG-PBLG nanoparticle-mediated HSV-TK/GCV gene therapy for oral squamous cell carcinoma. Nanomedicine 3:813–821. https://doi.org/10.2217/17435889.3.6.813

    Article  CAS  PubMed  Google Scholar 

  41. Moore NM, Sheppard CL, Sakiyama-Elbert SE (2009) Characterization of a multifunctional PEG-based gene delivery system containing nuclear localization signals and endosomal escape peptides. Acta Biomater 5:854–864. https://doi.org/10.1016/j.actbio.2008.09.009

    Article  CAS  PubMed  Google Scholar 

  42. Majzoub RN, Ewert KK, Safinya CR (2016) Cationic liposome-nucleic acid nanoparticle assemblies with applications in gene delivery and gene silencing. Philos Trans A Math Phys Eng Sci 374(2072):20150129. https://doi.org/10.1098/rsta.2015.0129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Van Wert SL, Saunders JA (1992) Electrofusion and electroporation of plants. Plant Physiol 99:365–367. https://doi.org/10.1104/pp.99.2.365

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kotnik T, Frey W, Sack M, Haberl Meglič S, Peterka M, Miklavčič D (2015) Electroporation-based applications in biotechnology. Trends Biotechnol 33:480–488. https://doi.org/10.1016/j.tibtech.2015.06.002

    Article  CAS  PubMed  Google Scholar 

  45. Kotnik T, Rems L, Tarek M, Miklavčič D (2019) Membrane electroporation and electropermeabilization: mechanisms and models. Annu Rev Biophys 48:63–91. https://doi.org/10.1146/annurev-biophys-052118-115451

    Article  CAS  PubMed  Google Scholar 

  46. Zhang HX, Zhang Y, Yin H (2019) Genome editing with mRNA encoding ZFN, TALEN and Cas9. Mol Ther 27(4):735–746. https://doi.org/10.1016/j.ymthe.2019.01.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Chen K, Gao C (2014) Targeted genome modification technologies and their applications in crop improvements. Plant Cell Rep 33:575–583. https://doi.org/10.1007/s00299-013-1539-6

    Article  CAS  PubMed  Google Scholar 

  48. Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14:49–55. https://doi.org/10.1038/nrm3486

    Article  CAS  Google Scholar 

  49. Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu JL, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617. https://doi.org/10.1038/ncomms12617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yarmush ML, Golberg A, Serša G, Kotnik T, Miklavčič D, (2014) Electroporation-based technologies for medicine: principles, applications, and challenges. Annu Rev Biomed Eng 16:295–320. https://doi.org/10.1146/annurev-bioeng-071813-104622

    Article  CAS  PubMed  Google Scholar 

  51. Kumar P, Nagarajan A, Uchil PD (2019) Electroporation. Cold Spring Harbor Protocols, Cold Spring Harbor Laboratory Press, pp 519–525. https://doi.org/10.1101/pdb.top096271

  52. Kotnik T, Kramar P, Pucihar G, Miklavcic D, Tarek M (2012) Cell membrane electroporation-Part 1: the phenomenon. IEEE Electr Insul Mag 28(5):14–23. https://doi.org/10.1109/MEI.2012.6268438

    Article  Google Scholar 

  53. Chen C, Smye SW, Robinson MP, Evans JA (2006) Membrane electroporation theories: a review. Med Bio Eng Comput 44(1–2):5–14. https://doi.org/10.1007/s11517-005-0020-2

    Article  CAS  Google Scholar 

  54. Mahnič-Kalamiza S, Kotnik T, Miklavčič D (2012) Educational application for visualization and analysis of electric field strength in multiple electrode electroporation. BMC Med Educ 12(1):102. https://doi.org/10.1186/1472-6920-12-102

    Article  PubMed  PubMed Central  Google Scholar 

  55. Vorobiev E, Lebovka N (2016) Pulsed electric energy assisted biorefinery of oil crops and residues. In: Miklavčič D (ed) Handbook of electroporation. Springer, Cham, pp 1–20. https://doi.org/10.1007/978-3-319-26779-1_159-1

    Chapter  Google Scholar 

  56. Kotnik T, Weaver JC (2016) Abiotic gene transfer: rare or rampant? J Membr Biol 249(5):623–631. https://doi.org/10.1007/s00232-016-9897-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kar S, Loganathan M, Dey K, Shinde P, Chang HY, Nagai M, Santra TS (2018) Single-cell electroporation: current trends, applications and future prospects. J Micromech Microeng 28:123002. https://doi.org/10.1088/1361-6439/aae5ae

    Article  CAS  Google Scholar 

  58. Faber KN, Harder W, Ab G, Veenhuis M (1995) Methylotrophic yeasts as factories for the production of foreign proteins. Yeast 11:1331–1344. https://doi.org/10.1002/yea.320111402

    Article  CAS  PubMed  Google Scholar 

  59. Brim H, Venkateswaran A, Kostandarithes HM, Fredrickson JK, Daly MJ (2003) Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments. Appl Environ Microbiol 69:4575–4582. https://doi.org/10.1128/AEM.69.8.4575-4582.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Li C, Corum L, Morgan D, Rosey E, Stanton T, Charon NW (2000) The spirochete FlaA periplasmic flagellar sheath protein impacts flagellar helicity. J Bacteriol 182:6698–6706. https://doi.org/10.1128/JB.182.23.6698-6706.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kámán-Tóth E, Pogány M, Dankó T, Szatmari A, Bozsó Z (2018) A simplified and efficient Agrobacterium tumefaciens electroporation method. 3 Biotech 8:148. https://doi.org/10.1007/s13205-018-1171-9

    Article  PubMed  PubMed Central  Google Scholar 

  62. Rieder A, Schwartz T, Schön-Hölz K, Marten SM, Süß J, Gusbeth C, Kohnen W, Swoboda W, Obst U, Freye W (2008) Molecular monitoring of inactivation efficiencies of bacteria during pulsed electric field treatment of clinical wastewater. J Appl Microbiol 105:2035–2045. https://doi.org/10.1111/j.1365-2672.2008.03972.x

    Article  CAS  PubMed  Google Scholar 

  63. Gusbeth CA, Frey W, Schwartz T, Rieder A (2009) Critical comparison between the pulsed electric field and thermal decontamination methods of hospital wastewater. Acta Phys Pol A 115:1092–1094. https://doi.org/10.12693/APhysPolA.115.1092

    Article  CAS  Google Scholar 

  64. Darwish A, Elgenedy MA, Finney SJ, Williams BW, Mcdonald JR (2019) A step-up modular high-voltage pulse generator based on isolated input-parallel/output-series voltage-boosting modules and modular multilevel submodules. IEEE Trans Ind Electron 66:2207–2216. https://doi.org/10.1109/TIE.2017.2772189

    Article  Google Scholar 

  65. Saulis G (2010) Electroporation of cell membranes: the fundamental effects of pulsed electric fields in food processing. Food Eng Rev 2:52–73. https://doi.org/10.1007/s12393-010-9023-3

    Article  Google Scholar 

  66. Mahnič-Kalamiza S, Vorobiev E, Miklavčič D (2014) Electroporation in good processing and biorefinery. J Membr Biol 247:1279–1304. https://doi.org/10.1007/s00232-014-9737-x

    Article  CAS  PubMed  Google Scholar 

  67. Sheng J, Vannela R, Rittmann BE (2012) Disruption of synechocystis PCC 6803 for lipid extraction. Water Sci Technol 65:567–573. https://doi.org/10.2166/wst.2012.879

    Article  CAS  PubMed  Google Scholar 

  68. Haberl S, Jarc M, Štrancar A, Peterka M, Hodžić D, Miklavčič D (2013) Comparison of alkaline lysis with electroextraction and optimization of electric pulses to extract plasmid dna from Escherichia coli. J Membr Biol 246:861–867. https://doi.org/10.1007/s00232-013-9580-5

    Article  CAS  PubMed  Google Scholar 

  69. Eing C, Goettel M, Straessner R, Gusbeth C, Frey W (2013) Pulsed electric field treatment of microalgae-benefits for microalgae biomass processing. IEEE Trans Plasma Sci 41:2901–2907. https://doi.org/10.1109/TPS.2013.2274805

    Article  CAS  Google Scholar 

  70. Vanthoor-Koopmans M, Wijffels RH, Barbosa MJ, Eppink MHM (2013) Biorefinery of microalgae for food and fuel. Bioresour Technol 135:142–149. https://doi.org/10.1016/j.biortech.2012.10.135

    Article  CAS  PubMed  Google Scholar 

  71. Nehmé R, Atieh C, Fayad S, Claude B, Chartier A, Tannoury M, Elleuch F, Abdelkafi S, Pichon C, Morin P (2017) Microalgae amino acid extraction and analysis at nanomolar level using electroporation and capillary electrophoresis with laser-induced fluorescence detection. J Sep Sci 40:558–566. https://doi.org/10.1002/jssc.201601005

    Article  CAS  PubMed  Google Scholar 

  72. Suga M, Hatakeyama T (2009) Gene transfer and protein release of fission yeast by application of a high voltage electric pulse. Anal Bioanal Chem 394:13–16. https://doi.org/10.1007/s00216-009-2678-z

    Article  CAS  PubMed  Google Scholar 

  73. Ganeva V, Galutzov B, Teissie J (2014) Evidence that pulsed electric field treatment enhances the cell wall porosity of yeast cells. Appl Biochem Biotechnol 172:1540–1552. https://doi.org/10.1007/s12010-013-0628-x

    Article  CAS  PubMed  Google Scholar 

  74. Puértolas E, Saldaña G, Condón S, Álvarez I, Raso J (2010) Evolution of polyphenolic compounds in red wine from Cabernet Sauvignon grapes processed by pulsed electric fields during aging in bottle. Food Chem 119:1063–1070. https://doi.org/10.1016/j.foodchem.2009.08.018

    Article  CAS  Google Scholar 

  75. Sack M, Sigler J, Eing C, Stukenbrock L, Stangle R, Wolf A, Muller G (2010) Operation of an electroporation device for grape mash. IEEE Trans Plasma Sci 38:1928–1934. https://doi.org/10.1109/TPS.2010.2050073

    Article  Google Scholar 

  76. Sack M, Eing C, Berghofe T, Buth L, Stangle R, Frey W, Bluhm H (2008) Electroporation-assisted dewatering as an alternative method for drying plants. IEEE Trans Plasma Sci 36:2577–2585. https://doi.org/10.1109/TPS.2008.2002440

    Article  CAS  Google Scholar 

  77. Reberšek M, Faurie C, Kandušer M, Čorović S, Teissié J, Rols MP, Miklavčič D (2007) Electroporator with automatic change of electric field direction improves gene electrotransfer in-vitro. Biomed Eng Online 6:25. https://doi.org/10.1186/1475-925X-6-25

    Article  PubMed  PubMed Central  Google Scholar 

  78. Bullmann T, Arendt T, Frey U, Hanashima C (2015) A transportable, inexpensive electroporator for in utero electroporation. Dev Growth Differ 57:369–377. https://doi.org/10.1111/dgd.12216

    Article  PubMed  Google Scholar 

  79. Escoffre JM, Portet T, Wasungu L, Teissié J, Dean DS, Rols MP (2009) What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues. Mol Biotechnol 41:286–295. https://doi.org/10.1007/s12033-008-9121-0

    Article  CAS  PubMed  Google Scholar 

  80. Siddiqui IA, Latouche EL, DeWitt MR, Swet J, Kirks RC, Baker EH, Iannitti DA, Vrochides D, Davalos RV, McKillop IH (2016) Induction of rapid, reproducible hepatic ablations using next-generation, high frequency irreversible electroporation (H-FIRE) in vivo. HPB (Oxford) 18:726–734. https://doi.org/10.1016/j.hpb.2016.06.015

    Article  Google Scholar 

  81. Hanze J, Fischer L, Koenen M, Worgall S, Rascher W (1998) Electroporation of nucleic acids into prokaryotic and eukaryotic cells by square wave pulses. Biotechnol Tech 12(2):159–163. https://doi.org/10.1023/A:1008800903452

    Article  CAS  Google Scholar 

  82. Rebersek M, Miklavcic D, Bertacchini C, Sack M (2014) Cell membrane electroporation-Part 3: the equipment. IEEE Electr Insul Mag 30(3):8–18. https://doi.org/10.1109/MEI.2014.6804737

    Article  Google Scholar 

  83. Weaver JC, Smith KC, Esser AT, Son RS, Gowrishankara TR (2012) A brief overview of electroporation pulse strength-duration space: a region where additional intracellular effects are expected. Bioelectrochemistry 87:236–243. https://doi.org/10.1016/j.bioelechem.2012.02.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kotnik T (2017) Lightning-triggered electroporation as a mechanism for horizontal gene transfer. In: Miklavčič D (ed) Handbook of electroporation. Springer, Cham, pp 369–385. https://doi.org/10.1007/978-3-319-32886-7_25

    Chapter  Google Scholar 

  85. Weaver JC, Chizmadzhev YA (1996) Theory of electroporation: a review. Bioelectrochem Bioenerg 41:135–160. https://doi.org/10.1016/S0302-4598(96)05062-3

    Article  CAS  Google Scholar 

  86. Bennett WFD, Sapay N, Tieleman DP (2014) Atomistic simulations of pore formation and closure in lipid bilayers. Biophys J 106:210–219. https://doi.org/10.1016/j.bpj.2013.11.4486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Sugar IP, Neumann E (1984) Stochastic model for electric field-induced membrane pores electroporation. Biophys Chem 19:211–225. https://doi.org/10.1016/0301-4622(84)87003-9

    Article  CAS  PubMed  Google Scholar 

  88. Kotnik T, Pucihar G, Miklavčič D (2010) Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport. J Membr Biol 236:3–13. https://doi.org/10.1007/s00232-010-9279-9

    Article  CAS  PubMed  Google Scholar 

  89. Flickinger B, Berghöfer T, Hohenberger P, Eing C, Frey W (2010) Transmembrane potential measurements on plant cells using the voltage-sensitive dye ANNINE-6. Protoplasma 247:3–12. https://doi.org/10.1007/s00709-010-0131-y

    Article  PubMed  Google Scholar 

  90. Pucihar G, Kotnik T, Kandušer M, Miklavčič D (2001) The influence of medium conductivity on electropermeabilization and survival of cells in vitro. Bioelectrochemistry 54:107–115. https://doi.org/10.1016/S1567-5394(01)00117-7

    Article  CAS  PubMed  Google Scholar 

  91. Baldwin WH, Gregory BW, Osgood CJ, Schoenbach KH, Kolb J (2010) Membrane permeability and cell survival after nanosecond pulsed-electric-field exposure-significance of exposure-media composition. IEEE Trans Plasma Sci 38:2948–2953. https://doi.org/10.1109/TPS.2010.2058129

    Article  Google Scholar 

  92. Markelc B, Čemažar M, Serša G (2017) Effects of reversible and irreversible electroporation on endothelial cells and tissue blood flow. In: Miklavčič D (ed) Handbook of electroporation. Springer, Cham, pp 607–620. https://doi.org/10.1007/978-3-319-32886-7_70

    Chapter  Google Scholar 

  93. Miklavčič D, Šemrov D, Mekid H, Mir LM (2000) A validated model of in vivo electric field distribution in tissues for electrochemotherapy and for DNA electrotransfer for gene therapy. Biochim Biophys Acta Gen Subj 1523(1):73–83. https://doi.org/10.1016/S0304-4165(00)00101-X

    Article  Google Scholar 

  94. Gurel F, Gozukirmizi N (2003) Electroporation transformation of barley. In: Jackson JF, Linskens HF (eds) Genetic transformation of plants, Molecular methods of plant analysis, vol 23 Springer, Berlin, pp 69–89. https://doi.org/10.1007/978-3-662-07424-4_523

    Chapter  Google Scholar 

  95. Dymek K, Rems L, Zorec B, Dejmek P, Galindo FG, Miklavčič D (2015) Modeling electroporation of the non-treated and vacuum impregnated heterogeneous tissue of spinach leaves. Innov Food Sci Emerg 29:55–64. https://doi.org/10.1016/j.ifset.2014.08.006

    Article  Google Scholar 

  96. Cukjati D, Batiuskaite D, André F, Miklavčič D, Mir LM (2007) Real time electroporation control for accurate and safe in vivo non-viral gene therapy. Bioelectrochemistry 70(2):501–507. https://doi.org/10.1016/j.bioelechem.2006.11.001

    Article  CAS  PubMed  Google Scholar 

  97. Pavliha D, Kos B, Marčan M, Zupanic A, Sersa G, Miklavčič D (2013) Planning of electroporation-based treatments using web-based treatment-planning software. J Membr Biol 246(11):833–842. https://doi.org/10.1007/s00232-013-9567-2

    Article  CAS  PubMed  Google Scholar 

  98. Kranjc M, Bajd F, Serša I, Miklavčič D (2014) Magnetic resonance electrical impedance tomography for measuring electrical conductivity during electroporation. Physiol Measur 35:985–996. https://doi.org/10.1088/0967-3334/35/6/985

    Article  CAS  Google Scholar 

  99. Aune TEV, Aachmann FL (2010) Methodologies to increase the transformation efficiencies and the range of bacteria that can be transformed. Appl Microbiol Biotechnol 85(5):1301–1313. https://doi.org/10.1007/s00253-009-2349-1

    Article  CAS  Google Scholar 

  100. Miller JF (1994) [30] Bacterial transformation by electroporation. In: Clark VL, Bavoil PM (eds) Methods in enzymology, vol 235. Academic Press, San Diego, pp 375–385. https://doi.org/10.1016/0076-6879(94)35156-2235

    Chapter  Google Scholar 

  101. Fournet-Fayard S, Joly B, Forestier C (1995) Transformation of wild type Klebsiella pneumoniae with plasmid DNA by electroporation. J Microbiol Methods 24(1):49–54. https://doi.org/10.1016/0167-7012(95)00053-4

    Article  Google Scholar 

  102. Dzul SP, Thornton MM, Hohne DN, Stewart EJ, Shah AA, Bortz DM, Solomon MJ, Younger JG (2011) Contribution of the Klebsiella pneumoniae capsule to bacterial aggregate and biofilm microstructures. Appl Environ Microbiol 77(5):1777–1782. https://doi.org/10.1128/AEM.01752-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Dower WJ, Miller JF, Ragsdale CW (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res 16:6127–6145. https://doi.org/10.1093/nar/16.13.6127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Kimoto H, Taketo A (1996) Studies on electrotransfer of DNA into Escherichia coli: effect of molecular form of DNA. Biochim Biophys Acta 1307:325–330. https://doi.org/10.1016/0167-4781(96)00027-9

    Article  PubMed  Google Scholar 

  105. Xie TD, Sun L, Tsong TY (1990) Study of mechanisms of electric field-induced DNA transfection. I. DNA entry by surface binding and diffusion through membrane pores. Biophys J 58(1):13–19. https://doi.org/10.1016/S0006-3495(90)82349-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Antonov PA, Maximova VA, Pancheva RP (1993) Heat shock and osmotically dependent steps by DNA uptake after Escherichia coli electroporation. Biochim Biophys Acta 1216:286–288. https://doi.org/10.1016/0167-4781(93)90155-7

    Article  CAS  PubMed  Google Scholar 

  107. Meddeb-Mouelhi F, Dulcey C, Beauregard M (2012) High transformation efficiency of Bacillus subtilis with integrative DNA using glycine betaine as osmoprotectant. Anal Biochem 424:127–129. https://doi.org/10.1016/j.ab.2012.01.032

    Article  CAS  PubMed  Google Scholar 

  108. Thompson JR, Register E, Curotto J, Kurtz M, Kelly R (1998) An improved protocol for the preparation of yeast cells for transformation by electroporation. Yeast 14(6):565–571. https://doi.org/10.1002/(SICI)1097-0061(19980430)14:6%3c565:AID-YEA251%3e3.0.CO;2-B

    Article  CAS  PubMed  Google Scholar 

  109. Chand PK, Ochatt SJ, Rech EL, Power JB, Davey MR (1988) Electroporation stimulates plant regeneration from protoplasts of the woody medicinal species Solanum dulcamara L. J Exp Bot 39(9):1267–1274. https://doi.org/10.1093/jxb/39.9.1267

    Article  Google Scholar 

  110. Ochatt SJ, Chand PK, Rech EL, Davey MR, Power JB (1988) Electroporation-mediated improvement of plant regeneration from colt cherry (Prunus avium × pseudocerasus) protoplasts. Plant Sci 54(2):165–169. https://doi.org/10.1016/0168-9452(88)90096-9

    Article  Google Scholar 

  111. Joersbo M, Brunstedt J (1990) Direct gene transfer to plant protoplasts by electroporation by alternating, rectangular and exponentially decaying pulses. Plant Cell Rep 8(12):701–705. https://doi.org/10.1007/BF00272098

    Article  CAS  PubMed  Google Scholar 

  112. Manders G, Dos Santos AVP, Vaz FDU, Davey MR, Power JB (1992) Transient gene expression in electroporated protoplasts of Eucalyptus citriodora Hook. Plant Cell Tissue Organ 30(1):69–75. https://doi.org/10.1007/BF00040003

    Article  CAS  Google Scholar 

  113. Rathus C, Birch RG (1992) Stable transformation of callus from electroporated sugarcane protoplasts. Plant Sci 82(1):81–89. https://doi.org/10.1016/0168-9452(92)90010-J

    Article  CAS  Google Scholar 

  114. D’Halluin K, Bonne E, Bossut M, De Beuckeleer M, Leemans J (1992) Transgenic maize plants by tissue electroporation. Plant Cell 4(12):1495–1505. https://doi.org/10.1105/tpc.4.12.1495

    Article  PubMed  PubMed Central  Google Scholar 

  115. He DG, Mouradov A, Yang YM, Mouradova E, Scott KJ (1994) Transformation of wheat (Triticum aestivum L.) through electroporation of protoplasts. Plant Cell Rep 14(2–3):192–196. https://doi.org/10.1007/BF00233789

    Article  CAS  PubMed  Google Scholar 

  116. Arencibia A, Molina PR, de la Riva G, Selman-Housein G (1995) Production of transgenic sugarcane (Saccharum officinarum L.) plants by intact cell electroporation. Plant Cell Rep 14:305–309. https://doi.org/10.1007/BF00232033

    Article  CAS  PubMed  Google Scholar 

  117. Salmenkallio-Marttila M, Aspegren K, Åkerman S, Kurtén U, Mannonen L, Ritala A, Teeri TH, Kauppinen V (1995) Transgenic barley (Hordeum vulgare L.) by electroporation of protoplasts. Plant Cell Rep 15(3–4):301–304. https://doi.org/10.1007/BF00193741

    Article  CAS  PubMed  Google Scholar 

  118. Valat L, Toutain S, Courtois N, Gaire F, Decout E, Pinck L, Mauro MC, Burrus M (2000) GFLV replication in electroporated grapevine protoplasts. Plant Sci 155(2):203–212. https://doi.org/10.1016/S0168-9452(00)00220-X

    Article  CAS  PubMed  Google Scholar 

  119. Li ST, Yang HY (2000) Gene transfer into isolated and cultured tobacco zygotes by a specially designed device for electroporation. Plant Cell Rep 19(12):1184–1187. https://doi.org/10.1007/s002990000249

    Article  CAS  PubMed  Google Scholar 

  120. Gurel F, Gozukirmizi N (2000) Optimization of gene transfer into barley (Hordeum vulgare L.) mature embryos by tissue electroporation. Plant Cell Rep 19(8):787–791. https://doi.org/10.1007/s002999900182

    Article  CAS  PubMed  Google Scholar 

  121. He GY, Lazzeri PA, Cannell ME (2001) Fertile transgenic plants obtained from Tritordeum inflorescences by tissue electroporation. Plant Cell Rep 20:67–72. https://doi.org/10.1007/s002990000285

    Article  CAS  PubMed  Google Scholar 

  122. Delaitre C, Ochatt S, Deleury E (2001) Electroporation modulates the embryogénie responses of asparagus (Asparagus officinalis L.) microspores. Protoplasma 216(1–2):39–46. https://doi.org/10.1007/BF02680129

    Article  CAS  PubMed  Google Scholar 

  123. Niedz RP, McKendree WL, Shatters RC (2003) Electroporation of embryogenic protoplasts of sweet orange (Citrus sinensis (L.) Osbeck) and regeneration of transformed plants. In Vitro Cell Dev Plant 39:586–594. https://doi.org/10.1079/IVP2003463

    Article  CAS  Google Scholar 

  124. Hassanein A, Hamama L, Loridon K, Dorion N (2009) Direct gene transfer study and transgenic plant regeneration after electroporation into mesophyll protoplasts of Pelargonium × hortorum, ‘Panaché Sud’. Plant Cell Rep 28:1521–1530. https://doi.org/10.1007/s00299-009-0751-x

    Article  CAS  PubMed  Google Scholar 

  125. Liu XZ, Li HL, Lou RH, Zhang YJ, Zhang HY (2010) Transgenic Pinus armandii plants containing BT obtained via electroporation of seed-derived embryos. Sci Res Essays 5(22):3443–3446

    Google Scholar 

  126. Wójcik A, Rybczyński JJ (2015) Electroporation and morphogenic potential of Gentiana kurroo (Royle) embryogenic cell suspension protoplasts. Biotechnologia 1(1):19–29. https://doi.org/10.5114/bta.2015.54170

    Article  Google Scholar 

  127. Furuhata Y, Sakai A, Murakami T, Morikawa M, Nakamura C, Yoshizumi T, Fujikura U, Nishida K, Kato Y (2019) A method using electroporation for the protein delivery of Cre recombinase into cultured Arabidopsis cells with an intact cell wall. Sci Rep 9(1):2163. https://doi.org/10.1038/s41598-018-38119-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Bonnassie S, Burini JF, Oreglia J, Trautwetter A, Patte JC, Sicard AM (1990) Transfer of plasmid DNA to Brevibacterium lactofermentum by electrotransformation. J Gen Microbiol 136(10):2107–2112. https://doi.org/10.1099/00221287-136-10-2107

    Article  CAS  PubMed  Google Scholar 

  129. Liebl W, Bayerl A, Schein B, Stillner U, Schleifer KH (1989) High efficiency electroporation of intact Corynebacterium glutamicum cells. FEMS Microbiol Lett 65(3):299–303. https://doi.org/10.1111/j.1574-6968.1989.tb03677.x

    Article  CAS  Google Scholar 

  130. Hermans J, Boschloo JG, De Bont JAM (1990) Transformation of Mycobacterium aurum by electroporation: the use of glycine, lysozyme and isonicotinic acid hydrazide in enhancing transformation efficiency. FEMS Microbiol Lett 72(1–2):221–224. https://doi.org/10.1111/j.1574-6968.1990.tb03892.x

    Article  CAS  Google Scholar 

  131. Ichimura M, Nakayama-Imaohji H, Wakimoto S, Morita H, Hayashi T, Kuwahara T (2010) Efficient electrotransformation of Bacteroides fragilis. Appl Environ Microbiol 76(10):3325–3332. https://doi.org/10.1128/AEM.02420-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Thomson AM, Flint HJ (1989) Electroporation induced transformation of Bacteroides ruminicola and Bacteroides uniformis by plasmid DNA. FEMS Microbiol Lett 61(1–2):101–104. https://doi.org/10.1111/j.1574-6968.1989.tb03560.x

    Article  CAS  Google Scholar 

  133. Ogata K, Aminov RI, Tajima K, Nakamura M, Matsui H, Nagamine T, Benno Y (1999) Construction of Prevotella ruminicola-Escherichia coli shuttle vector pRAM45 and transformation of P. ruminicola strains by electroporation. J Biosci Bioeng 88(3):316–318. https://doi.org/10.1016/S1389-1723(00)80016-X

    Article  CAS  PubMed  Google Scholar 

  134. Binet R, Maurelli AT (2009) Transformation and isolation of allelic exchange mutants of Chlamydia psittaci using recombinant DNA introduced by electroporation. Proc Natl Acad Sci USA 106(1):292–297. https://doi.org/10.1073/pnas.0806768106

    Article  PubMed  Google Scholar 

  135. Tam JE, Davis CH, Wyrick PB (1994) Expression of recombinant DNA introduced into Chlamydia trachomatis by electroporation. Can J Microbiol 40(7):583–591. https://doi.org/10.1139/m94-093

    Article  CAS  PubMed  Google Scholar 

  136. Kjærulff S, Diep DB, Okkels JS, Scheller HV, Ormerod JG (1994) Highly efficient integration of foreign DNA into the genome of the green sulfur bacterium, Chlorobium vibrioforme by homologous recombination. Photosynth Res 41(1):277–283. https://doi.org/10.1007/BF02184168

    Article  PubMed  Google Scholar 

  137. Toyomizu M, Suzuki K, Kawata Y, Kojima H, Akiba Y (2001) Effective transformation of the cyanobacterium Spirulina platensis using electroporation. J Appl Phycol 13(3):209–214. https://doi.org/10.1023/A:1011182613761

    Article  CAS  Google Scholar 

  138. Bruns BU, Briggs WR, Grossman AR (1989) Molecular characterization of phycobilisome regulatory mutants of Fremyella diplosiphon. J Bacteriol 171(2):901–908. https://doi.org/10.1128/jb.171.2.901-908.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Miyake M, Asada Y (1997) Direct electroporation of clostridial hydrogenase into cyanobacterial cells. Biotechnol Tech 11(11):787–790. https://doi.org/10.1023/A:1018417023074

    Article  CAS  Google Scholar 

  140. Chen T, Lian L, Mu Y, Yang Z (2010) Research on pprI gene of Deinococcus radiodurans transfered by electroporation in vivo for remedy of the γ-rays radiation injury with mice. J Radiat Res Radiat Process 28(3):166–171

    CAS  Google Scholar 

  141. de Grado M, Castán P, Berenguer J (1999) A high-transformation-efficiency cloning vector for Thermus thermophilus. Plasmid 42(3):241–245. https://doi.org/10.1006/plas.1999.1427

    Article  CAS  PubMed  Google Scholar 

  142. Belliveau BH, Trevors JT (1989) Transformation of Bacillus cereus vegetative cells by electroporation. Appl Environ Microbiol 55(6):1649–1652. https://doi.org/10.1128/AEM.55.6.1649-1652.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Scott PT, Rood JI (1989) Electroporation-mediated transformation of lysostaphin-treated Clostridium perfringens. Gene 82(2):327–333. https://doi.org/10.1016/0378-1119(89)90059-0

    Article  CAS  PubMed  Google Scholar 

  144. Shepard BD, Gilmore MS (1995) Electroporation and efficient transformation of Enterococcus faecalis grown in high concentrations of glycine. In: Nickoloff JA (ed) Electroporation protocols for microorganisms, Methods in molecular biology, vol 47. Humana Press, Totowa, pp 217–226. https://doi.org/10.1385/0-89603-310-4:21747

    Chapter  Google Scholar 

  145. Kim YH, Han KS, Oh S, You S, Kim SH (2005) Optimization of technical conditions for the transformation of Lactobacillus acidophilus strains by electroporation. J Appl Microbiol 99(1):167–174. https://doi.org/10.1111/j.1365-2672.2005.02563.x

    Article  CAS  PubMed  Google Scholar 

  146. Aukrust TW, Brurberg MB, Nes IF (1995) Transformation of Lactobacillus by electroporation. In: Nickoloff JA (ed) Electroporation protocols for microorganisms, Methods in molecular biology, vol 47. Humana Press, Totowa, pp 201–208. https://doi.org/10.1385/0-89603-310-4:20147

    Chapter  Google Scholar 

  147. Shifang J, Yinyu W, Xinhua G, Liandong H (1998) The factors affected transformation efficiency of Lactobacillus by electroporation. Chin J Biotechnol. https://doi.org/10.13345/j.cjb.1998.04.014

    Article  Google Scholar 

  148. Park SF, Stewart GS (1990) High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94(1):129–132. https://doi.org/10.1016/0378-1119(90)90479-B

    Article  CAS  PubMed  Google Scholar 

  149. Suvorov A, Kok J, Venema G (1988) Transformation of group A streptococci by electroporation. FEMS Microbiol Lett 56(1):95–99. https://doi.org/10.1111/j.1574-6968.1988.tb03156.x

    Article  CAS  Google Scholar 

  150. Somkuti GA, Steinberg DH (1988) Genetic transformation of Streptococcus thermophilus by electroporation. Biochimie 70(4):579–585. https://doi.org/10.1016/0300-9084(88)90095-8

    Article  CAS  PubMed  Google Scholar 

  151. Haake SK, Yoder S, Gerardo SH (2006) Efficient gene transfer and targeted mutagenesis in Fusobacterium nucleatum. Plasmid 55(1):27–38. https://doi.org/10.1016/j.plasmid.2005.06.002

    Article  CAS  Google Scholar 

  152. Jogler M, Jogler C (2013) Toward the development of genetic tools for planctomycetes. In: Fuerst J (ed) Planctomycetes: cell structure, origins and biology. Humana Press, Totowa, pp 141–164. https://doi.org/10.1007/978-1-62703-502-6_6

    Chapter  Google Scholar 

  153. Rivas-Marín E, Canosa I, Santero E, Devos DP (2016) Development of genetic tools for the manipulation of the planctomycetes. Front Microbiol 7:914. https://doi.org/10.3389/fmicb.2016.00914

    Article  PubMed  PubMed Central  Google Scholar 

  154. Miller JF, Dower WJ, Tompkins LS (1988) High-voltage electroporation of bacteria: genetic transformation of Campylobacter jejuni with plasmid DNA. Proc Natl Acad Sci USA 85(3):856–860. https://doi.org/10.1073/pnas.85.3.856

    Article  CAS  PubMed  Google Scholar 

  155. Taketo A (1988) DNA transfection of Escherichia coli by electroporation. BBA Gene Struct Expr 949(3):318–324. https://doi.org/10.1016/0167-4781(88)90158-3

    Article  CAS  Google Scholar 

  156. Artiguenave F, Vilaginès R, Danglot C (1997) High-efficiency transposon mutagenesis by electroporation of a Pseudomonas fluorescens strain. FEMS Microbiol Lett 153(2):363–369. https://doi.org/10.1111/j.1574-6968.1997.tb12597.x

    Article  CAS  PubMed  Google Scholar 

  157. O'Callaghan D, Charbit A (1990) High efficiency transformation of Salmonella typhimurium and Salmonella typhi by electroporation. Mol Gen Genet 223(1):156–158. https://doi.org/10.1007/BF00315809

    Article  CAS  PubMed  Google Scholar 

  158. Ferri L, Gori A, Biondi EG, Mengoni A, Bazzicalupo M (2010) Plasmid electroporation of Sinorhizobium strains: the role of the restriction gene hsdR in type strain Rm1021. Plasmid 63(3):128–135. https://doi.org/10.1016/j.plasmid.2010.01.001

    Article  CAS  PubMed  Google Scholar 

  159. English RS, Jin S, Shively JM (1995) Use of electroporation to generate a Thiobacillus neapolitanus carboxysome mutant. Appl Environ Microbiol 61(9):3256–3260. https://doi.org/10.1128/AEM.61.9.3256-3260.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Conchas RF, Carniel E (1990) A highly efficient electroporation system for transformation of Yersinia. Gene 87(1):133–137. https://doi.org/10.1016/0378-1119(90)90505-L

    Article  CAS  PubMed  Google Scholar 

  161. Samuels DS (1995) Electrotransformation of the spirochete Borrelia burgdorferi. In: Nickoloff JA (ed) Electroporation protocols for microorganisms, Methods in molecular biology, vol 47. Humana Press, Totowa, pp 253–259. https://doi.org/10.1385/0-89603-310-4:253

    Chapter  Google Scholar 

  162. Hedreyda CT, Lee KK, Krause DC (1993) Transformation of Mycoplasma pneumoniae with Tn4001 by electroporation. Plasmid 30(2):170–175. https://doi.org/10.1006/plas.1993.1047

    Article  CAS  PubMed  Google Scholar 

  163. Vieille C, Hess JM, Kelly RM, Zeikus JG (1995) xylA cloning and sequencing and biochemical characterization of xylose isomerase from Thermotoga neapolitana. Appl Environ Microbiol 61(5):1867–1875. https://doi.org/10.1128/aem.61.5.1867-1875.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. McCarthy S, Ai C, Blum P (2018) Enhancement of Metallosphaera sedula bioleaching by targeted recombination and adaptive laboratory evolution. In: Gadd GM, Sariaslani S (eds) Advances in applied microbiology, vol 104. Academic Press, Cambridge, pp 135–165. https://doi.org/10.1016/bs.aambs.2018.03.002

    Chapter  Google Scholar 

  165. Deng L, Zhu H, Chen Z, Liang YX, She Q (2009) Unmarked gene deletion and host-vector system for the hyperthermophilic crenarchaeon Sulfolobus islandicus. Extremophiles 13(4):735. https://doi.org/10.1007/s00792-009-0254-2

    Article  CAS  PubMed  Google Scholar 

  166. Elferink MG, Schleper C, Zillig W (1996) Transformation of the extremely thermoacidophilic archaeon Sulfolobus solfataricus via a self-spreading vector. FEMS Microbiol Lett 137(1):31–35. https://doi.org/10.1016/0378-1097(96)00019-5

    Article  CAS  PubMed  Google Scholar 

  167. Patel GB, Nash JH, Agnew BJ, Sprott GD (1994) Natural and electroporation-mediated transformation of Methanococcus voltae protoplasts. Appl Environ Microbiol 60(3):903–907. https://doi.org/10.1128/AEM.60.3.903-907.1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Joannes C, Sipaut CS, Dayou J, Yasir SM, Mansa RF (2015) Review paper on cell membrane electroporation of microalgae using electric field treatment method for microalgae lipid extraction. IOP Conf Ser 78:012034. https://doi.org/10.1088/1757-899X/78/1/012034

    Article  CAS  Google Scholar 

  169. Goettel M, Eing C, Gusbeth C, Straessner R, Frey W (2013) Pulsed electric field assisted extraction of intracellular valuables from microalgae. Algal Res 2(4):401–408. https://doi.org/10.1016/j.algal.2013.07.004

    Article  Google Scholar 

  170. Shimogawara K, Fujiwara S, Grossman A, Usuda H (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148(4):1821–1828

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Liu L, Wang Y, Zhang Y, Chen X, Zhang P, Ma S (2013) Development of a new method for genetic transformation of the green alga Chlorella ellipsoidea. Mol Biotechnol 54(2):211–219. https://doi.org/10.1007/s12033-012-9554-3

    Article  CAS  PubMed  Google Scholar 

  172. Chow KC, Tung WL (1999) Electrotransformation of Chlorella vulgaris. Plant Cell Rep 18(9):778–780. https://doi.org/10.1007/s002990050660

    Article  CAS  Google Scholar 

  173. Sun Y, Yang Z, Gao X, Li Q, Zhang Q, Xu Z (2005) Expression of foreign genes in Dunaliella by electroporation. Mol Biotechnol 30(3):185–192. https://doi.org/10.1385/MB:30:3:185

    Article  CAS  PubMed  Google Scholar 

  174. Guo SL, Zhao XQ, Tang Y, Wan C, Alam MA, Ho SH, Bai F, Chang JS (2013) Establishment of an efficient genetic transformation system in Scenedesmus obliquus. J Biotechnol 163(1):61–68. https://doi.org/10.1016/j.jbiotec.2012.10.020

    Article  CAS  PubMed  Google Scholar 

  175. Li F, Gao D, Hu H (2014) High-efficiency nuclear transformation of the oleaginous marine Nannochloropsis species using PCR product. Biosci Biotechnol Biochem 78(5):812–817. https://doi.org/10.1080/09168451.2014.905184

    Article  CAS  PubMed  Google Scholar 

  176. Zhang C, Hu H (2014) High-efficiency nuclear transformation of the diatom Phaeodactylum tricornutum by electroporation. Mar Genom 16(1):63–66. https://doi.org/10.1016/j.margen.2013.10.003

    Article  CAS  Google Scholar 

  177. Ohnuma M, Yokoyama T, Inouye T, Sekine Y, Tanaka K (2008) Polyethylene glycol (PEG)-mediated transient gene expression in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 49(1):117–120. https://doi.org/10.1093/pcp/pcm157

    Article  CAS  PubMed  Google Scholar 

  178. De Backer MD, Maes D, Vandoninck S, Logghe M, Contreras R, Luyten WH (1999) Transformation of Candida albicans by electroporation. Yeast 15(15):1609–1618. https://doi.org/10.1002/(SICI)1097-0061(199911)15:15%3c1609:AID-YEA485%3e3.0.CO;2-Y

    Article  PubMed  Google Scholar 

  179. Kasüske A, Wedler H, Schulze S, Becher D (1992) Efficient electropulse transformation of intact Candida maltosa cells by different homologous vector plasmids. Yeast 8(9):691–697. https://doi.org/10.1002/yea.320080902

    Article  PubMed  Google Scholar 

  180. Stoyanov A, Petrova P, Lahtchev K (2014) Enhanced heterologous gene expression in diploid cells of methylotrophic yeast Hansenula (Ogataea) polymorpha. J Biosci Biotechnol 3(3):247–2526

    Google Scholar 

  181. Wu S, Letchworth GJ (2004) High efficiency transformation by electroporation of Pichia pastoris pretreated with lithium acetate and dithiothreitol. Biotechniques 36(1):152–154. https://doi.org/10.2144/04361DD02

    Article  CAS  PubMed  Google Scholar 

  182. Delorme E (1989) Transformation of Saccharomyces cerevisiae by electroporation. Appl Environ Microbiol 55(9):2242–2246. https://doi.org/10.1128/AEM.55.9.2242-2246.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Prentice HL (1992) High efficiency transformation of Schizosaccharomyces pombe by electroporation. Nucleic Acids Res 20(3):621. https://doi.org/10.1093/nar/20.3.621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Lin X, Chacko N, Wang L, Pavuluri Y (2014) Generation of stable mutants and targeted gene deletion strains in Cryptococcus neoformans through electroporation. Med Mycol 53(3):225–234. https://doi.org/10.1093/mmy/myu083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Morita T, Habe H, Fukuoka T, Imura T, Kitamoto D (2007) Convenient transformation of anamorphic basidiomycetous yeasts belonging to genus Pseudozyma induced by electroporation. J Biosci Bioeng 104(6):517–520. https://doi.org/10.1263/jbb.104.517

    Article  CAS  PubMed  Google Scholar 

  186. Neveu B, Belzile F, Bélanger RR (2007) Cloning of the glyceraldehyde-3-phosphate dehydrogenase gene from Pseudozyma flocculosa and functionality of its promoter in two Pseudozyma species. Antonie Van Leeuwenhoek J Microb 92(2):245–255. https://doi.org/10.1007/s10482-007-9160-8

    Article  CAS  Google Scholar 

  187. Lucas S, Toffin L, Zivanovic Y, Charlier D, Moussard H, Forterre P, Prieur D, Erauso G (2002) Construction of a shuttle vector for, and spheroplast transformation of, the hyperthermophilic archaeon Pyrococcus abyssi. Appl Environ Microbiol 68:5528–5536. https://doi.org/10.1128/AEM.68.11.5528-5536.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Panov PV, Akimov SA, Batishchev OV (2014) Isoprenoid lipid chains increase membrane resistance to pore formation. Biochem (Moscow) Suppl Ser A 8:304–308. https://doi.org/10.1134/S1990747814050067

    Article  Google Scholar 

  189. Polak A, Tarek M, Tomšič M, Valant J, Ulrih NP, Jamnik A, Kramar P, Miklavčič D (2014) Electroporation of archaeal lipid membranes using MD simulations. Bioelectrochemistry 100:18–26. https://doi.org/10.1016/j.bioelechem.2013.12.006

    Article  CAS  PubMed  Google Scholar 

  190. Sersa G, Bosnjak M, Cemazar M, Heller R (2016) Preclinical studies on electrochemotherapy. In: Miklavčič D (ed) Handbook of electroporation. Springer, Cham, pp 1511–1525. https://doi.org/10.1007/978-3-319-32886-7_45

    Chapter  Google Scholar 

  191. Orlowski S, Belehradek J Jr, Paoletti C, Mir LM (1988) Transient electropermeabilization of cells in culture: increase of the cytotoxicity of anticancer drugs. Biochem Pharmacol 37(24):4727–4733. https://doi.org/10.1016/0006-2952(88)90344-9

    Article  CAS  PubMed  Google Scholar 

  192. Bock J, Szabó I, Jekle A, Gulbins E (2002) Actinomycin D-induced apoptosis involves the potassium channel KV1.3. Biochem Biophys Res Commun 295(2):526–531. https://doi.org/10.1016/S0006-291X(02)00695-2

    Article  CAS  PubMed  Google Scholar 

  193. Sersa G, Jarm T, Kotnik T, Coer A, Podkrajsek M, Sentjurc M, Miklavčič D, Kadivec M, Kranjc S, Secerov A, Cemazar M (2008) Vascular disrupting action of electroporation and electrochemotherapy with bleomycin in murine sarcoma. Br J Cancer 98(2):388–398. https://doi.org/10.1038/sj.bjc.6604168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Souza C, Villarino NF, Farnsworth K, Black ME (2017) Enhanced cytotoxicity of bleomycin, cisplatin, and carboplatin on equine sarcoid cells following electroporation-mediated delivery in vitro. J Vet Pharmacol Ther 40(1):97–100. https://doi.org/10.1111/jvp.12331

    Article  CAS  PubMed  Google Scholar 

  195. Kranjc S, Cemazar M, Grosel A, Scancar J, Sersa G (2003) Electroporation of LPB sarcoma cells in vitro and tumors in vivo increases the radiosensitizing effect of cisplatin. Anticancer Res 23(1A):275–281

    CAS  PubMed  Google Scholar 

  196. Jaroszeski MJ, Dang V, Pottinger C, Hickey J, Gilbert R, Heller R (2000) Toxicity of anticancer agents mediated by electroporation in vitro. Anti-Cancer Drug 11(3):201–208. https://doi.org/10.1097/00001813-200003000-00008

    Article  CAS  Google Scholar 

  197. Vásquez JL, Gehl J, Hermann GG (2012) Electroporation enhances mitomycin C cytotoxicity on T24 bladder cancer cell line: a potential improvement of intravesical chemotherapy in bladder cancer. Bioelectrochemistry 88:127–133. https://doi.org/10.1016/j.bioelechem.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  198. Martin RCG II, McFarland K, Ellis S, Velanovich V (2012) Irreversible electroporation therapy in the management of locally advanced pancreatic adenocarcinoma. J Am Coll Surg 215(3):361–369. https://doi.org/10.1016/j.jamcollsurg.2012.05.021

    Article  PubMed  Google Scholar 

  199. Mitsui K, Taki T, Yamada Y, Honda N, Fukatsu H, Yoshikawa K (2000) In-vitro and in-vivo studies of the efficacy of electrochemotherapy for renal cell carcinoma. Int J Clin Oncol 5(5):303–307. https://doi.org/10.1007/PL00012054

    Article  Google Scholar 

  200. Wang J, Fang Q, Sun D, Chen J, Zhou X, Lin GW, Lu HZ, Fei J (2001) Genetic modification of hematopoietic progenitor cells for combined resistance to 4-hydroperoxycyclophosphamide, vincristine, and daunorubicin. Acta Pharmacol Sin 22(10):949–955

    CAS  PubMed  Google Scholar 

  201. Frandsen SK, Gibot L, Moinecha M, Gehl J, Rols MP (2015) Calcium electroporation: evidence for differential effects in normal and malignant cell lines, evaluated in a 3D spheroid model. PLoS ONE 10(12):e0144028. https://doi.org/10.1371/journal.pone.0144028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Broholm M, Stigaard T, Bulut M, Vogelsang R, Gögenur I, Gehl J (2019) Calcium electroporation for the treatment of colorectal cancer calcium endove-preliminary results. Eur J Surg Oncol 45(2):e119. https://doi.org/10.1016/j.ejso.2018.10.409

    Article  Google Scholar 

  203. Maresch R, Mueller S, Veltkamp C, Öllinger R, Friedrich M, Heid I, Steiger K, Weber J, Engleitner T, Barenboim M, Klein S, Louzada S, Banerjee R, Strong A, Stauber T, Gross N, Geumann U, Lange S, Ringelhan M, Varela I, Unger K, Yang F, Schmid RM, Vassiliou GS, Braren R, Schneider G, Heikenwalder M, Bradley A, Saur D, Rad R (2016) Multiplexed pancreatic genome engineering and cancer induction by transfection-based CRISPR/Cas9 delivery in mice. Nat Commun 7:10770. https://doi.org/10.1038/ncomms10770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  204. Tanihara F, Hirata M, Nguyen NT, Le QA, Hirano T, Takemoto T, Nakai M, Fuchimoto DI, Otoi T (2018) Generation of a TP53-modified porcine cancer model by CRISPR/Cas9-mediated gene modification in porcine zygotes via electroporation. PLoS ONE 13(10):e0206360. https://doi.org/10.1371/journal.pone.0206360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Agerholm-Larsen B, Iversen HK, Ibsen P, Moller JM, Mahmood F, Jensen KS, Gehl J (2011) Preclinical validation of electrochemotherapy as an effective treatment for brain tumors. Cancer Res 71:3753–3762. https://doi.org/10.1158/0008-5472.CAN-11-0451

    Article  CAS  PubMed  Google Scholar 

  206. Neal RE II, Singh R, Hatcher HC, Kock ND, Davalos RV (2010) Treatment of breast cancer through the application of irreversible electroporation using a novel minimally invasive single needle electrode. Breast Cancer Res Treat 123(1):295–301. https://doi.org/10.1007/s10549-010-0803-5

    Article  PubMed  PubMed Central  Google Scholar 

  207. Laufer S, Ivorra A, Reuter VE, Rubinsky B, Solomon SB (2010) Electrical impedance characterization of normal and cancerous human hepatic tissue. Physiol Meas 31(7):995–1009. https://doi.org/10.1088/0967-3334/31/7/009

    Article  PubMed  Google Scholar 

  208. Meijerink MR, Nilsson A, Narayanan G, Martin R (2018) Irreversible electroporation of pancreatic tumors. In: Meijerink MR, Scheffer HJ, Narayanan G (eds) Irreversible electroporation in clinical practice. Springer, Cham, pp 167–190. https://doi.org/10.1007/978-3-319-55113-5_11

    Chapter  Google Scholar 

  209. Guenther E, Klein N, Zapf S, Weil S, Schlosser C, Rubinsky B, Stehling MK (2019) Prostate cancer treatment with irreversible electroporation (IRE): safety, efficacy and clinical experience in 471 treatments. PLoS ONE 14(4):e0215093. https://doi.org/10.1371/journal.pone.0215093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Zhang HM, Yang H, Rech EL, Golds TJ, Davis AS, Mulligan BJ, Cocking EC, Davey MR (1988) Transgenic rice plants produced by electroporation-mediated plasmid uptake into protoplasts. Plant Cell Rep 7:379–384. https://doi.org/10.1007/BF00269517

    Article  CAS  PubMed  Google Scholar 

  211. Saunders JA, Smith CR, Kaper JM (1989) Effects of electroporation pulse wave on the incorporation of viral RNA into tobacco protoplasts. Biotechniques 7(10):1124–1131

    CAS  PubMed  Google Scholar 

  212. Tada Y, Sakamoto M, Fujimura T (1990) Efficient gene introduction into rice by electroporation and analysis of transgenic plants: use of electroporation buffer lacking chloride ions. Theor Appl Genet 80(4):475–480. https://doi.org/10.1007/BF00226748

    Article  CAS  PubMed  Google Scholar 

  213. Xu X, Li B (1994) Fertile transgenic Indica rice plants obtained by electroporation of the seed embryo cells. Plant Cell Rep 13(3):237–242. https://doi.org/10.1007/BF00239900

    Article  CAS  PubMed  Google Scholar 

  214. Asano Y, Ugaki M (1994) Transgenic plants of Agrostis alba obtained by electroporation-mediated direct gene transfer into protoplasts. Plant Cell Rep 13(5):243–246. https://doi.org/10.1007/BF00233312

    Article  CAS  PubMed  Google Scholar 

  215. Arencibia A, Gentinetta E, Cuzzoni E, Castiglione S, Kohli A, Vain P, Leech M, Christou P, Sala F (1998) Molecular analysis of the genome of transgenic rice (Oryza sativa L.) plants produced via particle bombardment or intact cell electroporation. Mol Breed 4(2):99–109. https://doi.org/10.1023/A:1009627409668

    Article  CAS  Google Scholar 

  216. Arencibia AD, Carmona ER, Cornide MT, Castiglione S, O'Relly J, Chinea A, Oramas P, Sala F (1999) Somaclonal variation in insect-resistant transgenic sugarcane (Saccharum hybrid) plants produced by cell electroporation. Transgenic Res 8(5):349–360. https://doi.org/10.1023/A:1008900230144

    Article  CAS  Google Scholar 

  217. Quecini VM, Vieira MLC (2001) Transient gene expression in electroporated intact tissues of Stylosanthes guianensis (AUBL.) SW. Sci Agric 58(4):759–765. https://doi.org/10.1590/S0103-90162001000400018

    Article  CAS  Google Scholar 

  218. Haliloglu K, Baenziger PS, Mitra A (2004) Genetic transformation of wheat (Triticum aestivum L.) anther culture-derived embryos by electroporation. Biotechnol Biotechnol Equip 18(2):62–68. https://doi.org/10.1080/13102818.2004.10817088

    Article  CAS  Google Scholar 

  219. Unno H, Yamamoto S (2005) Introduction of exogenous substance into protoplasts of perennial ryegrass by electroporation. Grassl Sci 51(2):165–168. https://doi.org/10.1111/j.1744-697X.2005.00025.x

    Article  CAS  Google Scholar 

  220. Almeida AM, Villalobos E, Araújo SS, Cardoso LA, Santos DM, Santos MA, Fevereiro P, Torné JM (2007) Electroporation of maize embryogenic calli with the trehalose-6-phosphate synthase gene from Arabidopsis thaliana. Acta Physiol Plant 29(3):273–281. https://doi.org/10.1007/s11738-007-0034-5

    Article  CAS  Google Scholar 

  221. de García E, Villarroel C (2007) Transgenic plantain (cv.’harton’) plants resistant to herbicide basta obtained by electroporation. Acta Hortic 738(738):509–514. https://doi.org/10.17660/ActaHortic.2007.738.65

    Article  Google Scholar 

  222. Adesoye A, Machuka J, Togun A (2008) CRY 1AB transgenic cowpea obtained by nodal electroporation. Afr J Biotechnol 7(18):3200–3210. https://doi.org/10.5897/AJB08.324

    Article  CAS  Google Scholar 

  223. Haijin X, Rong D, Lamei Z, Dihong L, Caifeng G, Yanling B, Xiuming Z, Mingqiang Q (2012) Study on electroporation transformation of isolated cucumber mitochondria. Acta Sci Naturalium Universitatis Nankaiensis 18(6):100–103

    Google Scholar 

  224. Zhang XH, Zhao XJ, Li B, Li FF, Liu PX, Min DH (2013) Factors optimization of pollen electroporation transformation and identification of transgenic wheat. Sci Agric Sin 46(12):2403–2411. https://doi.org/10.3864/j.issn.0578-1752.2013.12.001

    Article  CAS  Google Scholar 

  225. Kwao S, Al-Hamimi S, Damas MEV, Rasmusson AG, Galindo FG (2016) Effect of guard cells electroporation on drying kinetics and aroma compounds of Genovese basil (Ocimum basilicum L.) leaves. Innov Food Sci Emerg Technol 38:15–23. https://doi.org/10.1016/j.ifset.2016.09.011

    Article  CAS  Google Scholar 

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Acknowledgements

Author is grateful to Bio-Rad Laboratories for providing the original pictures of Gene Pulser Xcell™ Electroporation System and its accessories, thankful to Dr. Yilmaz Kaya for rechecking the document, Dr. Fatma Yanik, Biologist MSc. Asli Hocaoglu-Ozyigit, and Ahmet Yilmaz for their technical supports.

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  1. Department of Biology, Faculty of Science and Arts, Marmara University, Goztepe, 34722, Istanbul, Turkey

    Ibrahim Ilker Ozyigit

  2. Department of Biology, Faculty of Science, Kyrgyz-Turkish Manas University, 720038, Bishkek, Kyrgyzstan

    Ibrahim Ilker Ozyigit

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Ozyigit, I.I. Gene transfer to plants by electroporation: methods and applications. Mol Biol Rep 47, 3195–3210 (2020). https://doi.org/10.1007/s11033-020-05343-4

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