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A Short History and Perspectives on Plant Genetic Transformation

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Biolistic DNA Delivery in Plants

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2124))

Abstract

Plant genetic transformation is an important technological advancement in modern science, which has not only facilitated gaining fundamental insights into plant biology but also started a new era in crop improvement and commercial farming. However, for many crop plants, efficient transformation and regeneration still remain a challenge even after more than 30 years of technical developments in this field. Recently, FokI endonuclease-based genome editing applications in plants offered an exciting avenue for augmenting crop productivity but it is mainly dependent on efficient genetic transformation and regeneration, which is a major roadblock for implementing genome editing technology in plants. In this chapter, we have outlined the major historical developments in plant genetic transformation for developing biotech crops. Overall, this field needs innovations in plant tissue culture methods for simplification of operational steps for enhancing the transformation efficiency. Similarly, discovering genes controlling developmental reprogramming and homologous recombination need considerable attention, followed by understanding their role in enhancing genetic transformation efficiency in plants. Further, there is an urgent need for exploring new and low-cost universal delivery systems for DNA/RNA and protein into plants. The advancements in synthetic biology, novel vector systems for precision genome editing and gene integration could potentially bring revolution in crop-genetic potential enhancement for a sustainable future. Therefore, efficient plant transformation system standardization across species holds the key for translating advances in plant molecular biology to crop improvement.

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References

  1. Schleiden MJ (1838) Beiträge zur phytogenesis. Arch Anat Physiol Wiss Med (J Müller) 1838:137–176

    Google Scholar 

  2. Schwann T (1910) Mikroskopische Untersuchungen über die Übereinstimmung in der Struktur und dem Wachstume der Tiere und Pflanzen. Oswalds Klassiker der Exakten Wissenschaften 176:242

    Google Scholar 

  3. Griffith F (1928) The significance of pneumococcal types. Epidemiol Infect 27:113–159

    CAS  Google Scholar 

  4. Haberlandt G (1969) Experiments on the culture of isolated plant cells. Bot Rev 35:68–88

    Article  Google Scholar 

  5. Gautheret R (1939) Sur la possibilité de réaliser la culture indéfinie des tissus de tubercules de carotte. CR Hebd Seances Acad Sc 208:118–120

    Google Scholar 

  6. White PR (1939) Potentially unlimited growth of excised plant callus in an artificial nutrient. Am J Bot 26:59–64

    Article  Google Scholar 

  7. Nobécourt P (1939) Sur la pérennité et l’augmentation de volume des cultures de tissues végétaux. CR Seances Soc Biol Ses Fil 130:1270–1271

    Google Scholar 

  8. Ball E (1946) Development in sterile culture of stem tips and subjacent regions of Tropaeolum majus L. and of Lupinus albus L. Am J Bot 33:301–318

    Article  Google Scholar 

  9. Muir W, Hildebrandt A, Riker A (1954) Plant tissue cultures produced from single isolated cells. Science 119:877–878

    Article  Google Scholar 

  10. Muir W, Hildebrandt A, Riker A (1958) The preparation, isolation, and growth in culture of single cells from higher plants. Am J Bot 45:589–597

    Article  Google Scholar 

  11. Skoog F, Miller C (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130

    CAS  PubMed  Google Scholar 

  12. Steward F, Mapes MO, Smith J (1958) Growth and organized development of cultured cells I. Growth and division of freely suspended cells. Am J Bot 45:693–703

    Article  Google Scholar 

  13. Steward F, Mapes MO, Mears K (1958) Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cell. Am J Bot 45:705–708

    Article  Google Scholar 

  14. Steward F, Pollard J (1958) 14C-Proline and hydroxyproline in the protein metabolism of plants: An episode in the relation of metabolism to cell growth and morphogenesis. Nature 182:828

    Article  CAS  PubMed  Google Scholar 

  15. Guha S, Maheshwari SC (1966) Cell division and differentiation of embryos in the pollen grains of Datura in vitro. Nature 212:97

    Article  Google Scholar 

  16. Carlson PS, Smith HH, Dearing RD (1972) Parasexual interspecific plant hybridization. Proc Natl Acad Sci U S A 69:2292–2294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Smith HO, Welcox K (1970) A restriction enzyme from Hemophilus influenzae: I Purification and general properties. J Mol Bio 51:379–391

    Article  CAS  Google Scholar 

  18. Kelly TJ Jr, Smith HO (1970) A restriction enzyme from Hemophilus influenzae: II. Base sequence of the recognition site. J Mol Biol 51:393–409

    Article  CAS  PubMed  Google Scholar 

  19. Danna K, Nathans D (1971) Specific cleavage of simian virus 40 DNA by restriction endonuclease of Hemophilus influenzae. Proc Natl Acad Sci U S A 68:2913–2917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Smith HO, Nathans D (1973) A suggested nomenclature for bacterial host modification and restriction systems and their enzymes. J Mol Biol 81:419–423

    Article  CAS  PubMed  Google Scholar 

  21. Jackson DA, Symons RH, Berg P (1992) Biochemical method for inserting new genetic information into DNA of Simian Virus 40: circular SV40 DNA molecules containing lambda phage genes and the galactose operon of Escherichia coli. Proc Natl Acad Sci U S A 69:2904–2909

    Article  Google Scholar 

  22. Cohen SN, Chang AC, Boyer HW, Helling RB (1973) Construction of biologically functional bacterial plasmids in vitro. Proc Natl Acad Sci U S A 70:3240–3244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. O'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021

    CAS  PubMed  Google Scholar 

  24. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  26. Mullis K, Faloona F, Scharf S, Saiki R, Horn G, Erlich H (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol 51(Pt 1):263–273

    Article  CAS  PubMed  Google Scholar 

  27. Mullis KB, Faloona FA (1987) Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol 155:335–350

    Article  CAS  PubMed  Google Scholar 

  28. Smith EF, Townsend CO (1907) A plant-tumor of bacterial origin. Science 25:671–673

    Article  CAS  PubMed  Google Scholar 

  29. White PR, Braun AC (1941) Crown gall production by bacteria-free tumor tissues. Science 94:239–241

    Article  CAS  PubMed  Google Scholar 

  30. Braun AC (1958) A physiological basis for autonomous growth of the crown-gall tumor cell. Proc Natl Acad Sci U S A 44:344–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Zaenen I, Van Larebeke N, Teuchy H, Van Montagu M, Schell J (1974) Supercoiled circular DNA in crown-gall inducing Agrobacterium strains. J Mol Biol 86:109–127

    Article  CAS  PubMed  Google Scholar 

  32. Chilton M-D, Drummond MH, Merlo DJ, Sciaky D, Montoya AL, Gordon MP, Nester EW (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263–271

    Article  CAS  PubMed  Google Scholar 

  33. Lemmers M, De Beuckeleer M, Holsters M, Zambryski P, Depicker A, Hernalsteens J-P, Van Montagu M, Schell J (1980) Internal organization, boundaries and integration of Ti-plasmid DNA in nopaline crown gall tumours. J Mol Biol 144:353–376

    Article  CAS  PubMed  Google Scholar 

  34. Thomashow MF, Nutter R, Montoya AL, Gordon MP, Nester EW (1980) Integration and organization of Ti plasmid sequences in crown gall tumors. Cell 19:729–739

    Article  CAS  PubMed  Google Scholar 

  35. Zambryski P, Holsters M, Kruger K, Depicker A, Schell J, Van Montagu M, Goodman HM (1980) Tumor DNA structure in plant cells transformed by A. tumefaciens. Science 209:1385–1391

    Article  CAS  PubMed  Google Scholar 

  36. Drummond MH, Gordon MP, Nester EW, Chilton M-D (1977) Foreign DNA of bacterial plasmid origin is transcribed in crown gall tumours. Nature 269:535–536

    Article  CAS  Google Scholar 

  37. Gelvin SB, Gordon MP, Nester EW, Aronson AI (1981) Transcription of the Agrobacterium Ti plasmid in the bacterium and in crown gall tumors. Plasmid 6:17–29

    Article  CAS  PubMed  Google Scholar 

  38. Hoekema A, Hirsch PR, Hooykaas PJ, Schilperoort RA (1983) A binary plant vector strategy based on separation of vir-and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179–180

    Article  CAS  Google Scholar 

  39. Herrera-Estrella L, Depicker A, Van Montagu M, Schell J (1983) Expression of chimaeric genes transferred into plant cells using a Ti-plasmid-derived vector. Nature 303:209–213

    Article  CAS  Google Scholar 

  40. Fraley RT, Rogers SG, Horsch RB, Sanders PR, Flick JS, Adams SP, Bittner ML, Brand LA, Fink CL, Fry JS, Galluppi GR, Goldberg SB, Hoffmann NL, Woo SC (1983) Expression of bacterial genes in plant cells. Proc Natl Acad Sci U S A 80:4803–4807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Escobar MA, Dandekar AM (2003) Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci 8:380–386

    Article  CAS  PubMed  Google Scholar 

  42. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  CAS  PubMed  Google Scholar 

  43. Chateau S, Sangwan RS, Sangwan-Norreel BS (2000) Competence of Arabidopsis thaliana genotypes and mutants for Agrobacterium tumefaciens-mediated gene transfer: role of phytohormones. J Exp Bot 51:1961–1968

    Article  CAS  PubMed  Google Scholar 

  44. Hooykaas-Van Slogteren G, Hooykaas P, Schilperoort R (1984) Expression of Ti plasmid genes in monocotyledonous plants infected with Agrobacterium tumefaciens. Nature 311:763–764

    Article  CAS  Google Scholar 

  45. Kumar SV, Misquitta RW, Reddy VS, Rao BJ, Rajam MV (2004) Genetic transformation of the green alga—Chlamydomonas reinhardtii by Agrobacterium tumefaciens. Plant Sci 166:731–738

    Article  CAS  Google Scholar 

  46. Bundock P, den Dulk-Ras A, Beijersbergen A, Hooykaas P (1995) Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14:3206–3214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. De Groot MJ, Bundock P, Hooykaas PJ, Beijersbergen AG (1998) Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat Biotechnol 16:839–842

    Article  PubMed  Google Scholar 

  48. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V (2001) Genetic transformation of HeLa cells by Agrobacterium. Proc Natl Acad Sci U S A 98:1871–1876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Szeto W, Hamer D, Carlson P, Thomas C (1977) Cloning of cauliflower mosaic virus (CLMV) DNA in Escherichia coli. Science 196:210–212

    Article  CAS  PubMed  Google Scholar 

  50. Hull R (1978) The possible use of plant viral DNAs in genetic manipulation in plants. Trends Biochem Sci 3:254–256

    Article  CAS  Google Scholar 

  51. Howell SH, Walker LL, Dudley R (1980) Cloned cauliflower mosaic virus DNA infects turnips (Brassica rapa). Science 208:1265–1267

    Article  CAS  PubMed  Google Scholar 

  52. Grimsley N, Hohn B, Hohn T, Walden R (1986) “Agroinfection,” an alternative route for viral infection of plants by using the Ti plasmid. Proc Natl Acad Sci U S A 83:3282–3286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Grimsley N, Hohn T, Davies JW, Hohn B (1987) Agrobacterium-mediated delivery of infectious maize streak virus into maize plants. Nature 325:177–179

    Article  CAS  Google Scholar 

  54. Leiser R, Ziegler-Graff V, Reutenauer A, Herrbach E, Lemaire O, Guilley H, Richards K, Jonard G (1992) Agroinfection as an alternative to insects for infecting plants with beet western yellows luteovirus. Proc Natl Acad Sci U S A 89:9136–9140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Robertson D (2004) VIGS vectors for gene silencing: many targets, many tools. Annu Rev Plant Biol 55:495–519

    Article  CAS  PubMed  Google Scholar 

  56. Becker A, Lange M (2010) VIGS–genomics goes functional. Trends Plant Sci 15:1–4

    Article  CAS  PubMed  Google Scholar 

  57. Sanford JC, Klein TM, Wolf ED, Allen N (1987) Delivery of substances into cells and tissues using a particle bombardment process. Particulate Sci Technol 5:27–37

    Article  CAS  Google Scholar 

  58. Klein TM, Wolf ED, Wu R, Sanford J (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327:70–73

    Article  CAS  Google Scholar 

  59. Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dessaux Y, Petit A, Tempé J (1992) Opines in Agrobacterium biology. Molecular signals in plant-microbe communications. CRC Press, Inc, Boca Raton, FL, pp 109–136

    Google Scholar 

  61. Hooykaas PJ, Beijersbergen AG (1994) The virulence system of Agrobacterium tumefaciens. Annu Rev Phytopathol 32:157–181

    Article  CAS  Google Scholar 

  62. Allardet-Servent A, Michaux-Charachon S, Jumas-Bilak E, Karayan L, Ramuz M (1993) Presence of one linear and one circular chromosome in the Agrobacterium tumefaciens C58 genome. J Bacteriol 175:7869–7874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, Goldman BS, Cao Y, Askenazi M, Halling C, Mullin L, Houmiel K, Gordon J, Vaudin M, Iartchouk O, Epp A, Liu F, Wollam C, Allinger M, Doughty D, Scott C, Lappas C, Markelz B, Flanagan C, Crowell C, Gurson J, Lomo C, Sear C, Strub G, Cielo C, Slater S (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323–2328

    Article  CAS  PubMed  Google Scholar 

  64. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almeida NF Jr, Woo L, Chen Y, Paulsen IT, Eisen JA, Karp PD, Bovee D Sr, Chapman P, Clendenning J, Deatherage G, Gillet W, Grant C, Kutyavin T, Levy R, Li MJ, McClelland E, Palmieri A, Raymond C, Rouse G, Saenphimmachak C, Wu Z, Romero P, Gordon D, Zhang S, Yoo H, Tao Y, Biddle P, Jung M, Krespan W, Perry M, Gordon-Kamm B, Liao L, Kim S, Hendrick C, Zhao ZY, Dolan M, Chumley F, Tingey SV, Tomb JF, Gordon MP, Olson MV, Nester EW (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317–2323

    Article  CAS  PubMed  Google Scholar 

  65. Stachel SE, Nester EW (1986) The genetic and transcriptional organization of the vir region of the A6 Ti plasmid of Agrobacterium tumefaciens. EMBO J 5:1445–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Gelvin SB (1998) The introduction and expression of transgenes in plants. Curr Opin Biotechnol 9:227–232

    Article  CAS  PubMed  Google Scholar 

  67. Eckardt NA (2004) Host proteins guide Agrobacterium-mediated plant transformation. Plant Cell 16:2837–2839

    Article  CAS  PubMed Central  Google Scholar 

  68. Sheng J, Citovsky V (1996) Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8:1699–1710

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Baron C, Zambryski PC (1996) Plant transformation: a pilus in Agrobacterium T-DNA transfer. Curr Biol 6:1567–1569

    Article  CAS  PubMed  Google Scholar 

  70. Zhu J, Oger PM, Schrammeijer B, Hooykaas PJ, Farrand SK, Winans SC (2000) The bases of crown gall tumorigenesis. J Bacteriol 182:3885–3895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Subramoni S, Nathoo N, Klimov E, Yuan Z-C (2014) Agrobacterium tumefaciens responses to plant-derived signaling molecules. Front Plant Sci 5:322

    Article  PubMed  PubMed Central  Google Scholar 

  72. Shimoda N, Toyoda-Yamamoto A, Aoki S, Machida Y (1993) Genetic evidence for an interaction between the VirA sensor protein and the ChvE sugar-binding protein of Agrobacterium. J Biol Chem 268:26552–26558

    CAS  PubMed  Google Scholar 

  73. Pollard TD, Cooper JA (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 55:987–1035

    Article  CAS  PubMed  Google Scholar 

  74. Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kalogeraki VS, Zhu J, Eberhard A, Madsen EL, Winans SC (1999) The phenolic vir gene inducer ferulic acid is O-demethylated by the VirH2 protein of an Agrobacterium tumefaciens Ti plasmid. Mol Microbiol 34:512–522

    Article  CAS  PubMed  Google Scholar 

  76. Brencic A, Eberhard A, Winans SC (2004) Signal quenching, detoxification and mineralization of vir gene-inducing phenolics by the VirH2 protein of Agrobacterium tumefaciens. Mol Microbiol 51:1103–1115

    Article  CAS  PubMed  Google Scholar 

  77. Li L, Jia Y, Hou Q, Charles TC, Nester EW, Pan SQ (2002) A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid. Proc Natl Acad Sci U S A 99:12369–12374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Zupan JR, Zambryski P (1995) Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol 107:1041–1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Toro N, Datta A, Carmi O, Young C, Prusti R, Nester E (1989) The Agrobacterium tumefaciens virC1 gene product binds to overdrive, a T-DNA transfer enhancer. J Bacteriol 171:6845–6849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Tzfira T, Rhee Y, Chen M-H, Kunik T, Citovsky V (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Ann Rev Microbiol 54:187–219

    Article  CAS  Google Scholar 

  81. Deng W, Chen L, Peng WT, Liang X, Sekiguchi S, Gordon MP, Comai L, Nester EW (1999) VirE1 is a specific molecular chaperone for the exported single-stranded-DNA-binding protein VirE2 in Agrobacterium. Mol Microbiol 31:1795–1807

    Article  CAS  PubMed  Google Scholar 

  82. Christie PJ, Whitaker N, González-Rivera C (2014) Mechanism and structure of the bacterial type IV secretion systems. Biochim Biophys Acta 1843:1578–1591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Atmakuri K, Cascales E, Christie PJ (2004) Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54:1199–1211

    Article  CAS  PubMed  Google Scholar 

  84. Zupan J, Hackworth CA, Aguilar J, Ward D, Zambryski P (2007) VirB1∗ promotes T-pilus formation in the vir-Type IV secretion system of Agrobacterium tumefaciens. J Bacteriol 189:6551–6563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CM, Regensburg-Tuïnk TJ, Hooykaas PJ (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:979–982

    Article  CAS  PubMed  Google Scholar 

  86. Vergunst AC, van Lier MC, den Dulk-Ras A, Hooykaas PJ (2003) Recognition of the Agrobacterium tumefaciens VirE2 translocation signal by the VirB/D4 transport system does not require VirE1. Plant Physiol 133:978–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Vergunst AC, van Lier MC, den Dulk-Ras A, Stüve TAG, Ouwehand A, Hooykaas PJ (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci U S A 102:832–837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Duckely M, Hohn B (2003) The VirE2 protein of Agrobacterium tumefaciens: the Yin and Yang of T-DNA transfer. FEMS Microbiol Lett 223:1–6

    Article  CAS  PubMed  Google Scholar 

  89. Ballas N, Citovsky V (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc Natl Acad Sci U S A 94:10723–10728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Deng W, Chen L, Wood DW, Metcalfe T, Liang X, Gordon MP, Comai L, Nester EW (1998) Agrobacterium VirD2 protein interacts with plant host cyclophilins. Proc Natl Acad Sci U S A 95:7040–7045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Bako L, Umeda M, Tiburcio AF, Schell J, Koncz C (2003) The VirD2 pilot protein of Agrobacterium-transferred DNA interacts with the TATA box-binding protein and a nuclear protein kinase in plants. Proc Natl Acad Sci U S A 100:10108–10113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Rossi L, Hohn B, Tinland B (1996) Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 93:126–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Tzfira T, Vaidya M, Citovsky V (2001) VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J 20:3596–3607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Lacroix B, Vaidya M, Tzfira T, Citovsky V (2005) The VirE3 protein of Agrobacterium mimics a host cell function required for plant genetic transformation. EMBO J 24:428–437

    Article  CAS  PubMed  Google Scholar 

  95. Li J, Krichevsky A, Vaidya M, Tzfira T, Citovsky V (2005) Uncoupling of the functions of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc Natl Acad Sci U S A 102:5733–5738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Gelvin SB (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Ann Rev Plant Biol 51:223–256

    Article  CAS  Google Scholar 

  97. Tzfira T, Li J, Lacroix B, Citovsky V (2004) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20:375–383

    Article  CAS  PubMed  Google Scholar 

  98. Brunaud V, Balzergue S, Dubreucq B, Aubourg S, Samson F, Chauvin S, Bechtold N, Cruaud C, DeRose R, Pelletier G, Lepiniec L, Caboche M, Lecharny A (2002) T-DNA integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep 3:1152–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Pelczar P, Kalck V, Gomez D, Hohn B (2004) Agrobacterium proteins VirD2 and VirE2 mediate precise integration of synthetic T-DNA complexes in mammalian cells. EMBO Rep 5:632–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Chilton M-DM, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133:956–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Altpeter F, Baisakh N, Beachy R, Bock R, Capell T, Christou P, Daniell H, Datta K, Datta S, Dix PJ, Fauquet C, Huang N, Kohli A, Mooibroek H, Nicholson L, Nguyen TT, Nugent G, Raemakers K, Romano A, Somers DA, Stoger E, Taylor N, Visser R (2005) Particle bombardment and the genetic enhancement of crops: myths and realities. Mol Breed 15:305–327

    Article  Google Scholar 

  102. Klein TM, Harper EC, Svab Z, Sanford JC, Fromm ME, Maliga P (1988) Stable genetic transformation of intact Nicotiana cells by the particle bombardment process. Proc Natl Acad Sci U S A 85:8502–8505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Klein TM, Kornstein L, Sanford JC, Fromm ME (1989) Genetic transformation of maize cells by particle bombardment. Plant Physiol 91:440–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Ananiev EV, Wu C, Chamberlin MA, Svitashev S, Schwartz C, Gordon-Kamm W, Tingey S (2009) Artificial chromosome formation in maize (Zea mays L.). Chromosoma 118:157–177

    Article  CAS  PubMed  Google Scholar 

  105. Somers DA, Makarevitch I (2004) Transgene integration in plants: poking or patching holes in promiscuous genomes? Curr Opin Biotechnol 15:126–131

    Article  CAS  PubMed  Google Scholar 

  106. Shou H, Frame BR, Whitham SA, Wang K (2004) Assessment of transgenic maize events produced by particle bombardment or Agrobacterium-mediated transformation. Mol Breed 13:201–208

    Article  CAS  Google Scholar 

  107. Zhang Y, Yin X, Yang A, Li G, Zhang J (2005) Stability of inheritance of transgenes in maize (Zea mays L.) lines produced using different transformation methods. Euphytica 144:11–22

    Article  CAS  Google Scholar 

  108. Gao C, Long D, Lenk I, Nielsen KK (2008) Comparative analysis of transgenic tall fescue (Festuca arundinacea Schreb.) plants obtained by Agrobacterium-mediated transformation and particle bombardment. Plant Cell Rep 27:1601–1609

    Article  CAS  PubMed  Google Scholar 

  109. Jackson MA, Anderson DJ, Birch RG (2013) Comparison of Agrobacterium and particle bombardment using whole plasmid or minimal cassette for production of high-expressing, low-copy transgenic plants. Transgenic Res 22:143–151

    Article  CAS  PubMed  Google Scholar 

  110. Bansal KC, Viret J-F, Haley J, Khan BM, Schantz R, Bogorad L (1992) Transient expression from cab-m1 and rbcS-m3 promoter sequences is different in mesophyll and bundle sheath cells in maize leaves. Proc Natl Acad Sci U S A 89:3654–3658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Bansal KC, Bogorad L (1993) Cell type-preferred expression of maize cab-m1: repression in bundle sheath cells and enhancement in mesophyll cells. Proc Natl Acad Sci U S A 90:4057–4061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Varagona MJ, Schmidt RJ, Raikhel NV (1992) Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2. Plant Cell 4:1213–1227

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6:325–330

    Article  CAS  PubMed  Google Scholar 

  114. Lenka SK, Muthusamy SK, Chinnusamy V, Bansal KC (2018) Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana. Mol Biotechnol 60:350–361

    Article  CAS  PubMed  Google Scholar 

  115. Ruberti I, Sessa G, Morelli G (2006) Functional analysis of transcription factors by microparticle bombardment. Methods Mol Biol 323:231–236

    PubMed  Google Scholar 

  116. Morello L, Bardini M, Cricrì M, Sala F, Breviario D (2006) Functional analysis of DNA sequences controlling the expression of the rice OsCDPK2 gene. Planta 223:479–491

    Article  CAS  PubMed  Google Scholar 

  117. Chiera JM, Bouchard RA, Dorsey SL, Park E, Buenrostro-Nava MT, Ling PP, Finer JJ (2007) Isolation of two highly active soybean (Glycine max (L.) Merr.) promoters and their characterization using a new automated image collection and analysis system. Plant Cell Rep 26:1501–1509

    Article  CAS  PubMed  Google Scholar 

  118. Lenka SK, Nims NE, Vongpaseuth K, Boshar RA, Roberts SC, Walker EL (2015) Jasmonate-responsive expression of paclitaxel biosynthesis genes in Taxus cuspidata cultured cells is negatively regulated by the bHLH transcription factors TcJAMYC1, TcJAMYC2, and TcJAMYC4. Front Plant Sci 6:115

    Article  PubMed  PubMed Central  Google Scholar 

  119. Bock R (2007) Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Curr Opin Biotechnol 18:100–106

    Article  CAS  PubMed  Google Scholar 

  120. Xiong L, Sayre RT (2004) Engineering the chloroplast encoded proteins of Chlamydomonas. Photosynth Res 80:411–419

    Article  CAS  PubMed  Google Scholar 

  121. Bonnefoy N, Remacle C, Fox TD (2007) Genetic transformation of Saccharomyces cerevisiae and Chlamydomonas reinhardtii mitochondria. Methods Cell Biol 80:525–548

    Article  CAS  PubMed  Google Scholar 

  122. Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher plants. Proc Natl Acad Sci 87:8526–8530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Sanford JC (2000) The development of the biolistic process. In Vitro Cell Dev Biol Plant 36:303–308

    Article  Google Scholar 

  124. Russell JA, Roy MK, Sanford JC (1992) Major improvements in biolistic transformation of suspension-cultured tobacco cells. In Vitro Plant 28:97–105

    Article  Google Scholar 

  125. Mazuś B, Krysiak C, Buchowicz J (2000) Tungsten particle-induced nicking of supercoiled plasmid DNA. Plasmid 44:89–93

    Article  PubMed  CAS  Google Scholar 

  126. Torney F, Trewyn BG, Lin VS-Y, Wang K (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotechnol 2:295–300

    Article  CAS  PubMed  Google Scholar 

  127. Kikkert JR, Humiston GA, Roy MK, Sanford JC (1999) Biological projectiles (phage, yeast, bacteria) for genetic transformation of plants. In Vitro Cell Dev Biol Plant 35:43–50

    Article  CAS  Google Scholar 

  128. Gaba V, Gal-On A (2006) Inoculation of plants using bombardment. Curr Protoc Microbiol 16:Unit16B.3

    PubMed  Google Scholar 

  129. Krishnamurthy K, Heppler M, Mitra R, Blancaflor E, Payton M, Nelson RS, Verchot-Lubicz J (2003) The potato virus X TGBp3 protein associates with the ER network for virus cell-to-cell movement. Virology 309:135–151

    Article  CAS  PubMed  Google Scholar 

  130. de Mesa MC, Jiménez-Bermúdez S, Pliego-Alfaro F, Quesada MA, Mercado JA (2000) Agrobacterium cells as microprojectile coating: a novel approach to enhance stable transformation rates in strawberry. Funct Plant Biol 27:1093–1100

    Article  Google Scholar 

  131. Chen H, Samadder PP, Tanaka Y, Ohira T, Okuizumi H, Yamaoka N, Miyao A, Hirochika H, Ohira T, Tsuchimoto S, Ohtsubo H, Nishiguchi M (2008) OsRecQ1, a QDE-3 homologue in rice, is required for RNA silencing induced by particle bombardment for inverted repeat DNA, but not for double-stranded RNA. Plant J 56:274–286

    Article  CAS  PubMed  Google Scholar 

  132. Gray MW, Archibald JM (2012) Origins of mitochondria and plastids. In: Bock R, Knoop V (eds) Genomics of chloroplasts and mitochondria. Springer, New York, NY, pp 1–30

    Google Scholar 

  133. Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB, Sanford JC (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240:1534–1538

    Article  CAS  PubMed  Google Scholar 

  134. Spörlein B, Streubel M, Dahlfeld G, Westhoff P, Koop H (1991) PEG-mediated plastid transformation: a new system for transient gene expression assays in chloroplasts. Theor Appl Genet 82:717–722

    Article  PubMed  Google Scholar 

  135. Golds T, Maliga P, Koop H-U (1993) Stable plastid transformation in PEG-treated protoplasts of Nicotiana tabacum. Bio/Technology 11:95–97

    CAS  Google Scholar 

  136. Singh A, Verma S, Bansal K (2010) Plastid transformation in eggplant (Solanum melongena L.). Transgenic Res 19:113–119

    Article  CAS  PubMed  Google Scholar 

  137. Wani SH, Sah SK, Sági L, Solymosi K (2015) Transplastomic plants for innovations in agriculture. A review. Agron Sustain Dev 35:1391–1430

    Article  CAS  Google Scholar 

  138. Johnston SA, Anziano PQ, Shark K, Sanford JC, Butow RA (1988) Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240:1538–1541

    Article  CAS  PubMed  Google Scholar 

  139. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. 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

    Article  CAS  PubMed  Google Scholar 

  141. Larosa V, Remacle C (2013) Transformation of the mitochondrial genome. Int J Dev Biol 57:659–665

    Article  CAS  PubMed  Google Scholar 

  142. Mileshina D, Koulintchenko M, Konstantinov Y, Dietrich A (2011) Transfection of plant mitochondria and in organello gene integration. Nucl Acids Res 39:e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Bock R (2015) Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Ann Rev Plant Biol 66:211–241

    Article  CAS  Google Scholar 

  144. Daniell H, Singh ND, Mason H, Streatfield SJ (2009) Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci 14:669–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Staub JM, Maliga P (1995) Expression of a chimeric uidA gene indicates that polycistronic mRNAs are efficiently translated in tobacco plastids. Plant J 7:845–848

    Article  CAS  PubMed  Google Scholar 

  146. Quesada-Vargas T, Ruiz ON, Daniell H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts. Transcription, processing, and translation. Plant Physiol 138:1746–1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Sone T, Nagamori E, Ikeuchi T, Mizukami A, Takakura Y, Si K, Fukusaki E, Harashima S, Kobayashi A, Fukui K (2002) A novel gene delivery system in plants with calcium alginate micro-beads. J Biosci Bioeng 94:87–91

    Article  CAS  PubMed  Google Scholar 

  148. Murakawa T, Kajiyama SI, Ikeuchi T, Kawakami S, Fukui K (2008) Improvement of transformation efficiency by bioactive-beads-mediated gene transfer using DNA-lipofectin complex as entrapped genetic material. Journal of bioscience and bioengineering 105(1):77–80

    Google Scholar 

  149. Mizukami A, Nagamori E, Takakura Y, Matsunaga S, Kaneko Y, Kajiyama S, Harashima S, Kobayashi A, Fukui K (2003) Transformation of yeast using calcium alginate microbeads with surface-immobilized chromosomal DNA. BioTechniques 35:734–740

    Article  CAS  PubMed  Google Scholar 

  150. Liu H, Kawabe A, Matsunaga S, Kim YH, Higashi T, Uchiyama S, Harashima S, Kobayashi A, Fukui K (2004) An Arabidopsis thaliana gene on the yeast artificial chromosome can be transcribed in tobacco cells. Cytologia 69:235–240

    Article  CAS  Google Scholar 

  151. Liu H, Kawabe A, Matsunaga S, Kobayashi A, Harashima S, Uchiyama S, Ohmido N, Fukui K (2004) Application of the bio-active beads method in rice transformation. Plant Biotechnol 21:303–306

    Article  Google Scholar 

  152. Liu H, Kawabe A, Matsunaga S, Murakawa T, Mizukami A, Yanagisawa M, Nagamori E, Harashima S, Kobayashi A, Fukui K (2004) Obtaining transgenic plants using the bio-active beads method. J Plant Res 117:95–99

    Article  CAS  PubMed  Google Scholar 

  153. Wada N, Si K, Akiyama Y, Kawakami S, No D, Uchiyama S, Otani M, Shimada T, Nose N, Suzuki G, Mukai Y, Fukui K (2009) Bioactive beads-mediated transformation of rice with large DNA fragments containing Aegilops tauschii genes. Plant Cell Rep 28:759–768

    Article  CAS  PubMed  Google Scholar 

  154. Jain SM (2001) Tissue culture-derived variation in crop improvement. Euphytica 118:153–166

    Article  CAS  Google Scholar 

  155. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  156. Hess D (1980) Investigations on the intra-and interspecific transfer of anthocyanin genes using pollen as vectors. Z Pflanzenphysiol 98:321–337

    Article  CAS  Google Scholar 

  157. Ohta Y (1986) High-efficiency genetic transformation of maize by a mixture of pollen and exogenous DNA. Proc Natl Acad Sci U S A 83:715–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Negrutiu I, Heberle-Bors E, Potrykus I (1986) Attempts to transform for kanamycin-resistance in mature pollen of tobacco. In: Negrutiu I, Heberle-Bors E, Potrykus I (eds) Biotechnology and ecology of pollen. Springer, New York, NY, pp 65–70

    Chapter  Google Scholar 

  159. Booy G, Krens F, Huizing H (1989) Attempted pollen-mediated transformation of maize. J Plant Physiol 135:319–324

    Article  CAS  Google Scholar 

  160. Zhou G-Y, Weng J, Zeng Y, Huang J, Qian S, Liu G (1983) Introduction of exogenous DNA into cotton embryos. Methods Enzymol 101:433–481

    Article  CAS  PubMed  Google Scholar 

  161. Z-x L, Wu R (1988) A simple method for the transformation of rice via the pollen-tube pathway. Plant Mol Biol Rep 6:165–174

    Article  Google Scholar 

  162. Bibi N, Fan K, Yuan S, Ni M, Ahmed IM, Malik W, Wang X (2013) An efficient and highly reproducible approach for the selection of upland transgenic cotton produced by pollen tube pathway method. Aust J Crop Sci 7:1714

    Google Scholar 

  163. Peffley EB, Allen R, Song P, Shang X (2003) Direct transformation of higher plants through pollen tube pathway. US Patent, US6583335B1

    Google Scholar 

  164. Resch T, Touraev A (2010) Pollen transformation technologies. In: Stewart CN Jr, Touraev A, Citovsky V, Tzfira T (eds) Plant transformation technologies. Blackwell Publishing Ltd, London, pp 83–91

    Google Scholar 

  165. Ali A, Bang SW, Chung S-M, Staub JE (2015) Plant transformation via pollen tube-mediated gene transfer. Plant Mol Biol Rep 33:742–747

    Article  CAS  Google Scholar 

  166. Matthews BF, Abdul-Baki AA, Saunders JA (1990) Expression of a foreign gene in electroporated pollen grains of tobacco. Sex Plant Reprod 3:147–151

    Article  Google Scholar 

  167. Smith CR, Saunders JA, Van Wert S, Cheng J, Matthews BF (1994) Expression of GUS and CAT activities using electrotransformed pollen. Plant Sci 104:49–58

    Article  CAS  Google Scholar 

  168. Twell D, Klein TM, Fromm ME, McCormick S (1989) Transient expression of chimeric genes delivered into pollen by microprojectile bombardment. Plant Physiol 91:1270–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Stöger E, Fink C, Pfosser M, Heberle-Bors E (1995) Plant transformation by particle bombardment of embryogenic pollen. Plant Cell Rep 14:273–278

    Article  PubMed  Google Scholar 

  170. Neuhaus G, Spangenberg G, Scheid OM, Schweiger H-G (1987) Transgenic rapeseed plants obtained by the microinjection of DNA into microspore-derived embryoids. Theor Appl Genet 75:30–36

    Article  Google Scholar 

  171. Kaeppler HF, Gu W, Somers DA, Rines HW, Cockburn AF (1990) Silicon carbide fiber-mediated DNA delivery into plant cells. Plant Cell Rep 9:415–418

    Article  CAS  PubMed  Google Scholar 

  172. Asad S, Arshad M (2011) Silicon carbide whisker-mediated plant transformation. Properties and applications of silicon carbide. IntechOpen, London

    Google Scholar 

  173. Singh N, Chawla H (1999) Use of silicon carbide fibers for Agrobacterium-mediated transformation in wheat. Curr Sci 76:1483–1485

    Google Scholar 

  174. Nagatani N, Honda H, Shimada T, Kobayashi T (1997) DNA delivery into rice cells and transformation using silicon carbide whiskers. Biotechnol Tech 11:471–473

    Article  CAS  Google Scholar 

  175. Zhao X, Meng Z, Wang Y, Chen W, Sun C, Cui B, Cui J, Yu M, Zeng Z, Guo S, Luo D, Cheng JQ, Zhang R, Cui H (2017) Pollen magnetofection for genetic modification with magnetic nanoparticles as gene carriers. Nat Plants 3:956–964

    Article  CAS  PubMed  Google Scholar 

  176. Demirer GS, Zhang H, Matos JL, Goh NS, Cunningham FJ, Sung Y, Chang R, Aditham AJ, Chio L, Cho MJ, Staskawicz B, Landry MP (2019) High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants. Nat Nanotechnol 14:456–464

    Article  CAS  PubMed  Google Scholar 

  177. Cunningham FJ, Goh NS, Demirer GS, Matos JL, Landry MP (2018) Nanoparticle-mediated delivery towards advancing plant genetic engineering. Trends Biotechnol 36:882–897

    Article  CAS  PubMed  Google Scholar 

  178. Joldersma D, Liu Z (2018) Plant genetics enters the nano age? J Integr Plant Biol 60:446–447

    Article  PubMed  Google Scholar 

  179. Shimamoto K, Terada R, Izawa T, Fujimoto H (1989) Fertile transgenic rice plants regenerated from transformed protoplasts. Nature 338:274–276

    Article  CAS  Google Scholar 

  180. Salmenkallio-Marttila M, Aspegren K, Åkerman S, Kurten U, Mannonen L, Ritala A, Teeri TH, Kauppinen V (1995) Transgenic barley (Hordeum vulgare L.) by electroporation of protoplasts. Plant Cell Rep 15:301–304

    Article  CAS  PubMed  Google Scholar 

  181. Ahokas H (1989) Transfection of germinating barley seed electrophoretically with exogenous DNA. Theor Appl Genet 77:469–472

    Article  CAS  PubMed  Google Scholar 

  182. Chowrira GM, Akella V, Lurquin PF (1995) Electroporation-mediated gene transfer into intact nodal meristemsin planta. Mol Biotechnol 3:17–23

    Article  CAS  PubMed  Google Scholar 

  183. Crossway A, Oakes JV, Irvine JM, Ward B, Knauf VC, Shewmaker C (1986) Integration of foreign DNA following microinjection of tobacco mesophyll protoplasts. Mol Gen Genet 202:179–185

    Article  CAS  Google Scholar 

  184. Jones-Villeneuve E, Huang B, Prudhomme I, Bird S, Kemble R, Hattori J, Miki B (1995) Assessment of microinjection for introducing DNA into uninuclear microspores of rapeseed. Plant Cell Tissue Organ Cult 40:97–100

    Article  Google Scholar 

  185. Holm PB, Olsen O, Schnorf M, Brinch-Pedersen H, Knudsen S (2009) Transformation of barley by microinjection into isolated zygote protoplasts. Transgenic Res 9:21–32

    Article  Google Scholar 

  186. Baskaran P, Soós V, Balázs E, Van Staden J (2016) Shoot apical meristem injection: a novel and efficient method to obtain transformed cucumber plants. South Afr J Bot 103:210–215

    Article  CAS  Google Scholar 

  187. Altpeter F, Springer NM, Bartley LE, Blechl AE, Brutnell TP, Citovsky V, Conrad LJ, Gelvin SB, Jackson DP, Kausch AP, Lemaux PG, Medford JI, Orozco-Cárdenas ML, Tricoli DM, Van Eck J, Voytas DF, Walbot V, Wang K, Zhang ZJ, Stewart CN Jr (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  188. Verma SS, Chinnusamy V, Bansal KC (2008) A simplified floral dip method for transformation of Brassica napus and B. carinata. J Plant Biochem Biotechnol 17:197–200

    Article  CAS  Google Scholar 

  189. Fang F, Oliva M, Ehi-Eromosele S, Zaccai M, Arazi T, Oren-Shamir M (2018) Successful floral-dipping transformation of post-anthesis lisianthus (Eustoma grandiflorum) flowers. Plant J 96:869–879

    Article  CAS  PubMed  Google Scholar 

  190. Lu C, Kang J (2008) Generation of transgenic plants of a potential oilseed crop Camelina sativa by Agrobacterium-mediated transformation. Plant Cell Rep 27:273–278

    Article  CAS  PubMed  Google Scholar 

  191. Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Florentin A, Damri M, Grafi G (2013) Stress induces plant somatic cells to acquire some features of stem cells accompanied by selective chromatin reorganization. Dev Dyn 242:1121–1133

    Article  CAS  PubMed  Google Scholar 

  193. Fehér A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta 1849:385–402

    Article  PubMed  CAS  Google Scholar 

  194. Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359

    Article  CAS  PubMed  Google Scholar 

  195. Bouchabke-Coussa O, Obellianne M, Linderme D, Montes E, Maia-Grondard A, Vilaine F, Pannetier C (2013) Wuschel overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro. Plant Cell Rep 32:675–686

    Article  CAS  PubMed  Google Scholar 

  196. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Sardesai N, Lee L-Y, Chen H, Yi H, Olbricht GR, Stirnberg A, Jeffries J, Xiong K, Doerge RW, Gelvin SB (2013) Cytokinins secreted by Agrobacterium promote transformation by repressing a plant myb transcription factor. Sci Signal 6:ra100

    Article  CAS  PubMed  Google Scholar 

  198. Dan Y, Zhang S, Zhong H, Yi H, Sainz MB (2015) Novel compounds that enhance Agrobacterium-mediated plant transformation by mitigating oxidative stress. Plant Cell Rep 34:291–309

    Article  CAS  PubMed  Google Scholar 

  199. Potrykus I (1989) Gene transfer to cereals: an assessment. Trends Biotechnol 7:269–273

    Article  Google Scholar 

  200. Hiei Y, Ishida Y, Komari T (2014) Progress of cereal transformation technology mediated by Agrobacterium tumefaciens. Front Plant Sci 5:628

    Article  PubMed  PubMed Central  Google Scholar 

  201. Singh RK, Prasad M (2016) Advances in Agrobacterium tumefaciens-mediated genetic transformation of graminaceous crops. Protoplasma 253:691–707

    Article  CAS  PubMed  Google Scholar 

  202. Komari T (1990) Transformation of cultured cells of Chenopodium quinoa by binary vectors that carry a fragment of DNA from the virulence region of pTiBo542. Plant Cell Rep 9:303–306

    Article  CAS  PubMed  Google Scholar 

  203. Ishida Y, Hiei Y, Komari T (2007) Agrobacterium-mediated transformation of maize. Nat Protoc 2:1614–1621

    Article  CAS  PubMed  Google Scholar 

  204. Ishida Y, Tsunashima M, Hiei Y, Komari T (2015) Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol Biol 1223:189–198

    Article  CAS  PubMed  Google Scholar 

  205. Hensel G, Valkov V, Middlefell-Williams J, Kumlehn J (2008) Efficient generation of transgenic barley: the way forward to modulate plant–microbe interactions. J Plant Physiol 165:71–82

    Article  CAS  PubMed  Google Scholar 

  206. Wu E, Lenderts B, Glassman K, Berezowska-Kaniewska M, Christensen H, Asmus T, Zhen S, Chu U, Cho MJ, Zhao ZY (2014) Optimized Agrobacterium-mediated sorghum transformation protocol and molecular data of transgenic sorghum plants. In Vitro Cell Dev Biol Plant 50:9–18

    Article  PubMed  CAS  Google Scholar 

  207. Someya T, Nonaka S, Nakamura K, Ezura H (2013) Increased 1-aminocyclopropane-1-carboxylate deaminase activity enhances Agrobacterium tumefaciens-mediated gene delivery into plant cells. Microbiology 2:873–880

    CAS  Google Scholar 

  208. Ishida Y, Saito H, Ohta S, Hiei Y, Komari T, Kumashiro T (1996) High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nat Biotechnol 14:745–750

    Article  CAS  PubMed  Google Scholar 

  209. Hernandez L (2000) Sugarcane (Saccharum hybrid) genetic transformation mediated by Agrobacterium tumefaciens: production of transgenic plants expressing proteins with agronomic and industrial value. Develop Plant Genet Breed 5:76–81

    Article  Google Scholar 

  210. Jha P, Rustagi A, Agnihotri PK, Kulkarni VM, Bhat V (2011) Efficient Agrobacterium-mediated transformation of Pennisetum glaucum (L.) R. Br. using shoot apices as explant source. Plant Cell Tissue Organ Cult 107:501–512

    Article  CAS  Google Scholar 

  211. Hiei Y, Ishida Y, Kasaoka K, Komari T (2006) Improved frequency of transformation in rice and maize by treatment of immature embryos with centrifugation and heat prior to infection with Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult 87:233–243

    Article  Google Scholar 

  212. Naing AH, Ai TN, Jeon SM, Lim SH, Kim CK (2016) An efficient protocol for Agrobacterium-mediated genetic transformation of recalcitrant chrysanthemum cultivar Shinma. Acta Physiol Plant 38:38

    Article  CAS  Google Scholar 

  213. Petolino JF, Kumar S (2016) Transgenic trait deployment using designed nucleases. Plant Biotechnol J 14:503–509

    Article  CAS  PubMed  Google Scholar 

  214. Ow DW (2016) The long road to recombinase-mediated plant transformation. Plant Biotechnol J 14:441–447

    Article  CAS  PubMed  Google Scholar 

  215. Iglesias VA, Moscone EA, Papp I, Neuhuber F, Michalowski S, Phelan T, Spiker S, Matzke M, Matzke AJ (1997) Molecular and cytogenetic analyses of stably and unstably expressed transgene loci in tobacco. Plant Cell 9:1251–1264

    CAS  PubMed  PubMed Central  Google Scholar 

  216. Takano M, Egawa H, Ikeda JE, Wakasa K (1997) The structures of integration sites in transgenic rice. Plant J 11:353–361

    Article  CAS  PubMed  Google Scholar 

  217. Alberts B, Sternglanz R (1990) Chromatin contract to silence. Nature 344:193

    Article  CAS  PubMed  Google Scholar 

  218. Matzke AJ, Matzke MA (1998) Position effects and epigenetic silencing of plant transgenes. Curr Opin Plant Biol 1:142–148

    Article  CAS  PubMed  Google Scholar 

  219. Ramkumar TR, Parameswari C, Sugapriya T, Veluthambi K (2015) Effect of orientation of transcription of a gene in an inverted transferred DNA repeat on transcriptional gene silencing in rice transgenics—a case study. Physiol Mol Biol Plants 21:151–157

    Article  CAS  PubMed  Google Scholar 

  220. Lindsey K, Wei W, Clarke MC, McArdle HF, Rooke LM, Topping JF (1993) Tagging genomic sequences that direct transgene expression by activation of a promoter trap in plants. Transgenic Res 2:33–47

    Article  CAS  PubMed  Google Scholar 

  221. Conner AJ, Jacobs JM (1999) Genetic engineering of crops as potential source of genetic hazard in the human diet. Mut Res 443:223–234

    Article  CAS  Google Scholar 

  222. Halpin C (2005) Gene stacking in transgenic plants–the challenge for 21st century plant biotechnology. Plant Biotechnol J 3:141–155

    Article  CAS  PubMed  Google Scholar 

  223. Collard BC, Mackill DJ (2007) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond Ser B Biol Sci 363:557–572

    Article  CAS  Google Scholar 

  224. Edwards D, Batley J (2010) Plant genome sequencing: applications for crop improvement. Plant Biotechnol J 8:2–9

    Article  CAS  PubMed  Google Scholar 

  225. Ficklin SP, Luo F, Feltus FA (2010) The association of multiple interacting genes with specific phenotypes in rice using gene coexpression networks. Plant Physiol 154:13–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Gilbertson L (2003) Cre–lox recombination: Cre-ative tools for plant biotechnology. Trends Biotechnol 21:550–555

    Article  CAS  PubMed  Google Scholar 

  227. Srivastava V, Nicholson SJ (2006) Cre/lox technologies for plant transformation. CAB Rev 1:1–12

    Article  CAS  Google Scholar 

  228. Lenka SK, Carbonaro N, Park R, Miller SM, Thorpe I, Li Y (2016) Current advances in molecular, biochemical, and computational modeling analysis of microalgal triacylglycerol biosynthesis. Biotechnol Adv 34:1046–1063

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  230. Wright DA, Townsend JA, Winfrey RJ Jr, Irwin PA, Rajagopal J, Lonosky PM, Hall BD, Jondle MD, Voytas DF (2005) High-frequency homologous recombination in plants mediated by zinc-finger nucleases. Plant J 44:693–705

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  234. Malzahn A, Lowder L, Qi Y (2017) Plant genome editing with TALEN and CRISPR. Cell Biosci 7:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  235. Liu X, Wu S, Xu J, Sui C, Wei J (2017) Application of CRISPR/Cas9 in plant biology. Acta Pharm Sin B 7:292–302

    Article  PubMed  PubMed Central  Google Scholar 

  236. Van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ (2009) CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34:401–407

    Article  PubMed  CAS  Google Scholar 

  237. Barrangou R (2015) The roles of CRISPR-Cas systems in adaptive immunity and beyond. Curr Opin Immunol 32:36–41

    Article  CAS  PubMed  Google Scholar 

  238. Jiang F, Doudna JA (2017) 2CRISPR-Cas9 structures and mechanisms. Annu Rev Biophys 46:505–529

    Article  CAS  PubMed  Google Scholar 

  239. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJ, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  240. Shmakov S, Abudayyeh OO, Makarova KS, Wolf YI, Gootenberg JS, Semenova E, Minakhin L, Joung J, Konermann S, Severinov K, Zhang F (2015) Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol Cell 60:385–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Jiang W, Zhou H, Bi H, Fromm M, Yang B, Weeks DP (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucl Acids Res 41:e188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Feng Z, Zhang B, Ding W, Liu X, Yang D-L, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 6:1975–1983

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  250. Baltes NJ, Gil-Humanes J, Cermak T, Atkins PA, Voytas DF (2014) DNA replicons for plant genome engineering. Plant Cell 26:151–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Woo JW, Kim J, Kwon SI, Corvalán C, Cho SW, Kim H, Kim SG, Kim ST, Choe S, Kim JS (2015) DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nat Biotechnol 33:1162–1164

    Article  CAS  PubMed  Google Scholar 

  252. Sugano SS, Shirakawa M, Takagi J, Matsuda Y, Shimada T, Hara-Nishimura I, Kohchi T (2014) CRISPR/Cas9-mediated targeted mutagenesis in the liverwort Marchantia polymorpha L. Plant Cell Physiol 55:475–481

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  255. Ron M, Kajala K, Pauluzzi G, Wang D, Reynoso MA, Zumstein K, Garcha J, Winte S, Masson H, Inagaki S, Federici F, Sinha N, Deal RB, Bailey-Serres J, Brady SM (2014) Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol 166:455–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Wang S, Zhang S, Wang W, Xiong X, Meng F, Cui X (2015) Efficient targeted mutagenesis in potato by the CRISPR/Cas9 system. Plant Cell Rep 34:1473–1476

    Article  CAS  PubMed  Google Scholar 

  257. Lawrenson T, Shorinola O, Stacey N, Li C, Østergaard L, Patron N, Uauy C, Harwood W (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol 16:258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  258. Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  259. Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  260. Jia H, Wang N (2014) Targeted genome editing of sweet orange using Cas9/sgRNA. PLoS One 9:e93806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  261. Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep 5:12217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Michno J-M, Wang X, Liu J, Curtin SJ, Kono TJ, Stupar RM (2015) CRISPR/Cas mutagenesis of soybean and Medicago truncatula using a new web-tool and a modified Cas9 enzyme. GM Crops Food 6:243–252

    Article  PubMed  PubMed Central  Google Scholar 

  263. Jaganathan D, Ramasamy K, Sellamuthu G, Jayabalan S, Venkataraman G (2018) CRISPR for crop improvement: An update review. Front Plant Sci 9:985

    Article  PubMed  PubMed Central  Google Scholar 

  264. Jang G, Joung YH (2019) CRISPR/Cas-mediated genome editing for crop improvement: current applications and future prospects. Plant Biotechnol Rep 13:1–10

    Article  Google Scholar 

  265. Zhou X, Jacobs TB, Xue LJ, Harding SA, Tsai CJ (2015) Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial populus reveals 4-coumarate: CoA ligase specificity and redundancy. New Phytol 208:298–301

    Article  CAS  PubMed  Google Scholar 

  266. Alagoz Y, Gurkok T, Zhang B, Unver T (2016) Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci Rep 6:30910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  267. Li R, Li R, Li X, Fu D, Zhu B, Tian H, Luo Y, Zhu H (2018) Multiplexed CRISPR/Cas9-mediated metabolic engineering of γ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16:415–427

    Article  CAS  PubMed  Google Scholar 

  268. Ali Z, Abulfaraj A, Idris A, Ali S, Tashkandi M, Mahfouz MM (2015) CRISPR/Cas9-mediated viral interference in plants. Genome Biol 16:238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  269. Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Weissman JS, Qi LS (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  270. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  271. Marzec M, Hensel G (2018) Targeted base editing systems are available for plants. Trends Plant Sci 23:955–957

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors acknowledge the continuous support of Director, TERI-Deakin Nanobiotechnology Centre, The Energy and Resources Institute (India).

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Authors and Affiliations

  1. Agronomy Department, IFAS, University of Florida, Gainesville, FL, USA

    Thakku R. Ramkumar

  2. TERI-Deakin NanoBiotechnology Centre, The Energy and Resources Institute, New Delhi, India

    Sangram K. Lenka, Sagar S. Arya & Kailash C. Bansal

Authors
  1. Thakku R. Ramkumar
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  2. Sangram K. Lenka
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  3. Sagar S. Arya
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  4. Kailash C. Bansal
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Corresponding author

Correspondence to Kailash C. Bansal .

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Editors and Affiliations

  1. Department of Plant and Environmental Sciences, School of Health Research, Pee Dee Research and Education Center, Clemson University, Florence, SC, USA

    Sachin Rustgi

  2. Department of Genetics and Biochemistry, Clemson University, Clemson, SC, USA

    Hong Luo

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Ramkumar, T.R., Lenka, S.K., Arya, S.S., Bansal, K.C. (2020). A Short History and Perspectives on Plant Genetic Transformation. In: Rustgi, S., Luo, H. (eds) Biolistic DNA Delivery in Plants. Methods in Molecular Biology, vol 2124. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-0356-7_3

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  • DOI: https://doi.org/10.1007/978-1-0716-0356-7_3

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