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Nanobiolistics: An Emerging Genetic Transformation Approach

  • Francis J. Cunningham
  • Gozde S. Demirer
  • Natalie S. Goh
  • Huan Zhang
  • Markita P. LandryEmail author
Protocol
  • 192 Downloads
Part of the Methods in Molecular Biology book series (MIMB, volume 2124)

Abstract

Biolistic delivery of biomolecular cargoes to plants with micron-scale projectiles is a well-established technique in plant biotechnology. However, the relatively large micron-scale biolistic projectiles can result in tissue damage, low regeneration efficiency, and create difficulties for the biolistic transformation of isomorphic small cells or subcellular target organelles (i.e., mitochondria and plastids). As an alternative to micron-sized carriers, nanomaterials provide a promising approach for biomolecule delivery to plants. While most studies exploring nanoscale biolistic carriers have been carried out in animal cells and tissues, which lack a cell wall, we can nonetheless extrapolate their utility for nanobiolistic delivery of biomolecules in plant targets. Specifically, nanobiolistics has shown promising results for use in animal systems, in which nanoscale projectiles yield lower levels of cell and tissue damage while maintaining similar transformation efficiencies as their micron-scale counterparts. In this chapter, we specifically discuss biolistic delivery of nanoparticles for plant genetic transformation purposes and identify the figures of merit requiring optimization for broad-scale implementation of nanobiolistics in plant genetic transformations.

Key words

Biolistics Nanobiolistics Plant transformation Agriculture Bionanotechnology Nanoparticles Gold nanoparticles Mesoporous silica nanoparticles (MSNs) Carbon nanotubes (CNTs) 

Notes

Acknowledgments

The authors acknowledge support from a Burroughs Wellcome Fund Career Award at the Scientific Interface (CASI), a Beckman Foundation Young Investigator Award, a USDA AFRI award, a grant from the Gordon and Betty Moore Foundation, a USDA NIFA award, an NIH MIRA award, support from the Chan-Zuckerberg foundation, and an FFAR New Innovator Award (to M.P.L). F.J.C is supported by an NSF Graduate Research Fellowship, N.S.G is supported by a FFAR Fellowship, and G.S.D. is supported by a Schlumberger Foundation Faculty for the Future Fellowship.

References

  1. 1.
    Subcommittee N (2007) The national nanotechnology initiative. Nanotechnology.  https://doi.org/10.4135/9781412972093.n338
  2. 2.
    Johlin E, Al-Obeidi A, Nogay G, Stuckelberger M, Buonassisi T, Grossman JC (2016) Nanohole structuring for improved performance of hydrogenated Amorphous silicon photovoltaics. ACS Appl Mater Interfaces 8:15169–15176PubMedCrossRefGoogle Scholar
  3. 3.
    Lee YM, Lee D, Kim J, Park H, Kim WJ (2015) RPM peptide conjugated bioreducible polyethylenimine targeting invasive colon cancer. J Control Release 205:172–180PubMedCrossRefGoogle Scholar
  4. 4.
    LaVan DA, McGuire T, Langer R (2003) Small-scale systems for in vivo drug delivery. Nat Biotechnol 21:1184–1191PubMedCrossRefGoogle Scholar
  5. 5.
    Cavalcanti A, Shirinzadeh B, Freitas RA Jr, Hogg T (2007) Nanorobot architecture for medical target identification. Nanotechnology 19:15103CrossRefGoogle Scholar
  6. 6.
    Zadegan RM, Norton ML (2012) Structural DNA nanotechnology: from design to applications. Int J Mol Sci 13:7149–7162PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Ghormade V, Deshpande MV, Paknikar KM (2011) Perspectives for nano-biotechnology enabled protection and nutrition of plants. Biotechnol Adv 29:792–803PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Thangavelu RM, Gunasekaran D, Jesse MI, Riyaz MSU, Sundarajan D, Krishnan K (2018) Nanobiotechnology approach using plant rooting hormone synthesized silver nanoparticle as “nanobullets” for the dynamic applications in horticulture – an in vitro and ex vitro study. Arab J Chem 11:48–61CrossRefGoogle Scholar
  9. 9.
    Barrena R, Casals E, Colón J, Font X, Sánchez A, Puntes V (2009) Evaluation of the ecotoxicity of model nanoparticles. Chemosphere 75:850–857PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Arora S, Sharma P, Kumar S, Nayan R, Khanna PK, Zaidi MGH (2012) Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea. Plant Growth Regul 66:303–310CrossRefGoogle Scholar
  11. 11.
    Salama HMH (2012) Effects of silver nanoparticles in some crop plants, common bean (Phaseolus vulgaris L.) and corn (Zea mays L.). Int Res J Biotechnol 3:190–197Google Scholar
  12. 12.
    Tian H, Chen J, Chen X (2013) Nanoparticles for gene delivery. Small 9:2034–2044PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Demirer GS, Okur AC, Kizilel S (2015) Synthesis and design of biologically inspired biocompatible iron oxide nanoparticles for biomedical applications. J Mater Chem B 3:7831–7849PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Laurent S, Saei AA, Behzadi S, Panahifar A, Mahmoudi M (2014) Superparamagnetic iron oxide nanoparticles for delivery of therapeutic agents: opportunities and challenges. Expert Opin Drug Deliv 11:1449–1470PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Nazli C, Demirer GS, Yar Y, Acar HY, Kizilel S (2014) Targeted delivery of doxorubicin into tumor cells via MMP-sensitive PEG hydrogel-coated magnetic iron oxide nanoparticles (MIONPs). Colloids Surfaces B Biointerfaces 122:674–683PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Mu Q, Jeon M, Hsiao M-H, Patton VK, Wang K, Press OW, Zhang M (2015) Stable and efficient paclitaxel nanoparticles for targeted glioblastoma therapy. Adv Healthc Mater 4:1236–1245PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Jin S, Leach JC, Ye K (2009) Nanoparticle-mediated gene delivery. In: Foote RS, Lee JW (eds) Micro and nano technologies in bioanalysis: methods and protocols. Humana, Totowa, NJ, pp 547–557CrossRefGoogle Scholar
  18. 18.
    Pissuwan D, Niidome T, Cortie MB (2011) The forthcoming applications of gold nanoparticles in drug and gene delivery systems. J Control Release 149:65–71PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Gu Y-J, Cheng J, Lin C-C, Lam YW, Cheng SH, Wong W-T (2009) Nuclear penetration of surface functionalized gold nanoparticles. Toxicol Appl Pharmacol 237:196–204PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Gibson JD, Khanal BP, Zubarev ER (2007) Paclitaxel-functionalized gold nanoparticles. J Am Chem Soc 129:11653–11661PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Shiotani A, Mori T, Niidome T, Niidome Y, Katayama Y (2007) Stable incorporation of gold nanorods into N-isopropylacrylamide hydrogels and their rapid shrinkage induced by near-infrared laser irradiation. Langmuir 23:4012–4018PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Han G, Martin CT, Rotello VM (2006) Stability of gold nanoparticle-bound DNA toward biological, physical, and chemical agents. Chem Biol Drug Des 67:78–82PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Han G, Chari NS, Verma A, Hong R, Martin CT, Rotello VM (2005) Controlled recovery of the transcription of nanoparticle-bound DNA by intracellular concentrations of glutathione. Bioconjug Chem 16:1356–1359PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Pezzoli D, Kajaste-Rudnitski A, Chiesa R, Candiani G (2013) Lipid-based nanoparticles as nonviral gene delivery vectors. In: Bergese P, Hamad-Schifferli K (eds) Nanomaterial interfaces in biology: methods and protocols. Humana, Totowa, NJ, pp 269–279CrossRefGoogle Scholar
  25. 25.
    Blanco E, Shen H, Ferrari M (2015) Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol 33:941–951PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Hui SW, Langner M, Zhao Y-L, Ross P, Hurley E, Chan K (1996) The role of helper lipids in cationic liposome-mediated gene transfer. Biophys J 71:590–599PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Chatin B, Mével M, Devallière J, Dallet L, Haudebourg T, Peuziat P, Colombani T, Berchel M, Lambert O, Edelman A, Pitard B (2015) Liposome-based formulation for intracellular delivery of functional proteins. Mol Ther Nucleic Acids 4:e244PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Wang M, Zuris JA, Meng F, Rees H, Sun S, Deng P, Han Y, Gao X, Pouli D, Wu Q, Georgakoudi I, Liu DR, Xu Q (2016) Efficient delivery of genome-editing proteins using bioreducible lipid nanoparticles. Proc Natl Acad Sci U S A 113:2868–2873PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Torchilin VP (2014) Multifunctional, stimuli-sensitive nanoparticulate systems for drug delivery. Nat Rev Drug Discov 13:813–827PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Nitta KS, Numata K (2013) Biopolymer-based nanoparticles for drug/gene delivery and tissue engineering. Int J Mol Sci 14:1629–1654PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Li J, Liang H, Liu J, Wang Z (2018) Poly (amidoamine) (PAMAM) dendrimer mediated delivery of drug and pDNA/siRNA for cancer therapy. Int J Pharm 546:215–225PubMedCrossRefGoogle Scholar
  32. 32.
    Pasupathy K, Lin S, Hu Q, Luo H, Ke PC (2008) Direct plant gene delivery with a poly(amidoamine) dendrimer. Biotechnol J 3:1078–1082PubMedCrossRefGoogle Scholar
  33. 33.
    Hartono SB, Phuoc NT, Yu M, Jia Z, Monteiro MJ, Qiao S, Yu C (2014) Functionalized large pore mesoporous silica nanoparticles for gene delivery featuring controlled release and co-delivery. J Mater Chem B 2:718–726PubMedCrossRefGoogle Scholar
  34. 34.
    Torney F, Trewyn BG, Lin VSY, Wang K (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotechnol 2:295–300PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Karimi M, Solati N, Ghasemi A, Estiar MA, Hashemkhani M, Kiani P, Mohamed E, Saeidi A, Taheri M, Avci P, Aref AR, Amiri M, Baniasadi F, Hamblin MR (2015) Carbon nanotubes part II: a remarkable carrier for drug and gene delivery. Expert Opin Drug Deliv 12:1089–1105PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Demirer GS, Landry MP (2017) Delivering genes to plants. Chem Eng Prog 113:40–45Google Scholar
  37. 37.
    Bhirde AA, Patel V, Gavard J, Zhang G, Sousa AA, Masedunskas A, Leapman RD, Weigert R, Gutkind JS, Rusling JF (2009) Targeted killing of cancer cells in vivo and in vitro with EGF-directed carbon nanotube-based drug delivery. ACS Nano 3:307–316PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Heister E, Neves V, Tîlmaciu C, Lipert K, Beltrán VS, Coley HM, Silva SRP, McFadden J (2009) Triple functionalisation of single-walled carbon nanotubes with doxorubicin, a monoclonal antibody, and a fluorescent marker for targeted cancer therapy. Carbon 47:2152–2160CrossRefGoogle Scholar
  39. 39.
    Liu Z, Chen K, Davis C, Sherlock S, Cao Q, Chen X, Dai H (2008) Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Res 68:6652–6660PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Shi Kam NW, Jessop TC, Wender PA, Dai H (2004) Nanotube molecular transporters: internalization of carbon nanotube− protein conjugates into mammalian cells. J Am Chem Soc 126:6850–6851PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Kam NWS, Liu Z, Dai H (2006) Carbon nanotubes as intracellular transporters for proteins and DNA: an investigation of the uptake mechanism and pathway. Angew Chem 118:591–595CrossRefGoogle Scholar
  42. 42.
    Dong H, Ding L, Yan F, Ji H, Ju H (2011) The use of polyethylenimine-grafted graphene nanoribbon for cellular delivery of locked nucleic acid modified molecular beacon for recognition of microRNA. Biomaterials 32:3875–3882PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Qin W, Yang K, Tang H, Tan L, Xie Q, Ma M, Zhang Y, Yao S (2011) Improved GFP gene transfection mediated by polyamidoamine dendrimer-functionalized multi-walled carbon nanotubes with high biocompatibility. Colloids Surfaces B Biointerfaces 84:206–213PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Karmakar A, Bratton SM, Dervishi E, Ghosh A, Mahmood M, Xu Y, Saeed LM, Mustafa T, Casciano D, Radominska-Pandya A, Biris AS (2011) Ethylenediamine functionalized-single-walled nanotube (f-SWNT)-assisted in vitro delivery of the oncogene suppressor p53 gene to breast cancer MCF-7 cells. Int J Nanomedicine 6:1045–1055PubMedPubMedCentralGoogle Scholar
  45. 45.
    Wu Y, Phillips JA, Liu H, Yang R, Tan W (2008) Carbon nanotubes protect DNA strands during cellular delivery. ACS Nano 2:2023–2028PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Zheng M, Jagota A, Semke ED, Diner BA, McLean RS, Lustig SR, Richardson RE, Tassi NG (2003) DNA-assisted dispersion and separation of carbon nanotubes. Nat Mater 2:338–342PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Wang H, Koleilat GI, Liu P, Jiménez-Osés G, Lai YC, Vosgueritchian M, Fang Y, Park S, Houk KN, Bao Z (2014) High-yield sorting of small-diameter carbon nanotubes for solar cells and transistors. ACS Nano 8:2609–2617PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Wong MH, Misra RP, Giraldo JP, Kwak SY, Son Y, Landry MP, Swan JW, Blankschtein D, Strano MS (2016) Lipid exchange envelope penetration (LEEP) of nanoparticles for plant engineering: a universal localization mechanism. Nano Lett 16:1161–1172PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Reuel NF, Hilmer AJ, Sen F, Brew JA, Strano MS (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13:400–408PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Demirer GS, Zhang H, Matos J, Goh NS, Cunningham FJ, Sung Y, Chang R, Aditham AJ, Chio L, Cho MJ, Staskawicz B, Landry MP (2018) High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants. Nat Nanotechnol 14:456–464CrossRefGoogle Scholar
  51. 51.
    Cunningham FJ, Goh NS, Demirer GS, Matos JL, Landry MP (2018) Nanoparticle-mediated delivery towards advancing plant genetic engineering. Trends Biotechnol 36:882–897PubMedCrossRefGoogle Scholar
  52. 52.
    Wang P, Lombi E, Zhao F-JJ, Kopittke PM (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21:699–712PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Sidorov VA, Kasten D, Pang S, Hajdukiewicz PT, Staub JM, Nehra NS (1999) Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J 19:209–216PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Kwak S-Y, Lew TTS, Sweeney CJ, Koman VB, Wong MH, Bohmert-Tatarev K, Snell KD, Seo JS, Chua NH, Strano MS (2016) Chloroplast-selective gene delivery and expression in planta using chitosan-complexed single-walled carbon nanotube carriers. Nat Nanotechnol 14:447–455CrossRefGoogle Scholar
  55. 55.
    Kreyling WG, Semmler-Behnke M, Chaudhry Q (2010) A complementary definition of nanomaterial. Nano Today 5:165–168CrossRefGoogle Scholar
  56. 56.
    Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179:154–163CrossRefGoogle Scholar
  57. 57.
    Parisi C, Vigani M, Rodríguez-Cerezo E (2015) Agricultural nanotechnologies: what are the current possibilities? Nano Today 10:124–127CrossRefGoogle Scholar
  58. 58.
    Miralles P, Church TL, Harris AT (2012) Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environ Sci Technol 46:9224–9239PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Pérez-de-Luque A (2017) Interaction of nanomaterials with plants: what do we need for real applications in agriculture? Front Environ Sci 5:12CrossRefGoogle Scholar
  60. 60.
    Zhang F, Wang R, Xiao Q, Wang Y, Zhang J (2006) Effects of slow/controlled-release fertilizer cemented and coated by nano-materials on biology. II Effects of slow/controlled-release fertilizer cemented and coated by nano-materials on plants. Nanoscience 11:18–26Google Scholar
  61. 61.
    Cañas JE, Long M, Nations S, Vadan R, Dai L, Luo M, Ambikapathi R, Lee EH, Olszyk D (2008) Effects of functionalized and nonfunctionalized single-walled carbon nanotubes on root elongation of select crop species. Environ Toxicol Chem 27:1922–1931PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Zhu H, Han J, Xiao JQ, Jin Y (2008) Uptake, translocation, and accumulation of manufactured iron oxide nanoparticles by pumpkin plants. J Environ Monit 10:713–717PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Grün M, Lauer I, Unger KK (1997) The synthesis of micrometer- and submicrometer-size spheres of ordered mesoporous oxide MCM-41. Adv Mater 9:254–257CrossRefGoogle Scholar
  65. 65.
    Wu S-H, Mou C-Y, Lin H-P (2013) Synthesis of mesoporous silica nanoparticles. Chem Soc Rev 42:3862–3875PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Slowing I, Trewyn BG, Lin VS (2006) Effect of surface functionalization of MCM-41-type mesoporous silica nanoparticles on the endocytosis by human cancer cells. J Am Chem Soc 128:14792–14793PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Lim MH, Blanford CF, Stein A (1998) Synthesis of ordered microporous silicates with organosulfur surface groups and their applications as solid acid catalysts. Chem Mater 102:467–470CrossRefGoogle Scholar
  68. 68.
    Lai CY, Trewyn BG, Jeftinija DM, Jeftinija K, Xu S, Jeftinija S, Lin VS (2003) A mesoporous silica nanosphere-based carrier system with chemically removable CdS nanoparticle caps for stimuli-responsive controlled release of neurotransmitters and drug molecules. J Am Chem Soc 125:4451–4459PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Frens G (1973) Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nat Phys Sci 241:20–22CrossRefGoogle Scholar
  70. 70.
    Brust M, Walker M, Bethell D, Schiffrin DJ, Whyman R (1994) Synthesis of thiol-derivatised gold nanoparticles in a two-phase liquid–liquid system. J Chem Soc Chem Commun 7:801–802CrossRefGoogle Scholar
  71. 71.
    Zhao P, Li N, Astruc D (2013) State of the art in gold nanoparticle synthesis. Coord Chem Rev 257:638–665CrossRefGoogle Scholar
  72. 72.
    Pérez-Juste J, Pastoriza-Santos I, Liz-Marzán LM, Mulvaney P (2005) Gold nanorods: synthesis, characterization and applications. Coord Chem Rev 249:1870–1901CrossRefGoogle Scholar
  73. 73.
    Bhattacharjee S (2016) DLS and zeta potential – what they are and what they are not? J Control Release 235:337–351PubMedCrossRefGoogle Scholar
  74. 74.
    Klein TM, Wolf ED, Wu R, Sanford JC (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327:70–73CrossRefGoogle Scholar
  75. 75.
    Roizenblatt R, Weiland JD, Carcieri S, Qiu G, Behrend M, Humayun MS, Chow RH (2006) Nanobiolistic delivery of indicators to the living mouse retina. J Neurosci Methods 153:154–161PubMedCrossRefGoogle Scholar
  76. 76.
    Arsenault J, O’Brien JA (2013) Optimized heterologous transfection of viable adult organotypic brain slices using an enhanced gene gun. BMC Res Notes 6:544PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    O’Brien JA, Lummis SC (2011) Nano-biolistics: a method of biolistic transfection of cells and tissues using a gene gun with novel nanometer-sized projectiles. BMC Biotechnol 11:66PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Lee P-W, Peng S-F, Su C-J, Mi FL, Chen HL, Wei MC, Lin HJ, Sung HW (2008) The use of biodegradable polymeric nanoparticles in combination with a low-pressure gene gun for transdermal DNA delivery. Biomaterials 29:742–751PubMedCrossRefGoogle Scholar
  79. 79.
    Lee P-W, Hsu S-H, Tsai J-S, Chen FR, Huang PJ, Ke CJ, Liao ZX, Hsiao CW, Lin HJ, Sung HW (2010) Multifunctional core-shell polymeric nanoparticles for transdermal DNA delivery and epidermal Langerhans cells tracking. Biomaterials 31:2425–2434PubMedCrossRefGoogle Scholar
  80. 80.
    Huang HN, Li TL, Chan YL, Chen CL, Wu CJ (2009) Transdermal immunization with low-pressure-gene-gun mediated chitosan-based DNA vaccines against Japanese encephalitis virus. Biomaterials 30:6017–6025PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Raji JA, Frame B, Little D, Santoso TJ, Wang K (2018) Agrobacterium- and biolistic-mediated transformation of maize b104 inbred. In: Lagrimini LM (ed) Maize: methods and protocols. Springer, New York, NY, pp 15–40CrossRefGoogle Scholar
  82. 82.
    Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun 7:13274PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Ismagul A, Yang N, Maltseva E, Iskakova G, Mazonka I, Skiba Y, Bi H, Eliby S, Jatayev S, Shavrukov Y, Borisjuk N, Langridge P (2018) A biolistic method for high-throughput production of transgenic wheat plants with single gene insertions. BMC Plant Biol 18:135PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Kumari M, Rai AK, Devanna BN, Singh PK, Kapoor R, Rajashekara H, Prakash G, Sharma V, Sharma TR (2017) Co-transformation mediated stacking of blast resistance genes Pi54 and Pi54rh in rice provides broad spectrum resistance against Magnaporthe oryzae. Plant Cell Rep 36:1747–1755PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Srivastava V, Underwood JL, Zhao S (2017) Dual-targeting by CRISPR/Cas9 for precise excision of transgenes from rice genome. Plant Cell Tissue Organ Cult 129:153–160CrossRefGoogle Scholar
  87. 87.
    Chaithra N, Gowda RPH, Guleria N (2015) Transformation of tomato with Cry2ax1 by biolistic gun method for fruit borer resistance. Int J Agric Environ Biotechnol 8:795–803CrossRefGoogle Scholar
  88. 88.
    Kumar N, Galli M, Ordon J, Stuttmann J, Kogel KH, Imani J (2018) Further analysis of barley MORC1 using a highly efficient RNA-guided Cas9 gene-editing system. Plant Biotechnol J 16:1892–1903PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Rafsanjani MS, Alvari A, Samim M, Hejazi MA, Abdin MZ (2012) Application of novel nanotechnology strategies in plant biotransformation: a contemporary overview. Recent Pat Biotechnol 6:69–79PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Zalewski W, Orczyk W, Gasparis S, Nadolska-Orczyk A (2012) HvCKX2 gene silencing by biolistic or Agrobacterium-mediated transformation in barley leads to different phenotypes. BMC Plant Biol 12:206PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Alok A, Sharma S, Kumar J, Verma S, Sood H (2017) Engineering in plant genome using Agrobacterium: progress and future. In: Kalia VC, Saini AK (eds) Metabolic engineering for bioactive compounds: Strategies and processes. Springer, Singapore, pp 91–111CrossRefGoogle Scholar
  93. 93.
    Anand A, Trick HN, Gill BS, Muthukrishnan S (2003) Stable transgene expression and random gene silencing in wheat. Plant Biotechnol J 1:241–251PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Kohli A, Leech M, Vain P, Laurie DA, Christou P (1998) Transgene organization in rice engineered through direct DNA transfer supports a two-phase integration mechanism mediated by the establishment of integration hot spots. Proc Natl Acad Sci U S A 95:7203–7208PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Tassy C, Partier A, Beckert M, Feuillet C, Barret P (2014) Biolistic transformation of wheat: increased production of plants with simple insertions and heritable transgene expression. Plant Cell Tissue Organ Cult 119:171–181CrossRefGoogle Scholar
  96. 96.
    Martin-Ortigosa S, Valenstein JS, Lin VS-Y, Trewyn BG, Wang K (2012) Gold functionalized mesoporous silica nanoparticle mediated protein and DNA codelivery to plant cells via the biolistic method. Adv Funct Mater 22:3576–3582CrossRefGoogle Scholar
  97. 97.
    Martin-Ortigosa S, Valenstein JS, Sun W, Moeller L, Fang N, Trewyn BG, Lin VS, Wang K (2012) Parameters affecting the efficient delivery of mesoporous silica nanoparticle materials and gold nanorods into plant tissues by the biolistic method. Small 8:413–422PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Martin-Ortigosa S, Peterson DJ, Valenstein JS, Lin VS, Trewyn BG, Lyznik LA, Wang K (2014) Mesoporous silica nanoparticle-mediated intracellular cre protein delivery for maize genome editing via loxP site excision. Plant Physiol 164:537–547PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Mortazavi SE, Zohrabi Z (2018) Biolistic co-transformation of rice using gold nanoparticles. Iran Agric Res 37:75–82Google Scholar
  100. 100.
    Okuzaki A, Kida S, Watanabe J, Hirasawa I, Tabei Y (2013) Efficient plastid transformation in tobacco using small gold particles (0.07–0.3 μm). Plant Biotechnol 30:65–72CrossRefGoogle Scholar
  101. 101.
    Demirer GS, Zhang H, Goh NS, Pinals RL, Chang R, Landry MP (2019). Carbon Nanocarriers Deliver siRNA to Intact Plant Cells for Efficient Gene Knockdown. bioRxiv, 564427Google Scholar
  102. 102.
    Zhang H, Demirer GS, Zhang H, Ye T, Goh NS, Aditham AJ, Cunningham FJ, Fan C, Landry MP (2019) DNA nanostructures coordinate gene silencing in mature plants. Proc Natl Acad Sci 116(15):7543–7548Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2020

Authors and Affiliations

  • Francis J. Cunningham
    • 1
  • Gozde S. Demirer
    • 1
  • Natalie S. Goh
    • 1
  • Huan Zhang
    • 1
  • Markita P. Landry
    • 1
    • 2
    • 3
    Email author
  1. 1.Department of Chemical and Biomolecular EngineeringUniversity of CaliforniaBerkeleyUSA
  2. 2.California Institute for Quantitative Biosciences, QB3University of CaliforniaBerkeleyUSA
  3. 3.Chan-Zuckerberg BiohubSan FranciscoUSA

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