Skip to main content
SpringerLink
Log in

Particle bombardment technology and its applications in plants

Molecular Biology Reports volume 47, pages 9831–9847 (2020)Cite this article

Abstract

Particle bombardment, or biolistics, has emerged as an excellent alternative approach for plant genetic transformation which circumvents the limitations of Agrobacterium-mediated genetic transformation. The method has no biological constraints and can transform a wide range of plant species. Besides, it has been the most efficient way to achieve organelle transformation (for both chloroplasts and mitochondria) so far. Along with the recent advances in genome editing technologies, conventional gene delivery tools are now being repurposed to deliver targeted gene editing reagents into the plants. One of the key advantages is that the particle bombardment allows DNA-free gene editing of the genome. It enables the direct delivery of proteins, RNAs, and RNPs into plants. Owing to the versatility and wide-range applicability of the particle bombardment, it will likely remain one of the major genetic transformation methods in the future. This article provides an overview of the current status of particle bombardment technology and its applications in the field of plant research and biotechnology.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

References

  1. Samal KC, Rout GR (2018) Chapter 10 - genetic ımprovement of vegetables using transgenic technology. In: Rout GR, Peter KV (eds) Genetic engineering of horticultural crops. Academic Press, Cambridge, pp 193–224

    Google Scholar 

  2. Sanagala R, Moola AK, Bollipo Diana RK (2017) A review on advanced methods in plant gene targeting. J Genet Eng Biotechnol 15(2):317–321. https://doi.org/10.1016/j.jgeb.2017.07.004

    Article  PubMed  PubMed Central  Google Scholar 

  3. Baltes NJ, Gil-Humanes J, Voytas DF (2017) Chapter one - genome engineering and agriculture: opportunities and challenges. In: Weeks DP, Yang B (eds) Progress in molecular biology and translational science, vol 149. Academic Press, Cambridge, pp 1–26

    Google Scholar 

  4. De Block M, Herrera-Estrella L, Van Montagu M, Schell J, Zambryski P (1984) Expression of foreign genes in regenerated plants and in their progeny. EMBO J 3(8):1681

    PubMed  PubMed Central  Google Scholar 

  5. Sivamani E, DeLong RK, Qu R (2009) Protamine-mediated DNA coating remarkably improves bombardment transformation efficiency in plant cells. Plant Cell Rep 28(2):213–221

    CAS  PubMed  Google Scholar 

  6. Ozyigit II, Can H, Dogan I (2020) Phytoremediation using genetically engineered plants to remove metals: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-020-01095-6

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Que Q, Chilton MM, Elumalai S, Zhong H, Dong S, Shi L (2019) Repurposing macromolecule delivery tools for plant genetic modification in the era of precision genome engineering. Methods Mol Biol 1864:3–18. https://doi.org/10.1007/978-1-4939-8778-8_1

    Article  CAS  PubMed  Google Scholar 

  9. Shiboleth Y, Tzfira T (2012) 7 - Agrobacterium-mediated plant genetic transformation. In: Altman A, Hasegawa PM (eds) Plant biotechnology and agriculture. Academic Press, San Diego, pp 99–116

    Google Scholar 

  10. Ozyigit II, Dogan I, Tarhan EA (2013) Agrobacterium rhizogenes-mediated transformation and its biotechnological applications in crops. In: Crop improvement. Springer, New York

    Google Scholar 

  11. Ozyigit II (2012) Agrobacterium tumefaciens and its use in plant biotechnology. In: Crop production for agricultural improvement. Springer, New York

    Google Scholar 

  12. 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 15–40

    Google Scholar 

  13. Hiei Y, Ishida Y, Komari T (2014) Progress of cereal transformation technology mediated by Agrobacterium tumefaciens. Front Plant Sci 5:628. https://doi.org/10.3389/fpls.2014.00628

    Article  PubMed  PubMed Central  Google Scholar 

  14. Li F, Li M, Zhan C, Wang S (2015) A reliable and high-efficiency Agrobacterium tumefaciens-mediated transformation system of Pogonatherum paniceum embryogenic callus using GFP as a reporter gene. PCTOC 120(1):155–165. https://doi.org/10.1007/s11240-014-0589-y

    Article  CAS  Google Scholar 

  15. Singh RK, Prasad M (2016) Advances in Agrobacterium tumefaciens-mediated genetic transformation of graminaceous crops. Protoplasma 253(3):691–707. https://doi.org/10.1007/s00709-015-0905-3

    Article  CAS  PubMed  Google Scholar 

  16. Quispe-Huamanquispe DG, Gheysen G, Kreuze JF (2017) Horizontal gene transfer contributes to plant evolution: the case of Agrobacterium T-DNAs. Front Plant Sci. https://doi.org/10.3389/fpls.2017.02015

    Article  PubMed  PubMed Central  Google Scholar 

  17. Sanford JC, Klein TM, Wolf ED, Allen N (1987) Delivery of substances into cells and tissues using a particle bombardment process. Particul Sci Technol 5(1):27–37

    CAS  Google Scholar 

  18. Matsumoto TK, Gonsalves D (2012) 8 - Biolistic and other non-Agrobacterium technologies of plant transformation. In: Altman A, Hasegawa PM (eds) Plant biotechnology and agriculture. Academic Press, San Diego, pp 117–129

    Google Scholar 

  19. Grevich JJ, Daniell H (2005) Chloroplast genetic engineering: recent advances and future perspectives. Crit Rev Plant Sci 24(2):83–107

    CAS  Google Scholar 

  20. Altpeter F, Baisakh N, Beachy R, Bock R, Capell T, Christou P, Daniell H, Datta K, Datta S, Dix PJ (2005) Particle bombardment and the genetic enhancement of crops: myths and realities. Mol Breed 15(3):305–327

    Google Scholar 

  21. Sanford JC (2000) The development of the biolistic process. Vitro Cell Dev Biol Plant 36(5):303–308. https://doi.org/10.1007/s11627-000-0056-9

    Article  Google Scholar 

  22. Kikkert JR, Vidal JR, Reisch BI (2004) Stable transformation of plant cells by particle bombardment/biolistics. In: Transgenic plants: methods and protocols. Springer, New York

    Google Scholar 

  23. Twyman RM, Christou P (2004) Plant transformation technology: particle bombardment. In: Christou P, Klee H (eds) Handbook of plant biotechnology. Wiley, Hoboken

    Google Scholar 

  24. Klein TM, Wolf E, Wu R, Sanford J (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327(6117):70–73

    CAS  Google Scholar 

  25. Christou P, McCabe DE, Swain WF (1988) Stable transformation of soybean callus by DNA-coated gold particles. Plant Physiol 87(3):671–674

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240(4858):1534–1538

    CAS  PubMed  Google Scholar 

  27. Johnston SA, Anziano PQ, Shark K, Sanford JC, Butow RA (1988) Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 240(4858):1538–1541

    CAS  PubMed  Google Scholar 

  28. 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. PNAS 85(22):8502–8505

    CAS  PubMed  Google Scholar 

  29. Klein TM, Fromm M, Weissinger A, Tomes D, Schaaf S, Sletten M, Sanford JC (1988) Transfer of foreign genes into intact maize cells with high-velocity microprojectiles. PNAS 85(12):4305–4309

    CAS  PubMed  Google Scholar 

  30. McCabe DE, Swain WF, Martinell BJ, Christou P (1988) Stable transformation of soybean (Glycine Max) by particle acceleration. Nat Biotechnol 6(8):923–926. https://doi.org/10.1038/nbt0888-923

    Article  Google Scholar 

  31. Christou P (1992) Genetic transformation of crop plants using microprojectile bombardment. Plant J 2(3):275–281

    CAS  Google Scholar 

  32. Finer J, Finer K, Ponappa T (2000) Particle bombardment mediated transformation. In: Plant biotechnology. Springer, New York

    Google Scholar 

  33. Plackett AR, Huang L, Sanders HL, Langdale JA (2014) High-efficiency stable transformation of the model fern species Ceratopteris richardii via microparticle bombardment. Plant Physiol 165(1):3–14. https://doi.org/10.1104/pp.113.231357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800. https://doi.org/10.1111/pbi.12312

    Article  CAS  PubMed  Google Scholar 

  35. Yu Q, Lutz KA, Maliga P (2017) Efficient plastid transformation in Arabidopsis. Plant Physiol 175(1):186–193. https://doi.org/10.1104/pp.17.00857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Corbin C, Lafontaine F, Sepúlveda LJ, Carqueijeiro I, Courtois M, Lanoue A, Dugé de Bernonville T, Besseau S, Glévarec G, Papon N, Atehortúa L, Giglioli-Guivarch N, Clastre M, St-Pierre B, Oudin A, Courdavault V (2017) Virus-induced gene silencing in Rauwolfia species. Protoplasma 254(4):1813–1818. https://doi.org/10.1007/s00709-017-1079-y

    Article  CAS  PubMed  Google Scholar 

  37. Akbar S, Tahir M, Wang M-B, Liu Q (2017) Expression analysis of hairpin RNA carrying sugarcane mosaic virus (SCMV) derived sequences and transgenic resistance development in a model rice plant. BioMed Res Int. https://doi.org/10.1155/2017/1646140

    Article  PubMed  PubMed Central  Google Scholar 

  38. McCabe D, Christou P (1993) Direct DNA transfer using electric discharge particle acceleration (ACCELL technology). Plant Cell Tiss Org Cult 33(3):227–236

    CAS  Google Scholar 

  39. Christou P, McCabe D (1992) Particle gun transformation of crop plants using electric discharge (ACCELL™ Technology). Probe: newsletter for the USDA Plant Genome Research Program (USA).

  40. Keller G, Spatola L, McCabe D, Martinell B, Swain W, John M (1997) Transgenic cotton resistant to herbicide bialaphos. Transgenic Res 6(6):385–392

    CAS  Google Scholar 

  41. Finer J, Vain P, Jones M, McMullen M (1992) Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep 11(7):323–328. https://doi.org/10.1007/BF00233358

    Article  CAS  PubMed  Google Scholar 

  42. Latha AM, Rao KV, Reddy TP, Reddy VD (2006) Development of transgenic pearl millet (Pennisetum glaucum (L.) R. Br.) plants resistant to downy mildew. Plant Cell Rep 25(9):927–935. https://doi.org/10.1007/s00299-006-0141-6

    Article  CAS  PubMed  Google Scholar 

  43. Hernandez-Garcia C, Bouchard R, Rushton P, Jones M, Chen X, Timko M, Finer J (2010) High level transgenic expression of soybean (Glycine max) GmERF and Gmubi gene promoters isolated by a novel promoter analysis pipeline. BMC Plant Biol 10(1):237

    PubMed  PubMed Central  Google Scholar 

  44. Kuriakose B, Du Toit ES, Jordaan A (2012) Transient gene expression assays in rose tissues using a Bio-Rad Helios® hand-held gene gun. S Afr J Bot 78:307–311. https://doi.org/10.1016/j.sajb.2011.06.002

    Article  CAS  Google Scholar 

  45. Joshi JB, Geetha S, Singh B, Kumar K, Kokiladevi E, Arul L, Balasubramanian P, Sudhakar D (2015) A maize α-zein promoter drives an endosperm-specific expression of transgene in rice. Physiol Mol Biol Plants 21(1):35–42

    CAS  PubMed  Google Scholar 

  46. Russell SH, Hoopes JL, Odell JT (1992) Directed excision of a transgene from the plant genome. MGG 234(1):49–59

    CAS  PubMed  Google Scholar 

  47. Mazuś B, Krysiak C, Buchowicz J (2000) Tungsten particle-induced nicking of supercoiled plasmid DNA. Plasmid 44(1):89–93

    PubMed  Google Scholar 

  48. 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(1):135. https://doi.org/10.1186/s12870-018-1326-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rasco-Gaunt S, Riley A, Barcelo P, Lazzeri P (1999) Analysis of particle bombardment parameters to optimise DNA delivery into wheat tissues. Plant Cell Rep 19(2):118–127

    CAS  PubMed  Google Scholar 

  50. Fu X, Fontana S, Bong BB, Tinjuangjun P, Sudhakar D, Twyman RM, Christou P, Kohli A (2000) Linear transgene constructs lacking vector backbone sequences generate low-copy-number transgenic plants with simple integration patterns. Transgenic Res 9(1):11–19

    CAS  PubMed  Google Scholar 

  51. 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(1):171–181

    CAS  Google Scholar 

  52. Mészáros K, Éva C, Kiss T, Bányai J, Kiss E, Téglás F, Láng L, Karsai I, Tamás L (2014) Generating marker-free transgenic wheat using minimal gene cassette and cold-ınducible Cre/Lox system. Plant Mol Biol Rep 33:1–11

    Google Scholar 

  53. Petrillo CP, Carneiro NP, Purcino AÁC, Carvalho CHS, Alves JD, Carneiro AA (2008) Optimization of particle bombardment parameters for the genetic transformation of Brazilian maize inbred lines. Pesqui Agropecu Bras 43:371–378

    Google Scholar 

  54. McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2(2):163–171. https://doi.org/10.1105/tpc.2.2.163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Zhang W, Wu R (1988) Efficient regeneration of transgenic plants from rice protoplasts and correctly regulated expression of the foreign gene in the plants. Theor Appl Genet 76(6):835–840. https://doi.org/10.1007/BF00273668

    Article  CAS  PubMed  Google Scholar 

  56. Millar AJ, Short SR, Hiratsuka K, Chua N-H, Kay SA (1992) Firefly luciferase as a reporter of regulated gene expression in higher plants. Plant Mol Biol Rep 10(4):324–337

    CAS  Google Scholar 

  57. Nguyen TX, Sticklen M (2013) Barley HVA1 gene confers drought and salt tolerance in transgenic maize (Zea mays L.). Adv Crop Sci Technol 1(105):2

    Google Scholar 

  58. Hamada H, Linghu Q, Nagira Y, Miki R, Taoka N, Imai R (2017) An in planta biolistic method for stable wheat transformation. Sci Rep 7(1):1–8

    Google Scholar 

  59. Cho M-J, Cerf DC, Xu D, Zhao Z-Y (2015) Direct and continuous root alone or root/shoot production from transgenic events derived from green regenerative tissues and ıts applications. US Patent 20,150,037,807,

  60. Kohli A, Twyman RM, Abranches R, Wegel E, Stoger E, Christou P (2003) Transgene integration, organization and interaction in plants. Plant Mol Biol 52(2):247–258

    CAS  PubMed  Google Scholar 

  61. 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. PNAS 95(12):7203–7208

    CAS  PubMed  Google Scholar 

  62. Gelvin SB (1998) Multigene plant transformation: More is better! Nat Biotechnol 16(11):1009–1010

    CAS  PubMed  Google Scholar 

  63. Pawlowski WP, Somers DA (1998) Transgenic DNA integrated into the oat genome is frequently interspersed by host DNA. PNAS 95(21):12106–12110

    CAS  PubMed  Google Scholar 

  64. Svitashev SK, Somers DA (2001) Genomic interspersions determine the size and complexity of transgene loci in transgenic plants produced by microprojectile bombardment. Genome 44(4):691–697

    CAS  PubMed  Google Scholar 

  65. Mookkan M (2018) Particle bombardment - mediated gene transfer and GFP transient expression in Seteria viridis. Plant Signal Behav 13(4):e1441657–e1441657. https://doi.org/10.1080/15592324.2018.1441657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ohno R, Takumi S (2015) Extracellular trafficking of a wheat cold-responsive protein, WLT10. J Plant Physiol 174:71–74

    CAS  PubMed  Google Scholar 

  67. Chen J, Yi Q, Cao Y, Wei B, Zheng L, Xiao Q, Xie Y, Gu Y, Li Y, Huang H, Wang Y, Hou X, Long T, Zhang J, Liu H, Liu Y, Yu G, Huang Y (2016) ZmbZIP91 regulates expression of starch synthesis-related genes by binding to ACTCAT elements in their promoters. J Exp Bot 67(5):1327–1338. https://doi.org/10.1093/jxb/erv527

    Article  CAS  PubMed  Google Scholar 

  68. Levy A, El-Mochtar C, Wang C, Goodin M, Orbovic V (2018) A new toolset for protein expression and subcellular localization studies in citrus and its application to citrus tristeza virus proteins. Plant Methods 14(1):2. https://doi.org/10.1186/s13007-017-0270-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Wiltshire EJ, Eady CC, Collings DA (2017) Induction of anthocyanin in the inner epidermis of red onion leaves by environmental stimuli and transient expression of transcription factors. Plant Cell Rep 36(6):987–1000. https://doi.org/10.1007/s00299-017-2132-1

    Article  CAS  PubMed  Google Scholar 

  70. Yu W, Yau YY, Birchler JA (2016) Plant artificial chromosome technology and its potential application in genetic engineering. Plant Biotechnol J 14(5):1175–1182

    CAS  PubMed  Google Scholar 

  71. Koziel MG, Beland GL, Bowman C, Carozzi NB, Crenshaw R, Crossland L, Dawson J, Desai N, Hill M, Kadwell S (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Nat Biotechnol 11(2):194–200

    CAS  Google Scholar 

  72. Sarangi S, Mandal C, Dutta S, Mukherjee P, Mondal R, Kumar SPJ, Choudhury PR, Singh VP, Tripathi DK, Mandal AB (2019) Microprojectile based particle bombardment in development of transgenic indica rice involving AmSOD gene to impart tolerance to salinity. Plant Gene 19:100183. https://doi.org/10.1016/j.plgene.2019.100183

    Article  CAS  Google Scholar 

  73. Du H, Shen X, Huang Y, Huang M, Zhang Z (2016) Overexpression of Vitreoscilla hemoglobin increases waterlogging tolerance in Arabidopsis and maize. BMC Plant Biol 16:35. https://doi.org/10.1186/s12870-016-0728-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Daniell H, Dhingra A (2002) Multigene engineering: dawn of an exciting new era in biotechnology. Curr Opin Biotechnol 13(2):136–141

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Svab Z, Hajdukiewicz P, Maliga P (1990) Stable transformation of plastids in higher plants. PNAS 87(21):8526–8530. https://doi.org/10.1073/pnas.87.21.8526

    Article  CAS  PubMed  Google Scholar 

  76. Wang Y-P, Wei Z-Y, Zhang Y-Y, Lin C-J, Zhong X-F, Wang Y-L, Ma J-Y, Ma J, Xing S-C (2015) Chloroplast-expressed MSI-99 in tobacco improves disease resistance and displays inhibitory effect against rice blast fungus. Int J Mol Sci 16(3):4628–4641

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Muralikrishna N, Srinivas K, Kumar KB, Sadanandam A (2016) Stable plastid transformation in Scoparia dulcis L. Physiol Mol Biol Plants 22(4):575–581. https://doi.org/10.1007/s12298-016-0386-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Zhang C, Yang C, Whitham SA, Hill JH (2009) Development and use of an efficient DNA-based viral gene silencing vector for soybean. Mol Plant-Microbe Interact 22(2):123–131

    CAS  PubMed  Google Scholar 

  79. Li C, Yamagishi N, Kasajima I, Yoshikawa N (2019) Virus-induced gene silencing and virus-induced flowering in strawberry (Fragaria × ananassa) using apple latent spherical virus vectors. Hortic Res 6:18–18. https://doi.org/10.1038/s41438-018-0106-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Klessig DF, Kang H-g, Kogel K-h, Manosalva P (2014) Compositions and Methods for the Generation of Disease Resistant Crops. US Patent 20,140,157,451,

  81. Fisher NM (2014) Gene silencing in bread wheat (Triticum aestivum L.) following a biolistics approach. http://hdl.handle.net/10019.1/86591

  82. Martin-Ortigosa S, Wang K (2014) Proteolistics: a biolistic method for intracellular delivery of proteins. Transgenic Res 23(5):743–756

    CAS  PubMed  Google Scholar 

  83. Xu C, Cheng Z, Yu W (2012) Construction of rice mini-chromosomes by telomere-mediated chromosomal truncation. Plant J 70(6):1070–1079

    CAS  PubMed  Google Scholar 

  84. Gaeta RT, Masonbrink RE, Zhao C, Sanyal A, Krishnaswamy L, Birchler JA (2013) In vivo modification of a maize engineered minichromosome. Chromosoma 122(3):221–232. https://doi.org/10.1007/s00412-013-0403-3

    Article  CAS  PubMed  Google Scholar 

  85. Yuan J, Shi Q, Guo X, Liu Y, Su H, Guo X, Lv Z, Han F (2017) Site-specific transfer of chromosomal segments and genes in wheat engineered chromosomes. J Genet Genomics 44(11):531–539. https://doi.org/10.1016/j.jgg.2017.08.005

    Article  PubMed  Google Scholar 

  86. Bothwell JH, Brownlee C, Hetherington AM, Ng CKY, Wheeler GL, McAinsh MR (2006) Biolistic delivery of Ca2+ dyes into plant and algal cells. Plant J 46(2):327–335

    CAS  PubMed  Google Scholar 

  87. 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(1):13274. https://doi.org/10.1038/ncomms13274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Mao Y, Botella JR, Liu Y, Zhu J-K (2019) Gene editing in plants: progress and challenges. Nat Sci Rev 6(3):421–437

    CAS  Google Scholar 

  89. Zhang H-X, 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 

  90. Raina M, Pandotra P, Salgotra R, Ali S, Mir ZA, Bhat JA, Ali A, Tyagi A, Upadhahy D (2018) Genetic engineering and environmental risk. In: Modern age environmental problems and their remediation. Springer, New York

    Google Scholar 

  91. Li Z, Liu Z-B, Xing A, Moon BP, Koellhoffer JP, Huang L, Ward RT, Clifton E, Falco SC, Cigan AM (2015) Cas9-guide RNA directed genome editing in soybean. Plant Physiol 169(2):960. https://doi.org/10.1104/pp.15.00783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Liang Z, Chen K, Li T, Zhang Y, Wang Y, Zhao Q, Liu J, Zhang H, Liu C, Ran Y (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8(1):1–5

    Google Scholar 

  93. Knittel N, Gruber V, Hahne G, Lénée P (1994) Transformation of sunflower (Helianthus annuus L.): a reliable protocol. Plant Cell Rep 14(2–3):81–86

    CAS  PubMed  Google Scholar 

  94. Wiebke-Strohm B, Droste A, Pasquali G, Osorio MB, Bücker-Neto L, Passaglia LMP, Bencke M, Homrich MS, Margis-Pinheiro M, Bodanese-Zanettini MH (2011) Transgenic fertile soybean plants derived from somatic embryos transformed via the combined DNA-free particle bombardment and Agrobacterium system. Euphytica 177(3):343–354

    Google Scholar 

  95. 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(12):1093–1100

    Google Scholar 

  96. Zorrilla-López U, Masip G, Arjó G, Bai C, Banakar R, Bassie L, Berman J, Farré G, Miralpeix B, Pérez-Massot E (2013) Engineering metabolic pathways in plants by multigene transformation. Int J Dev Biol 57:565–576

    PubMed  Google Scholar 

  97. Elghabi Z, Ruf S, Bock R (2011) Biolistic co-transformation of the nuclear and plastid genomes. Plant J 67(5):941–948

    CAS  PubMed  Google Scholar 

  98. Sharma M, Bennewitz B, Klösgen RB (2018) Dual or not dual? Comparative analysis of fluorescence microscopy-based approaches to study organelle targeting specificity of nuclear-encoded plant proteins. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01350

    Article  PubMed  PubMed Central  Google Scholar 

  99. Zhang L, Gu L, Ringler P, Smith S, Rushton PJ, Shen QJ (2015) Three WRKY transcription factors additively repress abscisic acid and gibberellin signaling in aleurone cells. Plant Sci 236:214–222. https://doi.org/10.1016/j.plantsci.2015.04.014

    Article  CAS  PubMed  Google Scholar 

  100. Zór K, Mark C, Heiskanen A, Madsen CK, Dufva M, Emnéus J, Brinch-Pedersen H, Finnie C (2017) Immobilisation of barley aleurone layers enables parallelisation of assays and analysis of transient gene expression in single cells. Plant Physiol Biochem 118:71–76. https://doi.org/10.1016/j.plaphy.2017.06.008

    Article  CAS  PubMed  Google Scholar 

  101. Narra M, Ellendula R, Kota S, Kalva B, Velivela Y, Abbagani S (2017) Efficient genetic transformation of Momordica charantia L. by microprojectile bombardment. 3 Biotech 8(1):2. https://doi.org/10.1007/s13205-017-1017-x

    Article  PubMed  PubMed Central  Google Scholar 

  102. Wu H, Acanda Y, Jia H, Wang N, Zale J (2016) Biolistic transformation of Carrizo citrange (Citrus sinensis Osb × Poncirus trifoliata L. Raf.). Plant Cell Rep 35(9):1955–1962. https://doi.org/10.1007/s00299-016-2010-2

    Article  CAS  PubMed  Google Scholar 

  103. Ramírez Rivera NG, García-Salinas C, Aragão FJL, Díaz de la Garza RI (2016) Metabolic engineering of folate and its precursors in Mexican common bean (Phaseolus vulgaris L.). Plant Biotechnol J 14(10):2021–2032. https://doi.org/10.1111/pbi.12561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Allam MA, Saker MM (2017) Microprojectile bombardment transformation of date palm using the ınsecticidal cholesterol oxidase (ChoA) gene. In: Al-Khayri JM, Jain SM, Johnson DV (eds) Date palm biotechnology protocols volume I: tissue culture applications. Springer, New York, NY, pp 281–293

    Google Scholar 

  105. Bhattacharyya J, Chakraborty A, Roy S, Pradhan S, Mitra J, Chakraborty M, Manna A, Sikdar N, Chakraborty S, Sen S (2015) Genetic transformation of cultivated jute (Corchorus capsularis L.) by particle bombardment using apical meristem tissue and development of stable transgenic plant. Plant Cell Tissue Organ Cult 1:11. https://doi.org/10.1007/s11240-014-0702-2

    Article  CAS  Google Scholar 

  106. Zhao Y, Zhang Y, Su P, Yang J, Huang L, Gao W (2018) Genetic transformation system for woody plant Tripterygium wilfordii and its application to product natural celastrol. Front Plant Sci 8:2221–2221. https://doi.org/10.3389/fpls.2017.02221

    Article  PubMed  PubMed Central  Google Scholar 

  107. Yu L-X, Shen X, Setter TL (2015) Molecular and functional characterization of two drought-induced zinc finger proteins, ZmZnF1 and ZmZnF2 from maize kernels. Environ Exp Bot 111:13–20. https://doi.org/10.1016/j.envexpbot.2014.10.004

    Article  CAS  Google Scholar 

  108. Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS 8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotechnol J 15(2):207–216

    CAS  PubMed  Google Scholar 

  109. Guerra FP, Reyes L, Vergara-Jaque A, Campos-Hernández C, Gutiérrez A, Pérez-Díaz J, Pérez-Díaz R, Blaudez D, Ruíz-Lara S (2015) Populus deltoides Kunitz trypsin inhibitor 3 confers metal tolerance and binds copper, revealing a new defensive role against heavy metal stress. Environ Exp Bot 115:28–37. https://doi.org/10.1016/j.envexpbot.2015.02.005

    Article  CAS  Google Scholar 

  110. Li J, Ban L, Wen H, Wang Z, Dzyubenko N, Chapurin V, Gao H, Wang X (2015) An aquaporin protein is associated with drought stress tolerance. Biochem Biophys Res Commun 459(2):208–213

    CAS  PubMed  Google Scholar 

  111. Skoulding NS, Chowdhary G, Deus MJ, Baker A, Reumann S, Warriner SL (2015) Experimental validation of plant peroxisomal targeting prediction algorithms by systematic comparison of in vivo import efficiency and in vitro PTS1 binding affinity. J Mol Biol 427(5):1085–1101. https://doi.org/10.1016/j.jmb.2014.12.003

    Article  CAS  PubMed  Google Scholar 

  112. Tang C, Deng L, Chang D, Chen S, Wang X, Kang Z (2016) TaADF3, an actin-depolymerizing factor, negatively modulates wheat resistance against Puccinia striiformis. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01214

    Article  PubMed  PubMed Central  Google Scholar 

  113. Jianyuan L, Xiaodong W, Lirong Z, Qingfang M, Na Z, Wenxiang Y, Daqun L (2017) A wheat NBS-LRR gene TaRGA19 participates in Lr19-mediated resistance to Puccinia triticina. Plant Physiol Biochem 119:1–8. https://doi.org/10.1016/j.plaphy.2017.08.009

    Article  CAS  PubMed  Google Scholar 

  114. Liew LC, Singh MB, Bhalla PL (2017) A novel role of the soybean clock gene LUX ARRHYTHMO in male reproductive development. Sci Rep 7:10605. https://doi.org/10.1038/s41598-017-10823-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Sutoh K, Washio K, Imai R, Wada M, Nakai T, Yamauchi D (2015) An N-terminal region of a Myb-like protein is involved in its intracellular localization and activation of a gibberellin-inducible proteinase gene in germinated rice seeds. Biosci Biotechnol Biochem 79(5):747–759. https://doi.org/10.1080/09168451.2014.998620

    Article  CAS  PubMed  Google Scholar 

  116. Lakra N, Nutan KK, Das P, Anwar K, Singla-Pareek SL, Pareek A (2015) A nuclear-localized histone-gene binding protein from rice (OsHBP1b) functions in salinity and drought stress tolerance by maintaining chlorophyll content and improving the antioxidant machinery. J Plant Physiol 176:36–46. https://doi.org/10.1016/j.jplph.2014.11.005

    Article  CAS  PubMed  Google Scholar 

  117. Xu J, Liu C, Li M, Hu J, Zhu L, Zeng D, Yang Y, Peng Y, Ruan B, Guo L, Li H (2015) A rice DEAD-box RNA helicase protein, OsRH17, suppresses 16S ribosomal RNA maturation in Escherichia coli. Gene 555(2):318–328. https://doi.org/10.1016/j.gene.2014.11.025

    Article  CAS  PubMed  Google Scholar 

  118. Miyamoto K, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2015) Overexpression of the bZIP transcription factor OsbZIP79 suppresses the production of diterpenoid phytoalexin in rice cells. J Plant Physiol 173:19–27. https://doi.org/10.1016/j.jplph.2014.09.001

    Article  CAS  PubMed  Google Scholar 

  119. Nandy S, Zhao S, Pathak BP, Manoharan M, Srivastava V (2015) Gene stacking in plant cell using recombinases for gene integration and nucleases for marker gene deletion. BMC Biotechnol 15(1):93

    PubMed  PubMed Central  Google Scholar 

  120. Jung J-W, Huy N-X, Kim H-B, Kim N-S, Van Giap D, Yang M-S (2017) Production of recombinant human acid α-glucosidase with high-mannose glycans in gnt1 rice for the treatment of Pompe disease. J Biotechnol 249:42–50. https://doi.org/10.1016/j.jbiotec.2017.03.033

    Article  CAS  PubMed  Google Scholar 

  121. Watanabe KA, Homayouni A, Gu L, Huang K-Y, Ho T-HD, Shen QJ (2017) Transcriptomic analysis of rice aleurone cells identified a novel abscisic acid response element. Plant Cell Environ 40(9):2004–2016. https://doi.org/10.1111/pce.13006

    Article  CAS  PubMed  Google Scholar 

  122. Kim M-Y, Kim T-G, Yang M-S (2017) Production and immunogenicity of Actinobacillus pleuropneumoniae ApxIIA protein in transgenic rice callus. Protein Expr Purif 132:116–123. https://doi.org/10.1016/j.pep.2016.05.010

    Article  CAS  PubMed  Google Scholar 

  123. 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(11):1747–1755. https://doi.org/10.1007/s00299-017-2189-x

    Article  CAS  PubMed  Google Scholar 

  124. Begemann MB, Gray BN, January E, Gordon GC, He Y, Liu H, Wu X, Brutnell TP, Mockler TC, Oufattole M (2017) Precise insertion and guided editing of higher plant genomes using Cpf1 CRISPR nucleases. Sci Rep 7(1):11606. https://doi.org/10.1038/s41598-017-11760-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Li J, Zhang X, Sun Y, Zhang J, Du W, Guo X, Li S, Zhao Y, Xia L (2018) Efficient allelic replacement in rice by gene editing: a case study of the NRT1. 1B gene. J Integr Plant Biol 60(7):536–540

    CAS  PubMed  Google Scholar 

  126. Li S, Li J, Zhang J, Du W, Fu J, Sutar S, Zhao Y, Xia L (2018) Synthesis-dependent repair of Cpf1-induced double strand DNA breaks enables targeted gene replacement in rice. J Exp Bot 69(20):4715–4721

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Toda E, Koiso N, Takebayashi A, Ichikawa M, Kiba T, Osakabe K, Osakabe Y, Sakakibara H, Kato N, Okamoto T (2019) An efficient DNA- and selectable-marker-free genome-editing system using zygotes in rice. Nat Plants 5(4):363–368. https://doi.org/10.1038/s41477-019-0386-z

    Article  CAS  PubMed  Google Scholar 

  128. Dong OX, Yu S, Jain R, Zhang N, Duong PQ, Butler C, Li Y, Lipzen A, Martin JA, Barry KW, Schmutz J, Tian L, Ronald PC (2020) Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nat Commun 11(1):1178. https://doi.org/10.1038/s41467-020-14981-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zhang Y, Ran Y, Nagy I, Lenk I, Qiu JL, Asp T, Jensen CS, Gao C (2020) Targeted mutagenesis in ryegrass (Lolium spp.) using the CRISPR/Cas9 system. Plant Biotechnol J. https://doi.org/10.1111/pbi.13359

    Article  PubMed  PubMed Central  Google Scholar 

  130. Belide S, Vanhercke T, Petrie JR, Singh SP (2017) Robust genetic transformation of sorghum (Sorghum bicolor L.) using differentiating embryogenic callus induced from immature embryos. Plant Methods 13(1):109. https://doi.org/10.1186/s13007-017-0260-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. De La Torre C, Finer J (2015) The intron and 5′ distal region of the soybean Gmubi promoter contribute to very high levels of gene expression in transiently and stably transformed tissues. Plant Cell Rep 34(1):111–120. https://doi.org/10.1007/s00299-014-1691-7

    Article  CAS  Google Scholar 

  132. Gao S, Yang Y, Wang C, Guo J, Zhou D, Wu Q, Su Y, Xu L, Que Y (2016) Transgenic sugarcane with a cry1Ac gene exhibited better phenotypic traits and enhanced resistance against sugarcane borer. PLoS ONE 11(4):e0153929. https://doi.org/10.1371/journal.pone.0153929

    Article  PubMed  PubMed Central  Google Scholar 

  133. Gao S, Yang Y, Xu L, Guo J, Su Y, Wu Q, Wang C, Que Y (2018) Particle bombardment of the cry2A gene cassette induces stem borer resistance in sugarcane. Int J Mol Sci 19(6):1692. https://doi.org/10.3390/ijms19061692

    Article  CAS  PubMed Central  Google Scholar 

  134. Tariq M, Khan A, Tabassum B, Toufiq N, Bhatti MU, Riaz S, Nasir IA, Husnain T (2018) Antifungal activity of chitinase II against Colletotrichum falcatum Went. causing red rot disease in transgenic sugarcane. Turk J Biol 42(1):45–53. https://doi.org/10.3906/biy-1709-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Augustine S, Ashwin Narayan J, Syamaladevi D, Appunu C, Chakravarthi M, Ravichandran V, Tuteja N, Subramonian N (2015) Overexpression of EaDREB2 and pyramiding of EaDREB2 with the pea DNA helicase gene (PDH45) enhance drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Cell Rep 34(2):247–263. https://doi.org/10.1007/s00299-014-1704-6

    Article  CAS  PubMed  Google Scholar 

  136. He L, Su C, Wang Y, Wei Z (2015) ATDOF5.8 protein is the upstream regulator of ANAC069 and is responsive to abiotic stress. Biochimie 110:17–24. https://doi.org/10.1016/j.biochi.2014.12.017

    Article  CAS  PubMed  Google Scholar 

  137. Sasaki N, Matsumaru M, Odaira S, Nakata A, Nakata K, Nakayama I, Yamaguchi K, Nyunoya H (2015) Transient expression of tobacco BBF1-related Dof proteins, BBF2 and BBF3, upregulates genes involved in virus resistance and pathogen defense. Physiol Mol Plant Pathol 89:70–77. https://doi.org/10.1016/j.pmpp.2014.12.005

    Article  CAS  Google Scholar 

  138. Yang G, Li J, Liu W, Yu Z, Shi Y, Lv B, Wang B, Han D (2015) Molecular cloning and characterization of MxNAS2, a gene encoding nicotianamine synthase in Malus xiaojinensis, with functions in tolerance to iron stress and misshapen flower in transgenic tobacco. Sci Hortic 183:77–86. https://doi.org/10.1016/j.scienta.2014.12.014

    Article  CAS  Google Scholar 

  139. Srinivas K, Muralikrishna N, Kumar KB, Raghu E, Mahender A, Kiranmayee K, Yashodahara V, Sadanandam A (2016) Biolistic transformation of Scoparia dulcis L. Physiol Mol Biol Plants 22(1):61–68. https://doi.org/10.1007/s12298-016-0338-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Osaki Y, Kodama Y (2017) Particle bombardment and subcellular protein localization analysis in the aquatic plant Egeria densa. PeerJ 5:e3779. https://doi.org/10.7717/peerj.3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Zhang K, Liu J, Zhang Y, Yang Z, Gao C (2015) Biolistic genetic transformation of a wide range of chinese elite wheat (Triticum aestivum L.) varieties. J Genet Genomics 42(1):39–42. https://doi.org/10.1016/j.jgg.2014.11.005

    Article  PubMed  Google Scholar 

  142. Miroshnichenko D, Ashin D, Pushin A, Dolgov S (2018) Genetic transformation of einkorn (Triticum monococcum L. ssp. monococcum L.), a diploid cultivated wheat species. BMC Biotechnol 18(1):68–68. https://doi.org/10.1186/s12896-018-0477-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Xue G-P, Drenth J, McIntyre CL (2015) TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. J Exp Bot 66(3):1025–1039. https://doi.org/10.1093/jxb/eru462

    Article  CAS  PubMed  Google Scholar 

  144. Han Y, Blechl A, Wang D (2015) The distribution of cotransformed transgenes in particle bombardment-mediated transformed wheat. Transgenic Res 24(6):1055–1063

    CAS  PubMed  Google Scholar 

  145. Cheng W, Li H-P, Zhang J-B, Du H-J, Wei Q-Y, Huang T, Yang P, Kong X-W, Liao Y-C (2015) Tissue-specific and pathogen-inducible expression of a fusion protein containing a Fusarium-specific antibody and a fungal chitinase protects wheat against Fusarium pathogens and mycotoxins. Plant Biotechnol J 13(5):664–674. https://doi.org/10.1111/pbi.12289

    Article  CAS  PubMed  Google Scholar 

  146. Gil-Humanes J, Wang Y, Liang Z, Shan Q, Ozuna CV, Sánchez-León S, Baltes NJ, Starker C, Barro F, Gao C (2017) High-efficiency gene targeting in hexaploid wheat using DNA replicons and CRISPR/Cas9. Plant J 89(6):1251–1262

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  148. Duan X, Hou Q, Liu G, Pang X, Niu Z, Wang X, Zhang Y, Li B, Liang R (2018) Expression of Pinellia pedatisecta lectin gene in transgenic wheat enhances resistance to wheat aphids. Molecules 23(4):748. https://doi.org/10.3390/molecules23040748

    Article  CAS  PubMed Central  Google Scholar 

  149. Zhang R, Liu J, Chai Z, Chen S, Bai Y, Zong Y, Chen K, Li J, Jiang L, Gao C (2019) Generation of herbicide tolerance traits and a new selectable marker in wheat using base editing. Nat Plants 5(5):480–485. https://doi.org/10.1038/s41477-019-0405-0

    Article  CAS  PubMed  Google Scholar 

  150. Hashem HA, Hassanein RA, Fahmy AH, Ibrahim AS, El Shihyh OM, Qaid EA (2018) Particle bombardment-mediated co-transformation of the Cht-2 gene in wheat and the associated changes in defense mechanisms in transgenic plants infected with Fusarium graminearum. Data Brief 21:1111–1118. https://doi.org/10.1016/j.dib.2018.09.130

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors thank to Bio-Rad Laboratories for providing the pictures of Biolistic® PDS-1000/He Particle Delivery System and Helios® Gene Gun. Also thankful to Biologist MSc. Asli Hocaoglu-Ozyigit for her technical support.

Author information

Authors and Affiliations

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

    Ibrahim Ilker Ozyigit

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

    Ibrahim Ilker Ozyigit

  3. Faculty of Science, Department of Molecular Biology and Genetics, Istanbul Medeniyet University, Uskudar, Istanbul, Turkey

    Kuaybe Yucebilgili Kurtoglu

Authors
  1. Ibrahim Ilker Ozyigit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kuaybe Yucebilgili Kurtoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

IIO had the idea for the article, KYK performed the literature search and drafted the review, KYK and IIO critically revised the work. Both authors read and approved the final manuscript.

Corresponding authors

Correspondence to Ibrahim Ilker Ozyigit or Kuaybe Yucebilgili Kurtoglu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human and/or animals rights

This study does not contain any parts with human participants or animals performed by any of the authors.

Informed consent

This study does not involve human participants, and a statement on welfare of animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ozyigit, I.I., Yucebilgili Kurtoglu, K. Particle bombardment technology and its applications in plants. Mol Biol Rep 47, 9831–9847 (2020). https://doi.org/10.1007/s11033-020-06001-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-020-06001-5

Keywords

search

Navigation