Skip to main content

Biolistic DNA Delivery and Its Applications in Sorghum bicolor

  • Protocol
  • First Online:
Biolistic DNA Delivery in Plants

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

Abstract

Biolistic DNA delivery has been considered a universal tool for genetic manipulation to transfer exotic genes to cells or tissues due to its simplicity, versatility, and high efficiency. It has been a preferred method for investigating plant gene function in most monocot crops. The first transgenic sorghum plants were successfully regenerated through biolistic DNA delivery in 1993, with a relatively low transformation efficiency of 0.3%. Since then, tremendous progress has been made in recent years where the highest transformation efficiency was reported at 46.6%. Overall, the successful biolistic DNA delivery system is credited to three fundamental cornerstones: robust tissue culture system, effective gene expression in sorghum, and optimal parameters of DNA delivery. In this chapter, the history, application, and current development of biolistic DNA delivery in sorghum are reviewed, and the prospect of sorghum genetic engineering is discussed.

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

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Mace ES, Tai SS, Gilding EK, Li YH, Prentis PJ, Bian LL, Campbell BC, Hu W, Innes DJ, Han X, Cruickshank A, Dai C, Frère C, Zhang H, Hunt CH, Wang X, Shatte T, Wang M, Su Z, Li J, Lin X, Godwin ID, Jordan DR, Wang J (2013) Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat Commun 4:2320

    Article  PubMed  Google Scholar 

  2. Mullet J, Morishige D, McCormick R, Truong S, Hilley J, McKinley B, Anderson R, Olson SN, Rooney W (2014) Energy sorghum-a genetic model for the design of C-4 grass bioenergy crops. J Exp Bot 65:3479–3489

    Article  PubMed  Google Scholar 

  3. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman WD, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  4. Duodu KG, Taylor JRN, Belton PS, Hamaker BR (2003) Factors affecting sorghum protein digestibility. J Cereal Sci 38:117–131

    Article  CAS  Google Scholar 

  5. Wong JH, Lau T, Cai N, Singh J, Pedersen JF, Vensel WH, Hurkman WJ, Wilson JD, Lemaux PG, Buchanan BB (2009) Digestibility of protein and starch from sorghum (Sorghum bicolor) is linked to biochemical and structural features of grain endosperm. J Cereal Sci 49:73–82

    Article  CAS  Google Scholar 

  6. Miflin B (2000) Crop improvement in the 21st century. J Exp Bot 51:1–8

    Article  CAS  PubMed  Google Scholar 

  7. Emani C, Sunilkumar G, Rathore KS (2002) Transgene silencing and reactivation in sorghum. Plant Sci 162:181–192

    Article  CAS  Google Scholar 

  8. Kim D, Alptekin B, Budak H (2018) CRISPR/Cas9 genome editing in wheat. Funct Integr Genomics 18:31–41

    Article  CAS  PubMed  Google Scholar 

  9. Yin XJ, Biswal AK, Dionora J, Perdigon KM, Balahadia CP, Mazumdar S, Chater C, Lin HC, Coe RA, Kretzschmar T, Gray JE, Quick PW, Bandyopadhyay A (2017) CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomatal developmental gene EPFL9 in rice. Plant Cell Rep 36:745–757

    Article  CAS  PubMed  Google Scholar 

  10. Char SN, Neelakandan AK, Nahampun H, Frame B, Main M, Spalding MH, Becraft PW, Meyers BC, Walbot V, Wang K, Yang B (2017) An agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol J 15:257–268

    Article  CAS  PubMed  Google Scholar 

  11. Casas AM, Kononowicz AK, Zehr UB, Tomes DT, Axtell JD, Butler LG, Bressan RA, Hasegawa PM (1993) Transgenic sorghum plants via microprojectile bombardment. Proc Natl Acad Sci U S A 90:11212–11216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Elkonin LA, Lopushanskaya RF, Pakhomova NV (1995) Initiation and maintenance of friable, embryogenic callus of sorghum [Sorghum bicolor (L.) Moench] by amino acids. Maydica 40:153–157

    Google Scholar 

  13. Cai T, Butler L (1990) Plant-regeneration from embryogenic callus initiated from immature inflorescences of several high-tannin sorghums. Plant Cell Tissue Organ Cult 20:101–110

    Article  Google Scholar 

  14. Elkonin LA, Tyrnov VS, Tsvetova MI, Ishin AG (1987) Regeneration of plants in the somatic tissue-culture of sorghum haploid. Tsitologiya I Genetika 21:18–22

    Google Scholar 

  15. 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 13:109

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Liu G, Gilding EK, Godwin ID (2015) A robust tissue culture system for sorghum [Sorghum bicolor (L.) Moench]. S Afr J Bot 98:157–160

    Article  CAS  Google Scholar 

  17. Liu GQ, Campbell BC, Godwin ID (2014) Sorghum genetic transformation by particle Bombardment. In: Henry RJ, Furtado A (eds) Cereal genomics: methods and protocols. methods in molecular biology, vol 1099. Humana Press, Totowa, New Jersey, pp 219–234

    Chapter  Google Scholar 

  18. 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 

  19. Liu GQ, Godwin ID (2012) Highly efficient sorghum transformation. Plant Cell Rep 31:999–1007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Gurel S, Gurel E, Kaur R, Wong J, Meng L, Tan H-Q, Lemaux PG (2009) Efficient, reproducible Agrobacterium-mediated transformation of sorghum using heat treatment of immature embryos. Plant Cell Rep 28:429–444

    Article  CAS  PubMed  Google Scholar 

  21. Pola S, Mani NS, Ramana T (2008) Plant tissue culture studies in Sorghum bicolor: immature embryo explants as the source material. Int J Plant Product 2:1–14

    Google Scholar 

  22. Nguyen TV, Thu TT, Claeys M, Angenon G (2007) Agrobacterium-mediated transformation of sorghum (Sorghum bicolor (L.) Moench) using an improved in vitro regeneration system. Plant Cell Tissue Organ Cult 91:155–164

    Article  CAS  Google Scholar 

  23. Howe A, Sato S, Dweikat I, Fromm M, Clemente T (2006) Rapid and reproducible Agrobacterium-mediated transformation of sorghum. Plant Cell Rep 25:784–791

    Article  CAS  PubMed  Google Scholar 

  24. Grootboom AW, Mkhonza NL, O'Kennedy MM, Chakauya E, Kunert K, Chikwamba RK (2010) Biolistic mediated sorghum (Sorghum bicolor L. Moench) transformation via mannose and bialaphos based selection systems. Int J Bot 6:89–94

    Article  CAS  Google Scholar 

  25. Mookkan M, Nelson-Vasilchik K, Hague J, Zhang ZYJ, Kausch AP (2017) Selectable marker independent transformation of recalcitrant maize inbred B73 and sorghum P898012 mediated by morphogenic regulators BABY BOOM and WUSCHEL2. Plant Cell Rep 36:1477–1491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho MJ, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, Rudrappa B, Shamseer PM, Bruce W, Newman L, Shen B, Zheng P, Bidney D, Falco C, Register J, Zhao ZY, Xu D, Jones T, Gordon-Kamm W (2016) Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Puchta H (2017) Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Curr Opin Plant Biol 36:1–8

    Article  CAS  PubMed  Google Scholar 

  28. Zhang Y, Liang Z, Zong Y, Wang YP, Liu JX, Chen KL, Qiu JL, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Woo JW, Kim J, Il Kwon S, Corvalan 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 

  30. Waltz E (2018) With a free pass, CRISPR-edited plants reach market in record time. Nat Biotechnol 36:6–7

    Article  CAS  PubMed  Google Scholar 

  31. Murty UR, Visarada AA, Bharathi M (1990) Developing tissue-culture system for sorghum, Sorghum-bicolor (L) Moench.2. Plant-regeneration from embryogenic callus. Cereal Res Commun 18:355–358

    Google Scholar 

  32. Sticklen MB, Oraby HF (2005) Invited review: shoot apical meristem: a sustainable explant for genetic transformation of cereal crops. In Vitro Cell Dev Biol-Plant 41:187–200

    Article  CAS  Google Scholar 

  33. Nirwan RS, Kothari SL (2004) High frequency shoot organogenesis in Sorghum bicolor (L) Moench. J Plant Biochem Biotechnol 13:149–152

    Article  CAS  Google Scholar 

  34. Oldach KH, Morgenstern A, Rother S, Girgi M, O'Kennedy M, Lorz H (2001) Efficient in vitro plant regeneration from immature zygotic embryos of pearl millet [Pennisetum glaucum (L.) R. Br.] and Sorghum bicolor (L.) Moench. Plant Cell Rep 20:416–421

    Article  CAS  PubMed  Google Scholar 

  35. Gamborg OL, Shyluk JP, Brar DS, Constabel F (1977) Morphogenesis and plant regeneration from callus of immature embryos of sorghum. Plant Sci Lett 10:67–74

    Article  CAS  Google Scholar 

  36. Gurel S, Gurel E, Miller TI, Lemaux PG (2012) Agrobacterium-mediated transformation of Sorghum bicolor using immature embryos. In: Dunwell JM, Wetten AC (eds) Transgenic plants: methods and protocols, second edition, methods Mol biol 847. Humana Press Inc, Totowa, pp 109–122

    Chapter  Google Scholar 

  37. Raghuwanshi A, Birch RG (2010) Genetic transformation of sweet sorghum. Plant Cell Rep 29:997–1005

    Article  CAS  PubMed  Google Scholar 

  38. Visarada K, Prasad GS, Royer M (2016) Genetic transformation and evaluation of two sweet sorghum genotypes for resistance to spotted stemborer, Chilo partellus (Swinhoe). Plant Biotechnol Rep 10:277–289

    Article  Google Scholar 

  39. Sato S, Clemente T, Dweikat I (2004) Identification of an elite sorghum genotype with high in vitro performance capacity. In Vitro Cell Dev Biol-Plant 40:57–60

    Article  Google Scholar 

  40. Deschamps S, Zhang Y, Llaca V, Ye L, Sanyal A, King M, May G, Lin H (2018) A chromosome-scale assembly of the sorghum genome using nanopore sequencing and optical mapping. Nat Commun 9:4844

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  42. Kaeppler HF, Pedersen JF (1996) Media effects on phenotype of callus cultures initiated from photoperiod-insensitive, elite inbred sorghum lines. Maydica 41:83–89

    Google Scholar 

  43. Sanjay G, Khanna VK, Rameshwar S, Garg GK (2002) Effect of media and explant on callus formation and plant regeneration in sorghum. J Plant Biol 29:39–44

    Google Scholar 

  44. Nawy T (2012) Reporting plant hormone levels: a disappearing act. Nat Methods 9:219–219

    Article  CAS  Google Scholar 

  45. Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96

    Article  CAS  PubMed  Google Scholar 

  46. Kende H, Zeevaart JAD (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  48. Skoog F, Miller CO (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 

  49. Zhao LM, Liu SJ, Song SQ (2010) Optimization of callus induction and plant regeneration from germinating seeds of sweet sorghum (Sorghum bicolor Moench). Afr J Biotechnol 9:2367–2374

    Article  CAS  Google Scholar 

  50. Anbumalarmathi J, Nadarajan N (2007) Callus induction and plant regeneration in sorghum (Sorgum bicolor L. Moench). Ind J Agric Res 41:10–16

    Google Scholar 

  51. 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 

  52. Elkonin LA, Pakhomova NV (2000) Influence of nitrogen and phosphorus on induction embryogenic callus of sorghum. Plant Cell Tissue Organ Cult 61:115–123

    Article  Google Scholar 

  53. Nirwan RS, Kothari SL (2003) High copper levels improve callus induction and plant regeneration in Sorghum bicolor (L.) Moench. In Vitro Cell Dev Bio-Plant 39:161–164

    Article  CAS  Google Scholar 

  54. Carvalho CHS, Zehr UB, Gunaratna N, Anderson J, Kononowicz HH, Hodges TK, Axtell JD (2004) Agrobacterium-mediated transformation of sorghum: factors that affect transformation efficiency. Genet Mol Biol 27:259–269

    Article  CAS  Google Scholar 

  55. Joyce PA, Sun Y (2019) Biolistic-mediated gene delivery in sugarcane. In: Rustgi S, Lup H (eds) Biolistic DNA delivery in plants. Springer, New York. (Chapter 12 this volume)

    Google Scholar 

  56. Vain P, McMullen MD, Finer JJ (1993) Osmotic treatment enhances particle bombardment-mediated transient and stable transformation of maize. Plant Cell Rep 12:84–88

    Article  CAS  PubMed  Google Scholar 

  57. Frame BR, Zhang H, Cocciolone SM, Sidorenko LV, Dietrich CR, Pegg SE, Zhen S, Schnable PS, Wang K (2000) Production of transgenic maize from bombarded type II callus: effect of gold particle size and callus morphology on transformation efficiency. In Vitro Cell Dev Biol-Plant 36:21–29

    Article  Google Scholar 

  58. Hagio T (2002) Adventitious shoot regeneration from immature embryos of sorghum. Plant Cell Tissue Organ Cult 68:65–72

    Article  CAS  Google Scholar 

  59. Craufurd PQ, Qi AM, Ellis RH, Summerfield RJ, Roberts EH, Mahalakshmi V (1998) Effect of temperature on time to panicle initiation and leaf appearance in sorghum. Crop Sci 38:942–947

    Article  Google Scholar 

  60. Russell JA, Roy MK, Sanford JC (1992) Physical trauma and tungsten toxicity reduce the efficiency of biolistic transformation. Plant Physiol 98:1050–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Miki B, McHugh S (2004) Selectable marker genes in transgenic plants: applications, alternatives and biosafety. J Biotechnol 107:193–232

    Article  CAS  PubMed  Google Scholar 

  62. He Z, Fu Y, Si H, Hu G, Zhang S, Yu Y, Sun Z (2004) Phosphomannose-isomerase (pmi) gene as a selectable marker for rice transformation via Agrobacterium. Plant Sci 166:17–22

    Article  CAS  Google Scholar 

  63. O’Kennedy MM, Stark HC, Dube N (2011) Biolistic-mediated transformation protocols for maize and pearl millet using pre-cultured immature zygotic embryos and embryogenic tissue. In: Thorpe TA, Yeung EC (eds) Plant embryo culture: methods and protocols. Humana Press, Totowa, NJ, pp 343–354

    Chapter  Google Scholar 

  64. Reed J, Privalle L, Powell ML, Meghji M, Dawson J, Dunder E, Sutthe J, Wenck A, Launis K, Kramer G, Chang Y-F, Hansen G, Wright M (2001) Phosphomannose isomerase: an efficient selectable marker for plant transformation. In Vitro Cell Dev Biol-Plant 37:127–132

    Article  CAS  Google Scholar 

  65. Duan YB, Zhai CG, Li H, Li J, Mei WQ, Gui HP, Ni D, Song F, Li L, Zhang W, Yang J (2012) An efficient and high-throughput protocol for agrobacterium-mediated transformation based on phosphomannose isomerase positive selection in japonica rice (Oryza sativa L.). Plant Cell Rep 31:1611–1624

    Article  CAS  PubMed  Google Scholar 

  66. Rao RN, Allen NE, Hobbs JN, Alborn WE, Kirst HA, Paschal JW (1983) Genetic and enzymatic basis of hygromycin B resistance in Escherichia coli. Antimicrob Agents Chemother 24:689–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zuraida AR, Rahiniza K, Zulkifli AS, Alizah Z, Zamri Z, Aziz A (2013) Hygromycin as selective marker in Agrobacterium-mediated genetic transformation of indica rice MR 219. J Trop Agric Food Sci 41:71–79

    Google Scholar 

  68. Meng Z-H, Liang A-H, Yang W-C (2007) Effects of hygromycin on cotton cultures and its application in agrobacterium-mediated cotton transformation. In Vitro Cell Dev Biol-Plant 43:111–118

    Article  CAS  Google Scholar 

  69. Gonzalez A, Jimenez A, Vazquez D, Davies JE, Schindler D (1978) Studies on the mode of action of hygromycin B, an inhibitor of translocation in eukaryotes. Biochim Biophys Acta 521:459–469

    Article  CAS  PubMed  Google Scholar 

  70. Gay PB, Gillespie SH (2005) Antibiotic resistance markers in genetically modified plants: a risk to human health? Lancet Infect Dis 5:637–646

    Article  CAS  PubMed  Google Scholar 

  71. Scholz-Starke J, Carpaneto A, Gambale F (2006) On the interaction of neomycin with the slow vacuolar channel of Arabidopsis thaliana. J Gen Physiol 127:329–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes—structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689

    Article  CAS  PubMed  Google Scholar 

  73. Hermann SR, Harding RM, Dale JL (2001) The banana actin 1 promoter drives near-constitutive transgene expression in vegetative tissues of banana (Musa spp.). Plant Cell Rep 20:525–530

    Article  CAS  Google Scholar 

  74. McElroy D, Zhang WG, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2:163–171

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Scully ED, Gries T, Sarath G, Palmer NA, Baird L, Serapiglia MJ, Dien BS, Boateng AA, Ge Z, Funnell-Harris DL, Twigg P, Clemente TE, Sattler SE (2016) Overexpression of SbMyb60 impacts phenylpropanoid biosynthesis and alters secondary cell wall composition in Sorghum bicolor. Plant J 85:378–395

    Article  CAS  PubMed  Google Scholar 

  76. Lamont KC, Mudge SR, Liu G, Godwin ID (2017) Expression patterns of the native Shrunken-2 promoter in Sorghum bicolor visualised through use of the GFP reporter gene. Plant Cell Rep 36:1689–1700

    Article  CAS  PubMed  Google Scholar 

  77. Liu G, Lamont KC, Ahmad N, Tomkins A, Mudge SR, Gilding EK, Godwin ID (2017) The functionality of α-kafirin promoter and α-kafirin signal peptide. Plant Cell Tissue Organ Cult 128:133–143

    Article  CAS  Google Scholar 

  78. Liu G, Gilding EK, Kerr ED, Schulz BL, Tabet B, Hamaker BR, Godwin ID (2019) Increasing protein content and digestibility in sorghum grain with a synthetic biology approach. J Cereal Sci 85:27–34

    Article  CAS  Google Scholar 

  79. Urriola J, Rathore KS (2014) Temporal and spatial activities of a rice glutelin promoter in transgenic sorghum. Plant Cell Tissue Organ Cult 116:227–234

    Article  CAS  Google Scholar 

  80. Bernstein E, Caudy AA, Hammond SM, Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366

    Article  CAS  PubMed  Google Scholar 

  81. Ketting RF, Fischer SE, Bernstein E, Sijen T, Hannon GJ, Plasterk RH (2001) Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev 15:2654–2659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Knight SW, Bass BL (2001) A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science 293:2269–2271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hammond SM, Boettcher S, Caudy AA, Kobayashi R, Hannon GJ (2001) Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293:1146–1150

    Article  CAS  PubMed  Google Scholar 

  84. Nykanen A, Haley B, Zamore PD (2001) ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107:309–321

    Article  CAS  PubMed  Google Scholar 

  85. Hutvagner G, Zamore PD (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297:2056–2060

    Article  CAS  PubMed  Google Scholar 

  86. Martinez J, Patkaniowska A, Urlaub H, Luhrmann R, Tuschl T (2002) Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 110:563–574

    Article  CAS  PubMed  Google Scholar 

  87. Jung JH, Vermerris W, Gallo M, Fedenko JR, Erickson JE, Altpeter F (2013) RNA interference suppression of lignin biosynthesis increases fermentable sugar yields for biofuel production from field-grown sugarcane. Plant Biotechnol J 11:709–716

    Article  CAS  PubMed  Google Scholar 

  88. Guo JL, Gao SW, Lin QL, Wang HB, Que YX, Xu LP (2015) Transgenic sugarcane resistant to sorghum mosaic virus based on coat protein gene silencing by RNA interference. Biomed Res Int 2015:861907

    PubMed  PubMed Central  Google Scholar 

  89. Grootboom AW, Mkhonza NL, Mbambo Z, O'Kennedy MM, da Silva LS, Taylor J, Taylor JR, Chikwamba R, Mehlo L (2014) Co-suppression of synthesis of major alpha-kafirin sub-class together with gamma-kafirin-1 and gamma-kafirin-2 required for substantially improved protein digestibility in transgenic sorghum. Plant Cell Rep 33:521–537

    Article  CAS  PubMed  Google Scholar 

  90. Mengiste T, Paszkowski J (1999) Prospects for the precise engineering of plant genomes by homologous recombination. Biol Chem 380:749–758

    Article  CAS  PubMed  Google Scholar 

  91. Lieberman-Lazarovich M, Levy AA (2011) Homologous recombination in plants: an antireview. Methods Mol Biol 701:51–65

    Article  CAS  PubMed  Google Scholar 

  92. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93:1156–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. 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 

  95. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F (2013) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8:2281–2308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170

    Article  CAS  PubMed  Google Scholar 

  97. Bolotin A, Ouinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–2561

    Article  CAS  PubMed  Google Scholar 

  98. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39:9275–9282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Doench JG, Hartenian E, Graham DB, Tothova Z, Hegde M, Smith I, Sullender M, Ebert BL, Xavier RJ, Root DE (2014) Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat Biotechnol 32:1262–1267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Cong L, Ran FA, Cox D, Lin SL, 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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Naito Y, Hino K, Bono H, Ui-Tei K (2015) CRISPRdirect: software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics 31:1120–1123

    Article  CAS  PubMed  Google Scholar 

  103. Xie KB, Zhang JW, Yang YN (2014) Genome-wide prediction of highly specific guide RNA spacers for CRISPR-Cas9-mediated genome editing in model plants and major crops. Mol Plant 7:923–926

    Article  CAS  PubMed  Google Scholar 

  104. Liu H, Ding YD, Zhou YQ, Jin WQ, Xie KB, Chen LL (2017) CRISPR-P 2.0: an improved CRISPR-Cas9 tool for genome editing in plants. Mol Plant 10:530–532

    Article  CAS  PubMed  Google Scholar 

  105. Haeussler M, Schonig K, Eckert H, Eschstruth A, Mianne J, Renaud JB, Schneider-Maunoury S, Shkumatava A, Teboul L, Kent J, Joly JS, Concordet JP (2016) Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol 17:148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  106. Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338

    Article  CAS  PubMed  Google Scholar 

  107. Muller M, Lee CM, Gasiunas G, Davis TH, Cradick TJ, Siksnys V, Bao G, Cathomen T, Mussolino C (2016) Streptococcus thermophilus CRISPR-Cas9 systems enable specific editing of the human genome. Mol Ther 24:636–644

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Karvelis T, Gasiunas G, Young JS, Bigelyte G, Silanskas A, Cigan M, Siksnys V (2015) Rapid characterization of CRISPR-Cas9 protospacer adjacent motif sequence elements. Genome Biol 16:253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  109. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Joung JK (2016) High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature 529:490–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Kleinstiver BP, Prew MS, Topkar VV, Tsai SQ, Joung JK (2015) Engineered Cas9 variants with novel PAM specificities expand the targeting range of CRISPR/Cas nucleases. Mol Ther 23:S26

    Article  Google Scholar 

  112. Slaymaker IM, Gao LY, Zetsche B, Scott DA, Yan WX, Zhang F (2016) Rationally engineered Cas9 nucleases with improved specificity. Science 351:84–88

    Article  CAS  PubMed  Google Scholar 

  113. Cromwell CR, Sung K, Park J, Krysler AR, Jovel J, Kim SK, Hubbard BP (2018) Incorporation of bridged nucleic acids into CRISPR RNAs improves Cas9 endonuclease specificity. Nat Commun 9:1448

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  114. Ma XL, Zhang QY, Zhu QL, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu YG (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284

    Article  CAS  PubMed  Google Scholar 

  115. Feng ZY, Mao YF, Xu NF, Zhang BT, Wei PL, Yang DL, Wang Z, Zhang Z, Zheng R, Yang L, Zeng L, Liu X, Zhu JK (2014) Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci U S A 111:4632–4637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Wang ZP, Xing HL, Dong L, Zhang HY, Han CY, Wang XC, Chen QJ (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol 16:144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Che P, Anand A, Wu E, Sander JD, Simon MK, Zhu WW, Sigmund AL, Zastrow-Hayes G, Miller M, Liu D, Lawit SJ, Zhao ZY, Albertsen MC, Jones TJ (2018) Developing a flexible, high-efficiency agrobacterium-mediated sorghum transformation system with broad application. Plant Biotechnol J 16:1388–1395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Liu G, Li J, Godwin ID (2019) Genome editing by CRISPR/Cas9 in sorghum through biolistic bombardment. Methods Mol Biol 1931:169–183

    Article  CAS  PubMed  Google Scholar 

  119. Subburaj S, Chung SJ, Lee C, Ryu SM, Kim DH, Kim JS, Bae S, Lee GJ (2016) Site-directed mutagenesis in petunia x hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. Plant Cell Rep 35:1535–1544

    Article  CAS  PubMed  Google Scholar 

  120. Liang Z, Chen KL, Zhang Y, Liu JX, Yin KQ, Qiu JL, Gao C (2018) Genome editing of bread wheat using biolistic delivery of CRISPR/Cas9 in vitro transcripts or ribonucleoproteins. Nat Protoc 13:413–430

    Article  CAS  PubMed  Google Scholar 

  121. Svitashev S, Schwartz C, Lenderts B, Young JK, Cigan AM (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein complexes. Nat Commun 7:13274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Lowder LG, Malzahn A, Qi YP (2018) Plant gene regulation using multiplex CRISPR-dCas9 artificial transcription factors. Methods Mol Biol 1676:197–214

    Article  CAS  PubMed  Google Scholar 

  123. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, Wang XC, Chen QJ (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Zong Y, Wang YP, Li C, Zhang R, Chen KL, Ran YD, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440

    Article  CAS  PubMed  Google Scholar 

  125. Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR (2017) Programmable base editing of A.T to G.C in genomic DNA without DNA cleavage. Nature 559:E8

    Article  CAS  Google Scholar 

  126. Li C, Zong Y, Wang YP, Jin S, Zhang DB, Song QN, Zhang R, Gao C (2018) Expanded base editing in rice and wheat using a Cas9-adenosine deaminase fusion. Genome Biol 19:59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

We are thankful to GRDC (Grains Research & Development Corporation) for funding the research project 9176038 (Better sorghum: larger grain with more protein).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guoquan Liu .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

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

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Liu, G., Massel, K., Tabet, B., Godwin, I.D. (2020). Biolistic DNA Delivery and Its Applications in Sorghum bicolor. 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_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-0356-7_10

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-0355-0

  • Online ISBN: 978-1-0716-0356-7

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics