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Maize transformation: history, progress, and perspectives

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Abstract

Maize functional genomics research and genetic improvement strategies have been greatly accelerated and refined through the development and utilization of genetic transformation systems. Maize transformation is a composite technology based on decades’ efforts in optimizing multiple factors involving microbiology and physical/biochemical DNA delivery, as well as cellular and molecular biology. This review provides a historical reflection on the development of maize transformation technology including the early failures and successful milestones. It also provides a current perspective on the understanding of tissue culture responses and their impact on plant regeneration, the pros and cons of different DNA delivery methods, the identification of a palette of selectable/screenable markers, and most recently the development of growth-stimulating or morphogenic genes to improve efficiencies and extend the range of transformable genotypes. Steady research progress in these interdependent components has been punctuated by benchmark reports celebrating the progress in maize transformation, which invariably relied on a large volume of supporting research that contributed to each step and to the current state of the art. The recent explosive use of CRISPR/Cas9-mediated genome editing has heightened the demand for higher transformation efficiencies, especially for important inbreds, to support increasingly sophisticated and complicated genomic modifications, in a manner that is widely accessible. These trends place an urgent demand on taking maize transformation to the next level, presaging a new generation of improvements on the horizon. Once realized, we anticipate a near-future where readily accessible, genotype-independent maize transformation, together with advanced genomics, genome editing, and accelerated breeding, will contribute to world agriculture and global food security.

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Data availability

The composite biological illustrations of Figs. 3, 4, and 5 and all of the individual illustrations they comprise are copyrighted by the author Albert P. Kausch (APK) who provides Springer the permission to publish them in this paper.

Code availability

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Abbreviations

ABA:

Abscisic acid

BBM:

Baby Boom transcription factor

BMS:

Black Mexican Sweet

CaMV:

Cauliflower mosaic virus

Cas9:

CRISPR-associated protein 9

CIMMYT:

Centro Internacional de Mejoramiento de Maíz y Trigo (in Spanish) International Maize and Wheat Improvement Centre

CRISPR:

Clustered Regularly Interspaced Short Palindromic Repeat

eSECs:

“Early” somatic embryogenic cells

DAP:

Days after pollination

EMS:

Ethyl methanesulfonate

EPSPS:

5-Enolpyruvylshikimate-3-phosphate synthase

EU:

European Union

FTO:

Freedom to operate

GM:

Genetically modified

GMO:

Genetically modified organism

GWAS:

Genome-wide association study

HPT:

Hygromycin phosphotransferase

IE:

Immature embryo

MRT:

Morphogenic regulator-mediated transformation

NPT:

Neomycin phosphotransferase

PEG:

Polyethylene glycol

PGS:

Plant Genetic Systems

RNPs:

Ribonucleoproteins

SAM:

Shoot apical meristem

SiC:

Silicon carbide

TALENS:

Transcription activator-like effector nucleases

WUS2:

Wuschel 2 transcription factor

ZFN:

Zinc finger nucleases

References

  • Aguado-Santacruz GA, García-Moya E, Aguilar-Acuña JL, Moreno-Gómez B, Solís-Moya E, Preciado-Ortiz ER, Jiménez-Bremont JF, Rascón-Cruz Q (2007) In vitro plant regeneration from quality protein maize (QPM). Vitro Cell Dev Biol Plant 43:215–224

    Article  CAS  Google Scholar 

  • Akram Z, Ali S, Ali GM, Zafar Y, Shah ZH, Alghabari F (2016) Whisker-mediated transformation of peanut with chitinase gene enhances resistance to leaf spot disease. Crop Breed Appl Biotechnol 16:108–114

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Altpeter F, Springer NM, Bartley LE, Blechl A, Brutnell TP, Citovsky V, Conrad L, Gelvin SB, Jackson D, Kausch AP, Lemaux PG, Medford JI, Orozo-Cardenas M, Tricoli D, VanEck J, Voytas DF, Walbot V, Wang K, Zhang ZJ, Stewart CN (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anami SNE, Coussens G, Aesaert S, Van Lijsebettens M (2013) Higher plant transformation: principles and molecular tools. Int J Dev Biol 57:483–494

    Article  CAS  PubMed  Google Scholar 

  • Anand A, Bass SH, Wu E, Wang N, McBride KE, Annaluru N, Miller M, Hua M, Jones TJ (2018) An improved ternary vector system for Agrobacterium-mediated rapid maize transformation. Plant Mol Biol 97:187–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anand A, Wu E, Li Z, TeRonde S, Arling M, Lenderts B, Mutti JS, Gordon-Kamm W, Jones TJ, Chilcoat ND (2019) High efficiency Agrobacterium-mediated site-specific gene integration in maize utilizing the FLP-FRT recombination system. Plant Biotechnol J 17:1636–1645

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Armstrong CL (1999) The first decade of maize transformation: a review and future perspective. Maydica 44:101–109

    Google Scholar 

  • Armstrong CL, Green CE (1985) Establishment and maintenance of friable, embryogenic maize callus and the involvement of L-proline. Planta 164:207–214

    Article  CAS  PubMed  Google Scholar 

  • Armstrong CL, Green CE, Phillips RL (1991) Development and availability of germplasm with high type II culture formation response. Maize Genet Coop Newsl 65:92–93

    Google Scholar 

  • Armstrong CL, Romero-Severson J, Hodges TK (1992) Improved tissue culture response of an elite maize inbred through backcross breeding, and identification of chromosomal regions important for regeneration by RFLP analysis. Theor Appl Genet 84:755–762

    Article  CAS  PubMed  Google Scholar 

  • Asad S, Mukhtar Z, Nazir F, Hashmi JA, Mansoor S, Zafar Y, Arshad M (2008) Silicon carbide whisker-mediated embryogenic callus transformation of cotton (Gossypium hirsutum L.) and regeneration of salt tolerant plants. Mol Biotechnol 40:161

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banno H, Ikeda Y, Niu Q-W, Chua N-H (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barampuram S, Zhang Z (2011) Recent advances in plant transformation. In: Birchler JA (ed) Plant chromosome engineering, vol 701. Methods in Molecular Biology. Humana Press, pp 1–35. https://doi.org/10.1007/978-1-61737-957-4_1

  • Barcelo P, Hagel C, Becker D, Martin A, Lörz H (1994) Transgenic cereal (tritordeum) plants obtained at high efficiency by microprojectile bombardment of inflorescence tissue. Plant J 5:583–592

    Article  CAS  PubMed  Google Scholar 

  • Barcelo P, Lazzeri PA (1995) Transformation of tritordeum and wheat by microprojectile bombardment of immature inflorescence and embryo tissues. In: Jones H (ed) Methods in molecular biology, vol XX. Humana Press Inc, Totowa

  • Barone P, Wu E, Lenderts B, Anand A, Gordon-Kamm W, Svitashev S, Kumar S (2020) Efficient gene targeting in maize using inducible CRISPR-Cas9 and marker-free donor template. Mol Plant 13:1219–1227

    Article  CAS  PubMed  Google Scholar 

  • Betts S, Basu S, Bolar J, Booth R, Chang S, Cigan AM, Farrell J, Gao H, Harkins K, Kinney A (2019) Uniform expression and relatively small position effects characterize sister transformants in maize and soybean. Front Plant Sci 10:1209

    Article  PubMed  PubMed Central  Google Scholar 

  • Bevan MW, Flavell RB, Chilton M-D (1983) A chimaeric antibiotic resistance gene as a selectable marker for plant cell transformation. Nature 304:184–187

    Article  CAS  Google Scholar 

  • Bevan MW, Mason SE, Goelet P (1985) Expression of tobacco mosaic virus coat protein by a cauliflower mosaic virus promoter in plants transformed by Agrobacterium. EMBO J 4:1921–1926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhowmik P, Ellison E, Polley B, Bollina V, Kulkarni M, Ghanbarnia K, Song H, Gao C, Voytas DF, Kagale S (2018) Targeted mutagenesis in wheat microspores using CRISPR/Cas9. Sci Rep 8:1–10

    Article  CAS  Google Scholar 

  • Bibikova M, Beumer K, Trautman JK, Carroll D (2003) Enhancing gene targeting with designed zinc finger nucleases. Science 300:764–764

    Article  CAS  PubMed  Google Scholar 

  • Biolistic DNA Delivery in Plants (2020b) Methods in molecular biology, vol 2124, 1st edn. Springer US

  • Blakeslee AF (1922) Variations in Datura due to changes in chromosome number. Am Nat 56:16–31

    Article  Google Scholar 

  • Bohorova NE, Luna B, Briton RM, Huerta LD, A. HD, (1995) Regeneration potential of tropical, and subtropical, mid altitude, and highland maize inbreds. Maydica 40:275–281

    Google Scholar 

  • Bohorova N, Zhang W, Julstrum P, McLean S, Luna B, Brito R, Diaz L, Ramos M, Estanol P, Pacheco M (1999) Production of transgenic tropical maize with cryIAb and cryIAc genes via microprojectile bombardment of immature embryos. Theor Appl Genet 99:437–444

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bower R, Birch RG (1992) Transgenic sugarcane plants via microprojectile bombardment. Plant J 2:409–416

    Article  CAS  Google Scholar 

  • Breyer D, Kopertekh L, Reheul D (2014) Alternatives to antibiotic resistance marker genes for in vitro selection of genetically modified plants – scientific developments, current use, operational access and biosafety considerations. Crit Rev Plant Sci 33:286–330

    Article  CAS  Google Scholar 

  • Brooks C, Nekrasov V, Lippman ZB, Van Eck J (2014) Efficient gene editing in tomato in the first generation using the Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR-associated9 system. Plant Physiol 166:1292–1297

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai CQ, Doyon Y, Ainley WM, Miller JC, DeKelver RC, Moehle EA, Rock JM, Lee Y-L, Garrison R, Schulenberg L, Blue R, Worden A, Baker L, Faraji F, Zhang L, Holmes MC, Rebar EJ, Collingwood TN, Rubin-Wilson B, Gregory PD, Urnov FD, Petolino JF (2009) Targeted transgene integration in plant cells using designed zinc finger nucleases. Plant Mol Biol 69:699–709

    Article  CAS  PubMed  Google Scholar 

  • Castillo AM, Vasil V, Vasil IK (1994) Rapid production of fertile transgenic plants of rye (Secale cereale L.). Nat Biotechnol 12:1366

    Article  CAS  Google Scholar 

  • Cavez D, Hachez C, Chaumont F (2009) Maize Black Mexican Sweet suspension cultured cells are a convenient tool for studying aquaporin activity and regulation. Plant Signal Behav 4:890–892. https://doi.org/10.4161/psb.4.9.9484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Čermák T, Curtin SJ, Gil-Humanes J, Čegan R, Kono TJY, Konečná E, Belanto JJ, Starker CG, Mathre JW, Greenstein RL, Voytas DF (2017) A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell 29:1196–1217

    Article  PubMed  PubMed Central  Google Scholar 

  • Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39:e82–e82. https://doi.org/10.1093/nar/gkr218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chalfie M, Tu Y, Euskirchen G, Ward W, Prasher D (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805

    Article  CAS  PubMed  Google Scholar 

  • Char S-N, Unger-Wallace E, Frame B, Briggs S, Main M, Spalding M, Vollbrecht E, Wang K, Yang B (2015) Heritable site-specific mutagenesis using TALENs in maize. Plant Biotechnol J 13:1002–1010

    Article  CAS  PubMed  Google Scholar 

  • Char S-N, 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 

  • Cheng M, Lowe B, Spencer T, Ye X, Armstrong C (2004) Factors influencing Agrobacterium-mediated transformation of monocotyledonous species. Vitro Cell Dev Biol Plant 40:31–45

    Article  Google Scholar 

  • Chilcoat D, Liu ZB, Sander J (2017) Use of CRISPR/Cas9 for crop improvement in maize and soybean. Prog Mol Biol Transl 149:27–46

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Christou P, McCabe DE (1992) Prediction of germ-line transformation events in chimeric Ro transgenic soybean plantlets using tissue-specific expression patterns. Plant J 2:283–290

    Article  CAS  Google Scholar 

  • Christian M, Qi Y, Zhang Y, Voytas DF (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 - Genes Genom Genet 3:1697–1705

    Google Scholar 

  • Chung S-M, Frankman EL, Tzfira T (2005) A versatile vector system for multiple gene expression in plants. Trends Plant Sci 10(8):357–361

    Article  CAS  PubMed  Google Scholar 

  • Clausen RE, Mann MC (1924) Inheritance in Nicotiana tabacum: V. The occurrence of haploid plants in interspecific progenies. Proc Natl Acad Sci USA 10:121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coe EH Jr (1959) A line of maize with high haploid frequency. Am Nat 93:381–382. https://doi.org/10.1086/282098

    Article  Google Scholar 

  • Coe Jr EH, Sarkar KR (1966) Preparation of nucleic acids and a genetic transformation attempt in maize1. Crop Sci 6:cropsci1966.0011183X000600050012x

    Article  Google Scholar 

  • Conger BV, Novak FJ, Afza R, Erdelsky K (1987) Somatic embryogenesis from cultured leaf segments of Zea mays. Plant Cell Rep 6:345–347

    Article  CAS  PubMed  Google Scholar 

  • Council for Agricultural Science and Technology (2018) Genome editing in agriculture: methods, applications, and governance - a paper in the series on The Need for Agricultural Innovation to Sustainably Feed the World by 2050. Issue Paper 60 edn. CAST, Ames

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

    Article  CAS  PubMed  Google Scholar 

  • D’Halluin K, De Block M, Denecke J, Janssen J, Leemans J, Reynaerts A, Botterman J (1992) The bar gene as selectable marker in plant engineering. Methods Enzymol 216:415–426

    Article  PubMed  Google Scholar 

  • Datla R, Anderson JW, Selvaraj G (1997) Plant promoters for transgene expression. In: El-Gewely MR (ed) Biotechnology annual review, vol 3. Elsevier, pp 269–296. https://doi.org/10.1016/S1387-2656(08)70037-1

  • De Block M, De Brouwer D, Tenning P (1989) Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the bar and neo genes in the transgenic plants. Plant Physiol 91:694–701

  • 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 3:1681–1689

    Article  PubMed  PubMed Central  Google Scholar 

  • Debernardi JM, Tricoli DM, Ercoli MF, Hayta S, Ronald P, Palatnik JF, Dubcovsky J (2020) A GRF-GIF chimeric protein improves the reneration efficiency of transgenic plants. Nat Plants 38:1274–1279

    CAS  Google Scholar 

  • Dekeyser R, Claes B, Marichal M, Van Montagu M, Caplan A (1989) Evaluation of selectable markers for rice transformation. Plant Physiol 90:217–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Deng W, Luo K, Li Z, Yang Y (2009) A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci 177:43–48

    Article  CAS  Google Scholar 

  • Domínguez A, Cervera M, Pérez RM, Romero J, Fagoaga C, Cubero J, López MM, Juárez JA, Navarro L, Peña L (2004) Characterisation of regenerants obtained under selective conditions after Agrobacterium-mediated transformation of citrus explants reveals production of silenced and chimeric plants at unexpected high frequencies. Mol Breeding 14:171–183

    Article  Google Scholar 

  • Dong X, Xu X, Li L, Liu C, Tian X, Li W, Chen S (2014) Marker-assisted selection and evaluation of high oil in vivo haploid inducers in maize. Mol Breed 34:1147–1158

    Article  CAS  Google Scholar 

  • Draget KI, Østgaard K, Smidsrød O (1989) Alginate-based solid media for plant tissue culture. Appl Microbiol Biotechnol 31:79–83

    Article  CAS  Google Scholar 

  • Du X, Fang T, Liu Y, Huang L, Zang M, Wang G, Liu Y, Fu J (2019) Transcriptome profiling predicts new genes to promote maize callus formation and transformation. Front Plant Sci 10:1633

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunahay TG, Adler SA, Jarvik JW (1997) Transformation of microalgae using silicon carbide whiskers. In: Tuan RS (ed) Recombinant gene expression protocols. Methods in molecular biology, vol 62. Humana Press, New Jersey, pp 503–509

  • Duncan D, Williams M, Zehr B, Widholm J (1985) The production of callus capable of plant regeneration from immature embryos of numerous Zea mays genotypes. Planta 165:322–332

    Article  CAS  PubMed  Google Scholar 

  • Eapen S (2011) Pollen grains as a target for introduction of foreign genes into plants: an assessment. Physiol Mol Biol Plants 17:1–8. https://doi.org/10.1007/s12298-010-0042-6

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebinuma H, Sugita K, Matsunaga E, Endo S, Yamada K, Komamine A (2001) Systems for the removal of a selection marker and their combination with a positive marker. Plant Cell Rep 20:383–392

    Article  CAS  PubMed  Google Scholar 

  • Ebinuma H, Sugita K, Matsunaga E, Yamakado M (1997) Selection of marker-free transgenic plants using the isopentenyl transferase gene. Proc Natl Acad Sci USA 94:2117–2121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emons A, Kieft H (1995) Somatic embryogenesis in maize (Zea mays L.). In: Bajaj YPS (ed) Somatic embryogenesis and synthetic seed II. Biotechnology in Agriculture and Forestry, vol 31. Springer, Berlin

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finer JJ, Finer KR, Ponappa T (2000) Particle bombardment mediated transformation. In: Hammond J, McGarvey P, Yusibov V (eds) Plant biotechnology: new products and applications. Springer Berlin Heidelberg, Berlin, pp 59–80. https://doi.org/10.1007/978-3-642-60234-4_3

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frame BR, Drayton PR, Bagnall SV, Lewnau CJ, Bullock WP, Wilson HM, Dunwell JM, Thompson JA, Wang K (1994) Production of fertile transgenic maize plants by silicon carbide whisker-mediated transformation. Plant J 6:941–948

    Article  CAS  Google Scholar 

  • Frame BR, Shou HX, Chikwamba RK, Zhang ZY, Xiang CB, Fonger TM, Pegg SEK, Li BC, Nettleton DS, Pei DQ, Wang K (2002) Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiol 129:13–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frame BR, McMurray JM, Fonger TM, Main ML, Taylor KW, Torney FJ, Paz MM, Wang K (2006) Improved Agrobacterium-mediated transformation of three maize inbred lines using MS salts. Plant Cell Rep 25:1024–1034

    Article  CAS  PubMed  Google Scholar 

  • Fromm M, Callis J, Taylor LP, Walbot V (1987) Electroporation of DNA and RNA into plant protoplasts. In: Methods in enzymology, vol 153. Academic Press, pp 351–366. https://doi.org/10.1016/0076-6879(87)53064-6

  • Fromm ME, Morrish F, Armstrong C, Williams R, Thomas J, Klein TM (1990) Inheritance and expression of chimeric genes in the progeny of transgenic maize plants. Bio Technol 8:833–839

    CAS  Google Scholar 

  • Fromm ME, Taylor LP, Walbot V (1986) Stable transformation of maize after gene transfer by electroporation. Nature 319:791–793

    Article  CAS  PubMed  Google Scholar 

  • Gaines EF, Aase HC (1926) A Haploid Wheat Plant. Am J Bot 13:373–385

    Article  Google Scholar 

  • Gallo-Meagher M, Irvine JE (1996) Herbicide resistant transgenic sugarcane plants containing the bar gene. Crop Sci 36:1367–1374

    Article  CAS  Google Scholar 

  • Gao H, Gadlage MJ, Lafitte HR, Lenderts B, Yang M, Schroder M, Farrell J, Snopek K, Peterson D, Feigenbutz L (2020) Superior field performance of waxy corn engineered using CRISPR–Cas9. Nat Biotechnol 38:579–581

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Jeff S, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, Lyznik LA (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176–187

    Article  CAS  PubMed  Google Scholar 

  • Gasser CS, Fraley RT (1989) Genetically engineering plants for crop improvement. Science 244:1293–1299

    Article  CAS  PubMed  Google Scholar 

  • Geiger HH (2009) Doubled Haploids. In: Bennetzen JL, Hake S (eds) Handbook of maize: genetics and genomics. Springer New York, New York, pp 641–657. https://doi.org/10.1007/978-0-387-77863-1_32

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gheysen G, Angenon G, Van Montagu M (1998) Agrobacterium-mediated plant transformation: a scientifically intriguing story with significant applications. In: Lindsey K (ed) Transgenic plant research. Harwood Academic, Amsterdam, pp 1–33

    Google Scholar 

  • Gilles LM, Khaled A, Laffaire J-B, Chaignon S, Gendrot G, Laplaige J, Bergès H, Beydon G, Bayle V, Barret P, Comadran J, Martinant J-P, Rogowsky PM, Widiez T (2017) Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. EMBO J 36:707–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gless C, Lörz H, Jähne-Gärtner A (1998a) Establishment of a highly efficient regeneration system from leaf base segments of oat (Avena sativa L.). Plant Cell Rep 17:441–445

    Article  CAS  PubMed  Google Scholar 

  • Gless C, Lörz H, Jähne-Gärtner A (1998b) Transgenic oat plants obtained at high efficiency by microprojectile bombardment of leaf base segments. J Plant Physiol 152:151–157

    Article  CAS  Google Scholar 

  • Golovkin MV, Ábrahám M, Mórocz S, Bottka S, Fehér A, Dudits D (1993) Production of transgenic maize plants by direct DNA uptake into embryogenic protoplasts. Plant Sci 90:41–52

    Article  CAS  Google Scholar 

  • Gordon-Kamm W, Dilkes BP, Lowe K, Hoerster G, Sun X, Ross M, Church L, Bunde C, Farrell J, Hill P, Maddock S, Snyder J, Sykes L, Li Z, Woo Y-m, Bidney D, Larkins BA (2002) Stimulation of the cell cycle and maize transformation by disruption of the plant retinoblastoma pathway. Proc Natl Acad Sci 99:11975–11980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon-Kamm WJ, Spencer TM, Brien JVO, Start WG, Daines RJ, Adams TR, Mangano ML, Chambers SA, Zachwieja SJ, Willetts NG, Adams WR Jr, Mackey CJ, Krueger RW, Kausch AP, Lemaux PG (1991) Transformation of maize using microprojectile bombardment: an update and perspective. Vitro Cell Devel Biol Plant 27:21–27

    Article  Google Scholar 

  • Gordon-Kamm WJ, Spencer TM, Mangano ML, Adams TR, Daines RJ, Start WG, O’Brien JV, Chambers SA, Adams WR, Willetts NG, Rice TB, Mackey CJ, Krueger RW, Kausch AP, Lemaux PG (1990) Transformation of Maize cells and regeneration of fertile transgenic plants. Plant Cell 2:603–618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green CE, Phillips RL (1975) Plant regeneration from tissue cultures of maize. Crop Sci 15:417–421

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Guha S, Maheshwari S (1964) In vitro production of embryos from anthers of Datura. Nature 204:497–497

    Article  Google Scholar 

  • Hagio T, Hirabayashi T, Machii H, Tomotsune H (1995) Production of fertile transgenic barley (Hordeum vulgare L.) plant using the hygromycin-resistance marker. Plant Cell Rep 14:329–334

    Article  CAS  PubMed  Google Scholar 

  • Hallauer AR, Lamkey KR, White PR (2000) Registration of B110, B111, B113, and B114 inbred lines of maize. Crop Sci 40:1518–1519

    Google Scholar 

  • Harwood WA, Chen DF, Creissen GP (1996) Transformation of pollen and microspores a review. In: Jain SM, Sopory SK, Veilleux RE (eds) In vitro haploid production in higher plants. Current plant science and biotechnology in agriculture, vol 24. Springer, Dordrecht, pp 53–71

  • Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA 94:2122–2127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heidmann I, De Lange B, Lambalk J, Angenent GC, Boutilier K (2011) Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep 30:1107–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Estrella L, De Block M, Messens E, Hernalsteens JP, Van Montagu M, Schell J (1983) Chimeric genes as dominant selectable markers in plant cells. EMBO J 2:987–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herrera-Estrella L, Simpson J, Martínez-Trujillo M (2005) Transgenic plants: an historical perspective. In: Peña L (ed) Transgenic plants: methods and protocols. Methods in molecular biology, vol 286. Humana Press, New Jersey, pp 3–31

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

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hodges TK, Kamo KK, Imbrie CW, Becwar MR (1986) Genotype specificity of somatic embryogenesis and regeneration in maize. Bio Technol 4:219–223

    Google Scholar 

  • Hoerster G, Wang N, Ryan L, Wu E, Anand A, McBride K, Lowe K, Jones T, Gordon-Kamm B (2020) Use of non-integrating Zm-Wus2 vectors to enhance maize transformation. Vitro Cell Dev Biol Plant 56:265–279

    Article  CAS  Google Scholar 

  • Hood EE, Helmer GL, Fraley RT, Chilton MD (1986) The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J Bacteriol 168:1291–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horsch RB, Fraley RT, Rogers SG, Sanders PR, Lloyd A, Hoffmann N (1984) Inheritance of functional foreign genes in plants. Science 223:496–498

    Article  CAS  PubMed  Google Scholar 

  • Horstman A, Bemer M, Boutilier K (2017) A transcriptional view on somatic embryogenesis. Regeneration 4:201–216

    Article  PubMed  PubMed Central  Google Scholar 

  • Howe AR, Gasser CS, Brown SM, Padgette SR, Hart J, Parker GB, Fromm ME, Armstrong CL (2002) Glyphosate as a selective agent for the production of fertile transgenic maize (Zea mays L.) plants. Mol Breed 10:153–164

    Article  CAS  Google Scholar 

  • Hu Y, Song D, Gao L, Ajayo BS, Wang Y, Huang H, Zhang J, Liu H, Liu Y, Yu G, Liu Y, Li Y, Huang Y (2020) Optimization of isolation and transfection conditions of maize endosperm protoplasts. Plant Methods 16:96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Wei Z (2005) Successful Agrobacterium-mediated genetic transformation of maize elite inbred lines. Plant Cell Tissue Organ Cult 83:187–200

    Article  Google Scholar 

  • Hwang H-H, Wang M-H, Lee Y-L, Tsai Y-L, Li Y-H, Yang F-J, Liao Y-C, Lin S-K, Lai E-M (2010) Agrobacterium-produced and exogenous cytokinin-modulated Agrobacterium-mediated plant transformation. Mol Plant Pathol 11:677–690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang H-H, Yu M, Lai E-M (2017) Agrobacterium-mediated plant transformation: biology and applications. Arabidopsis Book 15:e0186–e0186. https://doi.org/10.1199/tab.0186

    Article  PubMed  PubMed Central  Google Scholar 

  • International Service for the Acquisition of Agri-Biotech Applications (2019) ISAAA brief 55-2019: executive summary. https://www.isaaa.org/resources/publications/briefs/55/executivesummary/default.asp. Accessed 25 May 2021

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Islam SS, Tuteja N (2012) Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci 182:134–144

    Article  CAS  PubMed  Google Scholar 

  • Jacobs TB, LaFayette PR, Schmitz RJ, Parrott WA (2015) Targeted genome modifications in soybean with CRISPR/Cas9. BMC Biotechnol 15:16. https://doi.org/10.1186/s12896-015-0131-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions - beta-glucuronidase as a sensitive and versatile gene fusion marker in higher-plants. EMBO J 6:3901–3907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joersbo M, Donaldson I, Kreiberg J, Petersen S, Brunstedt J, Okkels F (1998) Analysis of mannose selection used for transformation of sugar beet. Mol Breed 4:111–117

    Article  CAS  Google Scholar 

  • Joersbo M, Okkels F (1996) A novel principle for selection of transgenic plant cells: positive selection. Plant Cell Rep 16:219–221

    Article  CAS  PubMed  Google Scholar 

  • Jones TJ (2009) Maize tissue culture and transformation: the first 20 years. In: Kriz AL, Larkins BA (eds) Molecular genetic approaches to maize improvement, vol 63. Biotechnology in Agriculture and Forestry. Springer, Berlin

  • Kaeppler H, Somers D, Rines H, Cockburn A (1992) Silicon carbide fiber-mediated stable transformation of plant cells. Theor Appl Genet 84:560–566

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kaeppler HF, Somers DA (1994) DNA delivery into maize cell cultures using silicon carbide fibers. In: Freeling M, Walbot V (eds) The maize handbook. Springer New York, New York, pp 610–613. https://doi.org/10.1007/978-1-4612-2694-9_108

  • Kaeppler HF, Carlson A, Menon G (2001) Routine utilization of green fluorescent protein as a visual selectable marker for cereal transformation. Vitro Cell Devel Biol Plant 37:120–126

    Article  CAS  Google Scholar 

  • Kamo KK, Chang KL, Lynn ME, Hodges TK (1987) Embryogenic callus formation from maize protoplasts. Planta 172:245–251

    Article  CAS  PubMed  Google Scholar 

  • Kamo KK, Hodges TK (1986) Establishment and characterization of long-term embryogenic maize callus and cell suspension cultures. Plant Sci 45:111–117

    Article  Google Scholar 

  • Kausch AP, Adams TR, Mangano M, Zachwieja SJ, Gordon-Kamm W, Daines R, Willetts NG, Chambers SA, Adams W, Anderson A, Williams G, Haines G (1995) Effects of microprojectile bombardment on embryogenic suspension cell cultures of maize (Zea mays L.) used for genetic transformation. Planta 196:501–509

    Article  CAS  Google Scholar 

  • Kausch AP, Nelson-Vasilchik K, Hague J, Mookkan M, Quemada H, Dellaporta S, Fragoso C, Zhang ZJ (2019) Edit at will: genotype independent plant transformation in the era of advanced genomics and genome editing. Plant Sci 281:186–205

    Article  CAS  PubMed  Google Scholar 

  • Kelliher T, Starr D, Richbourg L, Chintamanani S, Delzer B, Nuccio ML, Green J, Chen Z, McCuiston J, Wang W (2017) MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542:105–109

    Article  CAS  PubMed  Google Scholar 

  • Kelliher T, Starr D, Su X, Tang G, Chen Z, Carter J, Wittich PE, Dong S, Green J, Burch E, McCuiston J, Gu W, Sun Y, Strebe T, Roberts J, Bate NJ, Que Q (2019) One-step genome editing of elite crop germplasm during haploid induction. Nat Biotechnol 37:287–292

    Article  CAS  PubMed  Google Scholar 

  • Kemper EL, Silva MJ, Arruda P (1996) Effect of microprojectile bombardment parameters and osmotic treatment on particle penetration and tissue damage in transiently transformed cultured immature maize (Zea mays L.) embryos. Plant Sci 121:85–93

    Article  Google Scholar 

  • Kiesselbach TA (1949) The structure and reproduction of corn (Research bulletin: Bulletin of the Agricultural Experiment Station of Nebraska No. 161)

  • Kilby NJ, Fyvie MJ, Sessions RA, Davies GJ, Murray JAH (2000) Controlled induction of GUS marked clonal sectors in Arabidopsis. J Exp Bot 51:853–863

    Article  CAS  PubMed  Google Scholar 

  • Kirihara JA (1994) Selection of stable transformants from Black Mexican Sweet maize suspension cultures. In: Freeling MVW (ed) The maize handbook. Springer, New York. https://doi.org/10.1007/978-1-4612-2694-9_124

  • Kivilaan A, Blaydes DF (1974) Attempts to achieve genetic transformation in plants. Michigan State University Research Report 246:2–5

    Google Scholar 

  • Klein T, Fromm M, Gradziel T, Sanford J (1988a) Gene transfer into Zea mays cells by high-velocity microprojectiles is monitored with β-glucuronidase marker. Bio Technol 6:559–563

    CAS  Google Scholar 

  • Klein TM, Fromm M, Weissinger A, Tomes D, Schaaf S, Sletten M, Sanford JC (1988b) Transfer of foreign genes into intact maize cells with high-velocity microprojectiles. Proc Natl Acad Sci USA 85:4305–4309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein TM, Roth BA, Fromm ME (1989) Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc Natl Acad Sci USA 86:6681–6685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Knapp JE, Kausch AP, Chandlee JM (2000) Transformation of three genera of orchid using the bar gene as a selectable marker. Plant Cell Rep 19:893–898

    Article  CAS  PubMed  Google Scholar 

  • Komari T, Hiei Y, Saito Y, Murai N, Kumashiro T (1996) Vectors carrying two separate T-DNAs for co-transformation of higher plants mediated by Agrobacterium tumefaciens and segregation of transformants free from selection markers. Plant J 10:165–174

    Article  CAS  PubMed  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Kong J, Martín-Ortigosa S, Finer J, Orchard N, Gunadi A, Batts LA, Thakare D, Rush B, Schmitz O, Stuiver M, Olhoft P, Pacheco-Villalobos D (2020) Overexpression of the transcription factor GROWTH-REGULATING FACTOR5 improves transformation of dicot and monocot species. Front Plant Sci 11:572319

    Article  PubMed  PubMed Central  Google Scholar 

  • Korohoda J, StrzaŁka K (1979) High Efficiency genetic transformation in maize induced by exogenous DNA. Z Pflanzenphysiol 94:95–99

    Article  CAS  Google Scholar 

  • Kovács LG, Pueppke SG (1994) Mapping and genetic organization of pTiChry5, a novel Ti plasmid from a highly virulent Agrobacterium tumefaciens strain. Mol Gen Genet 242:327–336

    Article  PubMed  Google Scholar 

  • Krakowsky M, Lee M, Garay L, Woodman-Clikeman W, Long M, Sharopova N, Frame B, Wang K (2006) Quantitative trait loci for callus initiation and totipotency in maize (Zea mays L.). Theor Appl Genet 113:821–830

    Article  CAS  PubMed  Google Scholar 

  • Kyo M, Maida K, Nishioka Y, Matsui K (2018) Coexpression of WUSCHEL related homeobox (WOX) 2 with WOX8 or WOX9 promotes regeneration from leaf segments and free cells in Nicotiana tabacum L. Plant Biotechnol 18:23–30

    Article  Google Scholar 

  • Lazo GR, Stein PA, Ludwig RA (1991) A DNA transformation–competent arabidopsis genomic library in Agrobacterium. Bio Technol 9:963–967

    Article  CAS  Google Scholar 

  • Lee H, Zhang ZJ (2016) Maize (Zea mays) Hi-II transformation via Agrobacterium-mediated T-DNA transfer. CurrProtoc Plant Biol 1:121–137

    Google Scholar 

  • Lee L-Y, Gelvin SB (2008) T-DNA binary vectors and systems. Plant Physiol 146:325–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Zhang D, Chen M, Liang W, Wei J, Qi Y, Yuan Z (2016) Development of japonica photo-sensitive genic male sterile rice lines by editing carbon starved anther using CRISPR/Cas9. J Genet Genomics 43:415–419

    Article  PubMed  Google Scholar 

  • Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392

    Article  CAS  PubMed  Google Scholar 

  • Li W, Masilamany P, Kasha KJ, Pauls KP (2002) Developmental, tissue culture, and genotypic factors affecting plant regeneration from shoot apical meristems of germinated Zea mays L. seedlings. Vitro Cell Dev Biol Plant 38:285–292

    Article  Google Scholar 

  • Li X, Meng D, Chen S, Luo H, Zhang Q, Jin W, Yan J (2017) Single nucleus sequencing reveals spermatid chromosome fragmentation as a possible cause of maize haploid induction. Nat Commun 8:1–9

    Google Scholar 

  • Li Z, Hayashimoto A, Murai N (1992) A sulfonylurea herbicide resistance gene from Arabidopsis thaliana as a new selectable marker for production of fertile transgenic rice plants. Plant Physiol 100:662–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lin B-C, Kado CI (1977) Studies on Agrobacterium tumefaciens. VII. Avirulence induced by temperature and ethidium bromide. Can J Microbiol 23:1554–1561

    Article  CAS  PubMed  Google Scholar 

  • Liu K, Goodman M, Muse S, Smith JS, Buckler E, Doebley J (2003) Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites. Genetics 165:2117–2128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Li X, Meng D, Zhong Y, Chen C, Dong X, Xu X, Chen B, Li W, Li L (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase A generates haploid induction in maize. Mol Plant 10:520–522

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Liu X, Zhang X, Sun B, Hao L, Liu C, Zhang D, Tang H, Li C, Li Y, Shi Y, Xie X, Song Y, Wang T, Li Y (2019) Genome-wide identification and comparative analysis of drought-related microRNAs in two maize inbred lines with contrasting drought tolerance by deep sequencing. PLOS ONE 14:e0219176–e0219176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Longo C, Lickwar C, Hu Q, Nelson-Vasilchik K, Viola D, Hague J, Chandlee JM, Luo H, Kausch AP (2006) Turf grasses. In: Wang K (ed) Agrobacterium protocols, vol 2. Humana Press, New Jersey, pp 83–95

  • Lorence A, Verpoorte R (2004) Gene transfer and expression in plants. In: Balbás P, Lorence A (eds) Recombinant gene expression: reviews and protocols. Humana Press, Totowa, pp 329–350. https://doi.org/10.1385/1-59259-774-2:329

  • Lörz H, Baker B, Schell J (1985) Gene transfer to cereal cells mediated by protoplast transformation. Mol Gen Genet 199:178–182

    Article  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West M, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  CAS  PubMed  Google Scholar 

  • Lowe K, Hoerster G, Sun X, Rasco-Gaunt S, Lazerri P, Ellis S, Abbitt S, Glassman K, Gordon-Kamm B (2003) Maize LEC1 improves transformation in both maize and wheat. In: Vasil IK (ed) Plant biotechnology 2002 and beyond. Springer, Dordrecht, pp 283–284

    Chapter  Google Scholar 

  • Lowe K, Bowen B, Hoerster G, Ross M, Bond D, Pierce D, Gordon-Kamm B (1995) Germline transformation of maize following manipulation of chimeric shoot meristems. Bio/Technol 13:677–682

    CAS  Google Scholar 

  • Lowe BA, Way MM, Kumpf JM, Rout J, Warner D, Johnson R, Armstrong CL, Spencer MT, Chomet PS (2006) Marker assisted breeding for transformability in maize. Mol Breeding 18:229–239

    Article  CAS  Google Scholar 

  • Lowe K, La Rota M, Hoerster G, Hastings C, Wang N, Chamberlin M, Wu E, Jones T, Gordon-Kamm W (2018) Rapid genotype “independent” Zea mays L. (maize) transformation via direct somatic embryogenesis. Vitro Cell Dev Biol Plant 54:240–252

    Article  CAS  PubMed  Google Scholar 

  • Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho M-J, 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 SC, RegisterIII JC, Zhao Z-Y, Xu D, Jones TJ, Gordon-Kamm WJ (2016) Morphogenic regulators Baby Boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loyola-Vargas VM, Ochoa-Alejo N (2016) Somatic embryogenesis. An overview. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Somatic embryogenesis: fundamental aspects and applications. Springer International Publishing, Cham, pp 1–8. https://doi.org/10.1007/978-3-319-33705-0_1

  • Luo Z-x, Wu R (1989) A simple method for the transformation of rice via the pollen-tube pathway. Plant Mol Biol Rep 7:69–77

    Article  Google Scholar 

  • Lutz KA, Martin C, Khairzada S, Maliga P (2015) Steroid-inducible BABY BOOM system for development of fertile Arabidopsis thaliana plants after prolonged tissue culture. Plant Cell Rep 34:1849–1856

    Article  CAS  PubMed  Google Scholar 

  • Massonneau A, Coronado M-J, Audran A, Bagniewska A, Mòl R, Testillano PS, Goralski G, Dumas C, Risueño M-C, Matthys-Rochon E (2005) Multicellular structures developing during maize microspore culture express endosperm and embryo-specific genes and show different embryogenic potentialities. Eur J Cell Biol 84:663–675

    Article  CAS  PubMed  Google Scholar 

  • Matsushita J, Otani M, Wakita Y, Tanaka O, Shimada T (1999) Transgenic plant regeneration through silicon carbide whisker-mediated transformation of rice (Oryza sativa L.). Breed Sci 49:21–26

    Article  Google Scholar 

  • Mehrotra S, Goyal V (2012) Agrobacterium-mediated gene transfer in plants and biosafety considerations. Appl Biochem Biotechnol 168:1953–1975

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mookkan M, Nelson-Vasilchik K, Hague J, Zhang ZJ, 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 

  • Morocz S, Donn G, Nérneth J, Dudits D (1990) An improved system to obtain fertile regenerants via maize protoplasts isolated from a highly embryogenic suspension culture. Theor Appl Genet 80:721–726

    Article  CAS  PubMed  Google Scholar 

  • Murakawa T, Si K, Fukui K (2008) Improvement of bioactive bead-mediated transformation by concomitant application of electroporation. Plant Biotechnol 25:387–390

    Article  Google Scholar 

  • Negrotto D, Jolley M, Beer S, Wenck AR, Hansen G (2000) The use of phosphomannose-isomerase as a selectable marker to recover transgenic maize plants (Zea mays L.) via Agrobacterium transformation. Plant Cell Rep 19:798–803

    Article  CAS  PubMed  Google Scholar 

  • Newell CA (2000) Plant transformation technology. Mol Biotechnol 16:53–65

    Article  CAS  PubMed  Google Scholar 

  • Ochatt S, Pech C, Grewal R, Conreux C, Lulsdorf M, Jacas L (2009) Abiotic stress enhances androgenesis from isolated microspores of some legume species (Fabaceae). J Plant Physiol 166:1314–1328

    Article  CAS  PubMed  Google Scholar 

  • Odell JT, Nagy F, Chua NH (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omirulleh S, Ábrahám M, Golovkin M, Stefanov I, Karabev MK, Mustárdy L, Mórocz S, Dudits D (1993) Activity of a chimeric promoter with the doubled CaMV 35S enhancer element in protoplast-derived cells and transgenic plants in maize. Plant Mol Biol 21:415–428

    Article  CAS  PubMed  Google Scholar 

  • Ooms G, Hooykaas PJJ, Van Veen RJM, Van Beelen P, Regensburg-Tuïnk TJG, Schilperoort RA (1982) Octopine Ti-plasmid deletion mutants of Agrobacterium tumefaciens with emphasis on the right side of the T-region. Plasmid 7:15–29

    Article  CAS  PubMed  Google Scholar 

  • Ortiz JPA, Reggiardo MI, Ravizzini RA, Altabe SG, Cervigni GDL, Spitteler MA, Morata MM, Elias FE, Vallejos RH (1996) Hygromycin resistance as an efficient selectable marker for wheat stable transformation. Plant Cell Rep 15:877–881

    Article  CAS  PubMed  Google Scholar 

  • Pareddy D, Petolino J (1990) Somatic embryogenesis and plant regeneration from immature inflorescences of several elite inbreds of maize. Plant Sci 67:211–219

    Article  Google Scholar 

  • Pasternak TP, Rudas VA, Lörz H, Kumlehn J (1999) Embryogenic callus formation and plant regeneration from leaf base segments of barley (Hordeum vulgare L.). J Plant Physiol 155:371–375

    Article  CAS  Google Scholar 

  • Petolino JF, Hopkins NL, Kosegi BD, Skokut M (2000) Whisker-mediated transformation of embryogenic callus of maize. Plant Cell Rep 19:781–786

    Article  CAS  PubMed  Google Scholar 

  • Poethig RS, Sussex IM (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165:158–169

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Potrykus I (1990) Gene transfer to cereals: an assessment. Bio Technol 8:535–542

    CAS  Google Scholar 

  • Potrykus I, Paszkowski J, Saul MW, Petruska J, Shillito RD (1985) Molecular and general genetics of a hybrid foreign gene introduced into tobacco by direct gene transfer. Mol Gen Genet 199:169–177

    Article  CAS  PubMed  Google Scholar 

  • Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ (1992) Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111:229–233

    Article  CAS  PubMed  Google Scholar 

  • Privalle LS (2002) Phosphomannose isomerase, a novel plant selection system. Annals New York Acad of Sci 964:129–138

  • Puchta H (1999) Double-strand break-induced recombination between ectopic homologous sequences in somatic plant cells. Genetics 152:1173–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Que Q, Elumalai S, Li X, Zhong H, Nalapalli S, Schweiner M, Fei X, Nuccio M, Kelliher T, Gu W, Chen Z, Chilton M-DM (2014) Maize transformation technology development for commercial event generation. Front Plant Sci 5:379–379

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramkumar TR, Lenka SK, Arya SS, Bansal KC (2020) A short history and perspectives on plant genetic transformation. In: Rustgi S, Luo H (eds) Biolistic DNA delivery in plants: methods and protocols. Springer US, New York, pp 39–68. https://doi.org/10.1007/978-1-0716-0356-7_3

  • Randolph LF (1936) Developmental morphology of the caryopsis in maize. J Agr Research 53:881–916

    Google Scholar 

  • Rathore KS, Chowdhury VK, Hodges TK (1993) Use of bar as a selectable marker gene and for the production of herbicide-resistant rice plants from protoplasts. Plant Mol Biol 21:871–884

    Article  CAS  PubMed  Google Scholar 

  • Ray DS, Ghosh PD (1990) Somatic Embryogenesis and plant regeneration from cultured leaf explants of Zea mays. Ann Bot 66:497–500

    Article  Google Scholar 

  • Reichel C, Mathur J, Eckes P, Langenkemper K, Koncz C, Schell J, Reiss B, Maas C (1996) Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proc Natl Acad Sci 93:5888–5893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhodes C, Pierce D, Mettler I, Mascarenhas D, Detmer J (1988a) Genetically transformed maize plants from protoplasts. Science 240:204–207

    Article  CAS  PubMed  Google Scholar 

  • Rhodes CA, Lowe KS, Ruby KL (1988b) Plant regeneration from protoplasts isolated from embryogenic maize cell cultures. Bio Technol 6:56–60

    Google Scholar 

  • Sairam R, Parani M, Franklin G, Lifeng Z, Smith B, MacDougall J, Wilber C, Sheikhi H, Kashikar N, Meeker K (2003) Shoot meristem: an ideal explant for Zea mays L. transformation. Genome 46:323–329

    Article  CAS  PubMed  Google Scholar 

  • Salvo S, Cook J, Carlson AR, Hirsch CN, Kaeppler SM, Kaeppler HF (2018) Genetic fine-mapping of a quantitative trait locus (QTL) associated with embryogenic tissue culture response and plant regeneration ability in maize (Zea mays L.). Plant Genome 11:170111

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Sengupta S, Eavarone D, Capila I, Zhao G, Watson N, Kiziltepe T, Sasisekharan R (2005) Temporal targeting of tumour cells and neovasculature with a nanoscale delivery system. Nature 436:568–572

    Article  CAS  PubMed  Google Scholar 

  • Shah DM, Horsch RB, Klee HJ, Kishore GM, Winter JA, Tumer NE, Hironaka CM, Sanders PR, Gasser CS, Aykent S, Siegel NR, Rogers SG, Fraley RT (1986) Engineering herbicide tolerance in transgenic plants. Science 233:478–481

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Meth 2:905–909

    Article  CAS  Google Scholar 

  • Shariatpanahi ME, Bal U, Heberle-Bors E, Touraev A (2006) Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis. Physiol Plant 127:519–534

    Article  CAS  Google Scholar 

  • Sheen J (2001) Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol 127:1466–1475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheen J, Hwang S, Niwa Y, Kobayashi H, Galbraith DW (1995) Green fluorescent protein as a new vital marker in plant cells. Plant J 8:777–784

    Article  CAS  PubMed  Google Scholar 

  • Sheridan WF (1975) Growth of corn cells in culture. J Cell Biol 67:396a

    Google Scholar 

  • Sheridan WF (1982) Black Mexican Sweet corn: its uses for tissue cultures. In: WF S (ed) Maize for biological research. Plant Mol Bio Assoc, Charlottesville, pp 385–388

  • Sheridan WF, Neuffer MG (1980) Defective kernel mutants of maize II Morphological and embryo culture studies. Genetics 95:945–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shewry PR, Tatham AS, Barro F, Barcelo P, Lazzeri P (1995) Biotechnology of breadmaking: unraveling and manipulating the multi-protein gluten complex. Bio Technol 13:1185–1190

    CAS  Google Scholar 

  • Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS8 variants generated by CRISPR-Cas9 improvemaize grain yield under field drought stress conditions. Plant Biotechnol J 15:207–216

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shires ME, Florez SL, Lai TS, Curtis WR (2017) Inducible somatic embryogenesis in Theobroma cacao achieved using the DEX-activatable transcription factor-glucocorticoid receptor fusion. Biotechnol Lett 39:1747–1755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrawat AK, Lorz H (2006) Agrobacterium-mediated transformation of cereals: a promising approach crossing barriers. Plant Biotechnol J 4:575–603

    Article  CAS  PubMed  Google Scholar 

  • Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu Y-Y, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD, Urnov FD (2009) Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459:437–441

    Article  CAS  PubMed  Google Scholar 

  • Sidorov V, Gilbertson L, Addae P, Duncan D (2006) Agrobacterium-mediated transformation of seedling-derived maize callus. Plant Cell Rep 25:320–328

    Article  CAS  PubMed  Google Scholar 

  • Somers DA, Birnberg PR, Petersen WL, Brenner ML (1987) The effect of conditioned medium on colony formation from ‘Black Mexican Sweet’ corn protoplasts. Plant Sci 53:249–256

    Article  Google Scholar 

  • Springer NM, Anderson SN, Andorf CM, Ahern KR, Bai F, Barad O, Barbazuk WB, Bass HW, Baruch K, Ben-Zvi G, Buckler ES, Bukowski R, Campbell MS, Cannon EKS, Chomet P, Dawe RK, Davenport R, Dooner HK, Du LH, Du C, Easterling KA, Gault C, Guan J-C, Hunter CT, Jander G, Jiao Y, Koch KE, Kol G, Köllner TG, Kudo T, Li Q, Lu F, Mayfield-Jones D, Mei W, McCarty DR, Noshay JM, Portwood JL, Ronen G, Settles AM, Shem-Tov D, Shi J, Soifer I, Stein JC, Stitzer MC, Suzuki M, Vera DL, Vollbrecht E, Vrebalov JT, Ware D, Wei S, Wimalanathan K, Woodhouse MR, Xiong W, Brutnell TP (2018) The maize W22 genome provides a foundation for functional genomics and transposon biology. Nature Genet 50:1282–1288

    Article  CAS  PubMed  Google Scholar 

  • Stokstad, E (2019) New genetically modified corn produces up to 10% more than similar types. Science. https://doi.org/10.1126/science.aba1013

  • Somers DA, Rines HW, Gu W, Kaeppler HF, Bushnell WR (1992) Fertile, transgenic oat plants. Bio Technol 10:1589–1594

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Songstad D, Armstrong C, Petersen W, Hairston B, Hinchee M (1996) Production of transgenic maize plants and progeny by bombardment of Hi-II immature embryos. Vitro Cell Dev Biol Plant 32:179–183

    Article  Google Scholar 

  • Songstad D, Petersen W, Armstrong C (1992) Establishment of friable embryogenic (type II) callus from immature tassels of Zea mays (Poaceae). Am J Bot 79:761–764

    Article  Google Scholar 

  • Songstad DD, Petolino JF, Voytas DF, Reichert NA (2017) Genome editing of plants. Crit Rev Plant Sci 36:1–23

    Article  Google Scholar 

  • Soriano M, Li H, Boutilier K (2013) Microspore embryogenesis: establishment of embryo identity and pattern in culture. Plant Repro 26:181–196

    Article  Google Scholar 

  • Spangenberg G, Wang Z-y, Wu X, Nagel J, Potrykus I (1995) Transgenic perennial ryegrass (Lolium perenne) plants from microprojectile bombardment of embryogenic suspension cells. Plant Sci 108:209–217

    Article  CAS  Google Scholar 

  • Stadler J, Phillips R, Leonard M (2011) Mitotic blocking agents for suspension cultures of maize ‘Black Mexican Sweet’ cell lines. Genome 32:475–478

    Article  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svitashev S, Schwartz C, Lenderts B, Young JK, Mark Cigan A (2016) Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes. Nat Comm 7:13274

    Article  CAS  Google Scholar 

  • Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015) Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol 169:931–945

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson JA, Drayton PR, Frame BR, Wang K, Dunwell JM (1995) Maize transformation utilizing silicon carbide whiskers: a review. In: Cassells AC, Jones PW (eds) The methodology of plant genetic manipulation: criteria for decision making: Proceedings of the Eucarpia Plant Genetic Manipulation Section Meeting held at Cork, Ireland from September 11 to September 14, 1994. Springer Netherlands, Dordrecht, pp 75–80. https://doi.org/10.1007/978-94-011-0357-2_8

  • Tian L, Séguin A, Charest PJ (1997) Expression of the green fluorescent protein gene in conifer tissues. Plant Cell Rep 16:267–271

    Article  CAS  PubMed  Google Scholar 

  • Tomes DT, Smith OS (1985) The effect of parental genotype on initiation of embryogenic callus from elite maize (Zea mays L.) germplasm. Theor Appl Genet 70:505–509

    Article  CAS  PubMed  Google Scholar 

  • Torisky RS, Kovacs L, Avdiushko S, Newman JD, Hunt AG, Collins GB (1997) Development of a binary vector system for plant transformation based on the supervirulent Agrobacterium tumefaciens strain Chry5. Plant Cell Rep 17:102–108

    Article  CAS  PubMed  Google Scholar 

  • Toriyama K, Arimoto Y, Uchimiya H, Hinata K (1988) Transgenic rice plants after direct gene transfer into protoplasts. Bio Technol 6:1072–1074

    CAS  Google Scholar 

  • Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathi M (2017) Synthetic seed technology and its applications: a review. Intl J Plant Biotech 3:11–16

    Google Scholar 

  • Vain P (2007) Thirty years of plant transformation technology development. Plant Biotechnol J 5:221–229

    Article  CAS  PubMed  Google Scholar 

  • van den Elzen PJM, Townsend J, Lee KY, Bedbrook JR (1985) A chimaeric hygromycin resistance gene as a selectable marker in plant cells. Plant Mol Biol 5:299–302

    Article  PubMed  Google Scholar 

  • Vasil IK (2008) A short history of plant biotechnology. Phytochemistry Rev 7:387–394

    Article  CAS  Google Scholar 

  • Vasil V, Castillo AM, Fromm ME, Vasil IK (1992) Herbicide resistant fertile transgenic wheat plants obtained by microprojectile bombardment of regenerable embryogenic callus. Bio/Technol 10:667–674

    CAS  Google Scholar 

  • Vega JM, Yu W, Kennon AR, Chen X, Zhang ZJ (2008) Improvement of Agrobacterium-mediated transformation in Hi-II maize (Zea mays) using standard binary vectors. Plant Cell Rep 27:297–305

    Article  CAS  PubMed  Google Scholar 

  • Vejlupkova Z, Warman C, Sharma R, Scheller HV, Mortimer JC, Fowler JE (2020) No evidence for transient transformation via pollen magnetofection in several monocot species. Nature Plants 6(11):1323–1324

  • Wada N, Cartagena JA, Khemkladngoen N, Fukui K (2012) Bioactive bead-mediated transformation of plants with large DNA fragments. In: Dunwell J, Wetten A (eds) Transgenic plants, methods in molecular biology (methods and protocols), vol 847. Humana Press, New Jersey, pp 91–106

  • Wada N, Si K, Akiyama Y, Kawakami S, No D, Uchiyama S, Otani M, Shimada T, Nose N, Suzuki G (2009) Bioactive beads-mediated transformation of rice with large DNA fragments containing Aegilops tauschii genes. Plant Cell Rep 28(5):759–768

    Article  CAS  PubMed  Google Scholar 

  • Walters DA, Vetsch CS, Potts DE, Lundquist RC (1992) Transformation and inheritance of a hygromycin phosphotransferase gene in maize plants. Plant Mol Biol 18:189–200

    Article  CAS  PubMed  Google Scholar 

  • Wan Y, Widholm JM, Lemaux PG (1995) Type I callus as a bombardment target for generating fertile transgenic maize (Zea mays L.). Planta 196:7–14

    Article  CAS  Google Scholar 

  • Wang AS, Evans RA, Altendorf PR, Hanten JA, Doyle MC, Rosichan JL (2000a) A mannose selection system for production of fertile transgenic maize plants from protoplasts. Plant Cell Rep 19:654–660

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Zhu L, Zhao B, Zhao Y, Xie Y, Zheng Z, Li Y, Sun J, Wang H (2019) Development of a haploid-inducer mediated genome editing system for accelerating maize breeding. Mol Plant 12:597–602

    Article  PubMed  Google Scholar 

  • Wang K, Frame BR, Drayton PR, Thompson JA (1995) Silicon carbide whisker-mediated transformation: regeneration of transgenic maize plants. In: Potrykus I, Spangenberg G (eds) Gene transfer to plants. Springer lab manual. Springer, Berlin, Heidelberg, pp 186–192

  • Wang M, van Bergen S, Van Duijn B (2000b) Insights into a key developmental switch and its importance for efficient plant breeding. Plant Physiol 124:523–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenck A, Hansen G (2005) Positive selection. Methods Mol Biol (Clifton, NJ) 286:227–236

    CAS  Google Scholar 

  • White J, Chang S-YP, Bibb MJ, Bibb MJ (1990) A cassette containing the bar gene of Streptomyces hygroscopicus: a selectable marker for plant transformation. Nucleic Acids Res 18:1062–1062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willman MR, Schroll SM, Hodges TK (1989) Inheritance of somatic embryogenesis and plantlet regeneration from primary (type 1) callus in maize. Vitro Cell Dev Biol Plant 25:95–100

    Google Scholar 

  • Wong MH, Misra RP, Giraldo JP, Kwak S-Y, 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 16:1161–1172

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Crow M, Rice BR, Li F, Harris B, Liu L, Demesa-Arevalo E, Lu Z, Wang L, Fox N, Wang X, Drenkow J, Luo A, Char SN, Yang B, Sylvester AW, Gingeras TR, Schmitz RJ, Ware D, Lipka AE, Gillis J, Jackson D (2021) Single-cell RNA sequencing of developing maize ears facilitates functional analysis and trait candidate gene discovery. Dev Cell 56(4):557–568.e6

  • Yadava P, Abhishek A, Singh R, Singh I, Kaul T, Pattanayak A, Agrawal PK (2017) Advances in maize transformation technologies and development of transgenic maize. Front Plant Sci 7:1949

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang L, Cui G, Wang Y, Hao Y, Du J, Zhang H, Wang C, Zhang H, Wu S-B, Sun Y (2017) Expression of foreign genes demonstrates the effectiveness of pollen-mediated transformation in Zea mays. Front Plant Sci 8:383

    PubMed  PubMed Central  Google Scholar 

  • Yao L, Zhang Y, Liu C, Liu Y, Wang Y, Liang D, Liu J, Sahoo G, Kelliher T (2018) OsMATL mutation induces haploid seed formation in indica rice. Nat Plants 4:530–533

    Article  CAS  PubMed  Google Scholar 

  • 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 76:835–840

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Williams-Carrier R, Jackson D, Lemaux PG (1998) Expression of CDC2ZM and KNOTTED1 during in-vitro axillary shoot meristem proliferation and adventitious shoot meristem formation in maize (Zea mays L.) and barley (Hordeum vulgare L.). Planta 204:542–549

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Williams-Carrier R, Lemaux P (2002) Transformation of recalcitrant maize elite inbreds using in vitro shoot meristematic cultures induced from germinated seedlings. Plant Cell Rep 21:263–270

    Article  CAS  Google Scholar 

  • Zang N, Zhai H, Gao S, Chen W, He S, Liu Q (2009) Efficient production of transgenic plants using the bar gene for herbicide resistance in sweetpotato. Scientia Hortic 122:649–653

    Article  CAS  Google Scholar 

  • Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu J-L, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nature Comm 7:12617

    Article  CAS  Google Scholar 

  • Zhang Q, Zhang Y, Lu M-H, Chai Y-P, Jiang Y-Y, Zhou Y, Wang X-C, Chen Q-J (2019) A novel ternary vector system united with morphogenic genes enhances CRISPR/Cas delivery in maize. Plant Physiol 181:1441–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Chen M, Siemiatkowska B, Toleco MR, Jing Y, Strotmann V, Zhang J, Stahl Y, Fernie AR (2020) A highly efficient Agrobacterium-mediated method for transient gene expression and functional studies in multiple plant species. Plant Commun 1:100028

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Zhang Q, Chen QJ (2020) Agrobacterium-mediated delivery of CRISPR/Cas reagents for genome editing in plants enters an era of ternary vector systems. Sci China Life Sci 63(10):1491–1498. https://doi.org/10.1007/s11427-020-1685-9

  • Zhao X, Xu X, Xie H, Chen S, Jin W (2013) Fertilization and uniparental chromosome elimination during crosses with maize haploid inducers. Plant Physiol 163:721–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhao Z-y, Gu W, Cai T, Tagliani L, Hondred D, Bond D, Schroeder S, Rudert M, Pierce D (2002) High throughput genetic transformation mediated by Agrobacterium tumefaciens in maize. Mol Breed 8:323–333

    Article  Google Scholar 

  • Zhong H, Bolyard MG, Srinivasan C, Sticklen MB (1993) Transgenic plants of turfgrass (Agrostis palustris Huds.) from microprojectile bombardment of embryogenic callus. Plant Cell Rep 13:1–6

    Article  CAS  PubMed  Google Scholar 

  • Zhong H, Srinivasan C, Sticklen MB (1992a) In-vitro morphogenesis of corn (Zea mays L.). Planta 187:490–497

    Article  CAS  PubMed  Google Scholar 

  • Zhong H, Srinivasan C, Sticklen MB (1992b) In-vitro morphogenesis of corn (Zea mays L.): II. Differentiation of ear and tassel clusters from cultured shoot apices and immature inflorescences. Planta 187:490–497

    Article  CAS  PubMed  Google Scholar 

  • Zhong H, Sun B, Warkentin D, Zhang S, Wu R, Wu T, Sticklen MB (1996) The competence of maize shoot meristems for integrative transformation and inherited expression of transgenes. Plant Physiol 110:1097–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors wish to acknowledge the contributions of Frank McFarland, University of Wisconsin, for Fig. 2a–g; Larisa Ryan, Corteva Agriscience, for Fig. 2 h and i; and Joel P. Hague, University of Rhode Island, for assistance with references cited.

Funding

National Science Foundation Plant Genome Research Program (NSF PGRP) Grant #1444478 and by Department of Energy BER Grant #DE-SCOO18277 to APK, by NSF PGRP Grants #1725122 and #191738 and by the USDA NIFA Hatch project #IOW04714 to KW, and by NSF PGRP Grant #1917138 and by NSF-BTT-EAGER Grant#1844701 to HEK.

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  1. Department of Cell and Molecular Biology, University of Rhode Island, South Kingstown, RI, 02892, USA

    Albert P. Kausch

  2. Department of Agronomy, Iowa State University, Ames, IA, 50011, USA

    Kan Wang

  3. Department of Agronomy, University of Wisconsin, Madison, WI, 53706, USA

    Heidi F. Kaeppler

  4. Corteva Agriscience, Johnston, IA, 50131, USA

    William Gordon-Kamm

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AK is the corresponding author and all authors wrote the review.

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WGK is an employee for Corteva Agriscience, Johnston, IA 50131, USA.

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Kausch, A.P., Wang, K., Kaeppler, H.F. et al. Maize transformation: history, progress, and perspectives. Mol Breeding 41, 38 (2021). https://doi.org/10.1007/s11032-021-01225-0

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