Maize transformation technology development for commercial event generation

Frontiers in Plant Science

Volumn 5, Issue AUG, 2014, Pages

  Que, Qiudeng ^a   Elumalai, Sivamani ^a   Li, Xianggan ^a   Zhong, Heng ^a   Nalapalli, Samson ^a   Schweiner, Michael ^a   Fei, Xiaoyin ^a   Nuccio, Michael ^a   Kelliher, Timothy ^a   Gu, Weining ^a   Chen, Zhongying ^a   Chilton, Mary Dell M ^a  

^a SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

Agrobacterium; Genome modification; Maize transformation; Multi gene stack; T DNA; Targeted insertion; Trait development; Transgenic events

Indexed keywords

EID: 84907359073     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00379     Document Type: Review

References (172)

1. Adams, W., Davis, B., Kucher, L., Lowe, B., Spencer, M., and Mann, M. T. (2005). Method and Apparatus for Substantially Isolating Plant Tissues. United States Patent Application Publication. US2005/0246786 A1.
2. Ahmadabadi, M., Ruf, S., and Bock, R. (2007). A leaf-based regeneration and transformation system for maize (Zea mays L.). Transgenic Res. 16, 437-448. doi: 10.1007/s11248-006-9046-y
3. Ainley, W. M., Sastry-Dent, L., Welter, M. E., Murray, M. G., Zeitler, B., Amora, R., et al. (2013). Trait stacking via targeted genome editing. Plant Biotechnol. J. 11, 1126-1134. doi: 10.1111/pbi.12107
4. Al-Abed, D., Rudrabhatla, S., Talla, R., and Goldman, S. (2006). Split-seed: a new tool for maize researchers. Planta 223, 1355-1360. doi: 10.1007/s00425-006-0237-9
5. Albert, H., Dale, E. C., Lee, E., and Ow, D. W. (1995). Site-specific integration of DNA into wild type and mutant lox sites placed in the plant genome. Plant J. 7, 649-659. doi: 10.1046/j.1365-313X.1995.7040649.x
6. Ananiev, E. V., Wu, C., Chamberlin, M. A., Svitashev, S., Schwartz, C., Gordon-Kamm, W., et al. (2009). Artificial chromosome formation in maize (Zea mays L.). Chromosoma 118, 157-177. doi: 10.1007/s00412-008-0191-3
7. Armstrong, C. L., and Green, C. E. (1985). Establishment and maintenance of friable, embryogenic maize callus and the involvement of L-proline. Planta 164, 207-214.
8. Armstrong, C. L., Green, C. E., and Phillips, R. L. (1991). Development and availability of germplasm with high Type II culture formation response. Maize Gen. Coop. Newsl. 65, 92-93.
9. Aulinger, I. E., Peter, S. O., Schmid, J. E., and Stamp, P. (2003). Gametic embryos of maize as a target for biolistic transformation: comparison to immature zygotic embryos. Plant Cell Rep. 21, 585-591. doi: 10.1007/s00299-002-0556-7
10. Ayer, A., Wehrkamp-Richter, S., Laffaire, J.-B., Le Goff, S., Levy, J., Chaignon, S., et al. (2013). Gene targeting in maize by somatic ectopic recombination. Plant Biotechnol. J. 11, 305-314. doi: 10.1111/pbi.12014
11. Barreiro, R., Cope, J. M., Goldman, D. M., Hunter, J. L., and Pellegrineschi, A. (2011). Apparatus and Methods to Gain Access to and Extract Intact Immature Embryo from Developing Maize Kernels or Specific Internal Tissue or Structure from one or more Seeds. United States Patent Application Publication. US2011/0054969 A1.
12. Baszczynski, C. L., Bowen, B. A., Peterson, D. J., and Tagliani, L. A. (2002). Compositions and Methods to Stack Multiple Nucleotide Sequences of Interest in the Genome of a Plant. United States Patent Publication. 6,455,315 B1.
13. Bayley, C., Trolinder, N., Ray, C., Morgan, M., Quisenberry, J. E., and Ow, D. W. (1992). Engineering 2,4-D resistance in cotton. Theor. Appl. Genet. 83, 645-649. doi: 10.1007/BF00226910
14. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., and Nekraso, V. (2013). Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9:39. doi: 10.1186/1746-4811-9-39
15. Belteki, G., Marina Gertsenstein, M., Ow, D. W., and Nagy, A. (2003). Site-specific cassette exchange and germline transmission with mouse ES cells expressing φ{symbol}C31 integrase. Nat. Biotechnol. 21, 321-324. doi: 10.1038/nbt787
16. Brettschneider, R., Becker, D., and Lörz, H. (1997). Efficient transformation of scutellar tissue of immature maize embryos. Theor. Appl. Genet. 94, 737-748. doi: 10.1007/s001220050473
17. Bullock, W. P. (2011). Method and Apparatus for Extraction of Plant Embryos. United States Patent Application Publication. US2011/0078819 A1.
18. Carlson, S. R., Rudgers, G. W., Zieler, H., Mach, J. M., Luo, S., Grunden, E., et al. (2007). Meiotic transmission of an in vitro-assembled autonomous maize minichromosome. PLoS Genet. 3:e179. doi: 10.1371/journal.pgen.0030179
19. Castle, L. A., Siehl, D. L., Gorton, R., Patten, P. A., Chen, Y. H., Bertain, S., et al. (2004). Discovery and directed evolution of a glyphosate tolerance gene. Science 304, 1151-1154. doi: 10.1126/science.1096770
20. Chen, Z., Zhong, H., Kim, M., Chilton, M.-D., Richbourg, L., Jiang, Y., et al. (2014). TALEN-mediated targeted insertion of transgenes in maize. Abstract of FASEB Conference on "Genome Engineering: Cutting edge research and application".
21. Cheng, M., Lowe, B. A., Spencer, T. M., Ye, X., and Armstrong, C. L. (2004). Factors influencing Agrobacterium-mediated transformation of monocotyledonous species. In Vitro Cell. Dev. Biol. Plant. 40, 31-45. doi: 10.1079/IVP2003501
22. D'Halluin, K., Bonne, E., Bossut, M., De Beuckeleer, M., and Leemans, J. (1992). Transgenic maize plants by tissue electroporation. Plant Cell 4, 1495-1505.
23. D'Halluin, K., Vanderstraeten, C., Stals, E., Cornelissen, M., and Ruiter, R. (2008). Homologous recombination: a basis for targeted genome optimization in crop species such as maize. Plant Biotechnol. J. 6, 93-102. doi: 10.1111/j.1467-7652.2007.00305.x
24. D'Halluin, K., Vanderstraeten, C., Van Hulle, J., Joanna Rosolowska, J., Van Den Brande, I., Pennewaert, A., et al. (2013). Targeted molecular trait stacking in cotton through targeted double-strand break induction. Plant Biotechnol. J. 11, 933-941. doi: 10.1111/pbi.12085
25. Davis, B. J., and Mann, M. T. (2006). Method for Excision of Plant Embryos for Transformation. United States Patent Publication. 7,150,993.
26. Day, C. D., Lee, E., Kobayashi, J., Holappa, L. D., Albert, H., and Ow, D. W. (2000). Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. Genes Dev. 14, 2869-2880. doi: 10.1101/gad.849600
27. De Buck, S., De Paepe, A., and Depicker, A. (2013). "Transgene expression in plants, Control of, " in Sustainable Food Production, ed P. Christou (Springer), 1570-1593. doi: 10.1007/978-1-4614-5797-8_412
28. De Framond, A. J., Black, E. W., Chilton, W. S., Kayes, L., and Chilton, M.-D. (1986). Two unlinked T-DNAs can transform the same tobacco plant cell and segregate in the F1 generation. Mol. Gen. Genet. 202, 125-131. doi: 10.1007/BF00330528
29. De Paepe, A., De Buck, S., Nolf, J., Van Lerberge, E., and Depicker, A. (2013). Site-specific T-DNA integration in Arabidopsis thaliana mediated by the combined action of CRE recombinase and ΦC31 integrase. Plant J. 75, 172-184. doi: 10.1111/tpj.12202
30. Depicker, A., Herman, L., Jacobs, A., Schell, J., and Van Montagu, M. (1985). Frequencies of simultaneous transformation with different T-DNAs and their relevance to the Agrobacterium-plant cell interaction. Mol. Gen. Genet. 201, 477-484. doi: 10.1007/BF00331342
31. Djukanovic, V., Smith, J., Lowe, K., Yang, M., Gao, H., Jones, S., et al. (2013). Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J. 76, 888-899. doi: 10.1111/tpj.12335
32. Duncan, D. R., Williams, M. E., Zehr, B. E., and Widholm, J. M. (1985). The production of callus capable of plant regeneration from immature embryos of numerous Zea mays genotypes. Planta 165, 322-332. doi: 10.1007/BF00392228
33. Eby, J., Held, B., Hou, L., and Wilson, H. (2004). Methods and Compositions for the Introduction of Molecules into Cells. United States Patent Application Publication. US2004/0219676.
34. El-Itriby, H. A., Assem, S. K., Hussein, E. H. A., Abdel-Galil, F. M., and Madkour, M. A. (2003). Regeneration and transformation of Egyptian maize inbred lines via immature embryo culture and a biolistic particle delivery system. In Vitro Cell. Dev. Biol. Plant. 39, 524-531. doi: 10.1079/IVP2003439
35. Elkonin, L., and Pakhomova, N. (2000). Influence of nitrogen and phosphorus on induction embryogenic callus of sorghum. Plant Cell Tissue Organ Cult. 61, 115-123. doi: 10.1023/A:1006472418218
36. Erikson, O., Hertzberg, M., and Nasholm, T. (2004). A conditional marker gene allowing both positive and negative selection in plants. Nat. Biotechnol. 22, 455-458. doi: 10.1038/nbt946
37. Frame, B. R., Drayton, P. R., Bagnall, S. V., Lewnau, C. J., Bullock, W. P., Wilson, H. M., et al. (1994). Production of fertile transgenic maize plants by silicon carbide whisker-mediated transformation. Plant J. 6, 941-948. doi: 10.1046/j.1365-313X.1994.6060941.x
38. Frame, B. R., McMurray, J. M., Fonger, T. M., Main, M. L., Taylor, K. W., Torney, F. J., et al. (2006). Improved Agrobacterium-mediated transformation of three maize inbred lines using MS salts. Plant Cell Rep. 25, 1024-1034. doi: 10.1007/s00299-006-0145-2
39. Frame, B. R., Shou, H., Chikwamba, R. K., Zhang, Z., Xiang, C., Fonger, T. M., et al. (2002). Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiol. 129, 13-22. doi: 10.1104/pp.000653
40. Frame, B. R., Zhang, H., Cocciolone, S. M., Sidorenko, L. V., Dietrich, C. R., Pegg, S. E., et al. (2000). Production of transgenic maize from bombarded type II callus: effect of particle size and callus morphology on transformation efficiency. In Vitro Cell. Dev. Biol.-Plant. 36, 21-29. doi: 10.1007/s11627-000-0007-5
41. Frary, A., and Hamilton, C. M. (2001). Efficiency and stability of high molecular weight DNA transformation: an analysis in tomato. Transgenic Res. 10, 121-132. doi: 10.1023/A:1008924726270
42. Fromm, M. E., Taylor, L. P., and Walbot, V. (1986). Stable transformation of maize after gene transfer by electroporation. Nature 319, 791-793. doi: 10.1038/319791a0
43. Fromm, M., Morrish, F., Armstrong, C., Williams, R., Thomas, J., and Klein, T. (1990). Inheritance and expression of chimeric genes in the progeny of transgenic maize plants. BioTechnology (N Y) 8, 833-839. doi: 10.1038/nbt0990-833
44. Fu, X. D., Duc, L. T., Fontana, S., Bong, B. B., Tinjuangjun, P., Sudhakar, D., et al. (2000). Linear transgene constructs lacking vector backbone sequences generate low-copy-number transgenic plants with simple integration patterns. Transgenic Res. 9, 11-19. doi: 10.1023/A:1008993730505
45. Gao, H., Smith, J., Yang, M., Jones, S., Djukanovic, V., Nicholson, M. G., et al. (2010). Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J. 61, 176-187. doi: 10.1111/j.1365-313X.2009.04041.x
46. Geiger, H. H., and Gordillo, G. A. (2009). Doubled haploids in hybrid maize breeding. Maydica 54, 485-499.
47. Gelvin, S. B. (2010). Plant proteins involved in Agrobacterium-mediated genetic transformation. Annu. Rev. Phytopathol. 48, 45-68. doi: 10.1146/annurev-phyto-080508-081852
48. Goodarzi, H., Najafabadi, H. S., Oikonomou, P., Greco, T. M., Fish, L., Salavati, R., et al. (2012). Systematic discovery of structural elements governing stability of mammalian messenger RNAs. Nature 485, 264-268. doi: 10.1038/nature11013
49. Gordon-Kamm, W., Dilkes, B. P., Lowe, K., Hoerster, G., Sun, X., Ross, M., et al. (2002). Stimulation of the cell cycle and maize transformation by disruption of the plant retinoblastoma pathway. Proc. Natl. Acad. Sci. U.S.A. 99, 11975-11980. doi: 10.1073/pnas.142409899
50. Gordon-Kamm, W. J., Spencer, T. M., Mangano, M. L., Adams, T. R., Daines, R. J., Start, W. G., et al. (1990). Transformation of maize cell and regeneration of fertile transgenic plants. Plant Cell 2, 603-618. doi: 10.1105/tpc.2.7.603
51. Gould, J., Devey, M., Hasegawa, O., Ulian, E. C., Peterson, G., and Smith, R. H. (1991). Transformation of Zea mays L. using Agrobacterium tumefaciens and the shoot apex. Plant Physiol. 95, 426-434. doi: 10.1104/pp.95.2.426
52. Graves, A. C. F., and Goldman, S. L. (1986). The transformation of Zea mays seedlings with Agrobacterium tumefaciens. Plant Mol. Biol. 7, 43-50. doi: 10.1007/BF00020130
53. Green, C. E., and Philips, R. L. (1975). Plant regeneration from tissue culture of maize. Crop Sci. 15, 417-421. doi: 10.2135/cropsci1975.0011183X001500030040x
54. Grimsley, N., Hohn, T., Davies, J. W., and Hohn, B. (1987). Agrobacterium-mediated delivery of infectious maize streak virus into maize plants. Nature 325, 177-179. doi: 10.1038/325177a0
55. Gudynaite-Savitch, L., Johnson, D. A., and Miki, B. L. (2009). Strategies to mitigate transgene-promoter interactions. Plant Biotechnol J. 7, 472-485. doi: 10.1111/j.1467-7652.2009.00416.x
56. Guo, X. M., Zhang, X. D., Liang, R. Q., Zhang, L. Q., and Chen, Y. F. (2007). Maize transformation using xylose isomerase gene as a selection marker. J. Plant Physiol. Mol. Biol. 33, 547-552.
57. Hamilton, C. M., Frary, A., Lewis, C., and Tanksley, S. D. (1996). Stable transfer of intact high molecular weight DNA into plant chromosomes. Proc. Natl. Acad. Sci. U.S.A. 93, 9975-9979. doi: 10.1073/pnas.93.18.9975
58. Hansen, G. (2000). Evidence for Agrobacterium-induced apoptosis in maize cells. Mol. Plant Microbe Interact. 13, 649-657. doi: 10.1094/MPMI.2000.13.6.649
59. Hansen, G., and Chilton, M. D. (1996). "Agrolistic" transformation of plant cells: integration of T-strands generated in planta. Proc. Natl. Acad. Sci. U.S.A. 93, 14978-14983. doi: 10.1073/pnas.93.25.14978
60. Hansen, G., and Wright, M. S. (1999). Recent advances in the transformation of plants. Trends Plant Sci. 4, 226-231. doi: 10.1016/S1360-1385(99)01412-0
61. Hanson, B., Engler, D., York Moy, Y., Newman, B., Ralston, E., and Gutterson, N. (1999). A simple method to enrich an Agrobacterium-transformed population for plants containing only T-DNA sequences. Plant J. 19, 727-734. doi: 10.1046/j.1365-313x.1999.00564.x
62. Harper, B., McClain, S., and Ganko, E. W. (2012). Interpreting the biological relevance of bioinformatic analyses with T-DNA sequence for protein allergenicity. Regul. Toxicol. Pharmacol. 63, 426-432. doi: 10.1016/j.yrtph.2012.05.014
63. Heck, G. R., Armstrong, C. L., Astwood, J. D., Behr, C. F., Bookout, J. T., Brown, S. M., et al. (2005). Development and characterization of a CP4 EPSPS-based, glyphosate-tolerant corn event. Crop Sci. 44, 329-339. doi: 10.2135/cropsci2005.0329
64. Hellens, R., Mullineaux, P., and Klee, H. (2000). Technical focus: a guide to Agrobacterium binary Ti vectors. Trends Plant Sci. 5, 446-451. doi: 10.1016/S1360-1385(00)01740-4
65. Hiei, Y., Ishida, Y., Kasaoka, K., and 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. doi: 10.1007/s11240-006-9157-4
66. Hily, J. M., Singer, S. D., Yang, Y., and Liu, Z. (2009). A transformation booster sequence (TBS) from Petunia hybrida functions as an enhancer-blocking insulator in Arabidopsis thaliana. Plant Cell Rep. 28, 1095-1104. doi: 10.1007/s00299-009-0700-8
67. Howe, A. R., Gasser, C. S., Brown, S. M., Padgette, S. R., Hart, J., Parker, G. B., et al. (2002). Glyphosate as aselection agent for the production of fertile transgenic maize (Zea mays L.) plants. Mol. Breed. 10, 153-164. doi: 10.1023/A:1020396708088
68. Huang, S., Gilbertson, L. A., Adams, T. H., Malloy, K. P., Reisenbigler, E. K., Birr, D. H., et al. (2004). Generation of marker free transgenics maize by regular two border Agrobacterium transformation vectors. Transgenic Res. 13, 451-461. doi: 10.1007/s11248-004-1453-3
69. Huang, X., and Wei, Z. (2005). Successful Agrobacterium-mediated genetic transformation of maize elite inbred lines. Plant Cell Tissue Organ Cult. 83, 187-200. doi: 10.1007/s11240-005-5772-8
70. Ishida, Y., Hiei, Y., and Komari, T. (2007). Agrobacterium-mediated transformation of maize. Nat. Protoc. 2, 1614-1621. doi: 10.1038/nprot.2007.241
71. Ishida, Y., Saito, H., Ohta, S., Hiei, Y., Komari, T., and Kumashiro, T. (1996). High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nat. Biotechnol. 14, 745-750. doi: 10.1038/nbt0696-745
72. Jayne, S., Barbour, E., and Meyer, T. (2000). Methods for Improving Transformation Efficiency. United States Patent Publication. 6,096,947.
73. Jones, T. L. (2009). "Maize tissue culture and transformation: the first 20 years, " in Molecular Genetic Approaches to Maize Improvement, eds A. L. Kriz and B. A. Larkins (Berlin; Heidelberg: Springer-Verlag), 6-26.
74. Joshi, C. P., Zhou, H., Huang, X., and Chiang, V. L. (1997). Context sequences of translation initiation codon in plants. Plant Mol. Biol. 35, 993-1001. doi: 10.1023/A:1005816823636
75. Kant, P., Gulati, A., Harris, L., Gleddie, S., Singh, J., and Pauls, K. P. (2012). Transgenic corn plants with modified ribosomal protein L3 show decreased ear rot disease after inoculation with Fusarium graminearum. Austral. J. Crop Sci. 6, 1598-1605.
76. Komari, T., Hiei, Y., Saito, Y., Murai, N., and 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. doi: 10.1046/j.1365-313X.1996.10010165.x
77. Kondrak, M., van der Meer, I. M., and Banfalvi, Z. (2006). Generation of marker-and backbone-free transgenic potatoes by site-specific recombination and a bi-functional marker gene in a non-regular one-border agrobacterium transformation vector. Transgenic Res. 15, 729-737. doi: 10.1007/s11248-006-9021-7
78. Kononov, M. E., Bassuner, B., and Gelvin, S. B. (1997). Integration of T-DNA binary vector "backbone" sequences into the tobacco genome: evidence for multiple complex patterns of integration. Plant J. 11, 945-957. doi: 10.1046/j.1365-313X.1997.11050945.x
79. Koziel, M. G., Beland, G. L., Bowman, C., Carozzi, N. B., Crenshaw, R., Crossland, L., et al. (1993). Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Biotechnology 11, 194-200. doi: 10.1038/nbt0293-194
80. Kuraya, Y., Ohta, S., Fukuda, M., Hiei, Y., Murai, N., Hamada, K., et al. (2004). Suppression of transfer of non-T-DNA "vector backbone" sequences by multiple left border repeats in vectors for transformation of higher plants mediated by Agrobacterium tumefaciens. Mol. Breed. 14, 309-320. doi: 10.1023/B:MOLB.0000047792.77219.bb
81. Ladics, G. S., Bannon, G. A., Silvanovich, A., Robert, F., and Cressman, R. F. (2007). Comparison of conventional FASTA identity searches with the 80 amino acid sliding window FASTA search for the elucidation of potential identities to known allergens. Mol. Nutr. Food Res. 51, 985-998. doi: 10.1002/mnfr.200600231
82. Lai, F. M., Mankin, L., Mei, K. F., Jones, T., and Song, H. S. (2007). Selection System for Maize Transformation. World Intellectual Property Organization Publication. WO 2007/014844 A2.
83. Lai, F.-M., Privalle, L., Mei, K., Ghoshal, D., Shen, Y., Klucinec, J., et al. (2011). Evaluation of the E. coli D-serine ammonia lyase gene (Ec. dsdA) for use as a selectable marker in maize transformation. In Vitro Cell. Dev. Biol.-Plant. 47, 467-479. doi: 10.1007/s11627-011-9351-x
84. Le, D. T., Choi, J.-D., and Tran, L.-S. P. (2010). Amino acids conferring herbicide resistance in tobacco acetohydroxyacid synthase. GM Crops 1, 62-67. doi: 10.4161/gmcr.1.2.10856
85. Lee, H. J., Duke, M. V., and Duke, S. O. (1993). Cellular localization of protoporphyrinogen-oxidizing activities of etiolated barley (Hordeum vulgare L.) leaves (Relationship to mechanism of action of protoporphyrinogen oxidase-inhibiting herbicides). Plant Physiol. 102, 881-889.
86. Lee, L.-Y., and Gelvin, S. B. (2008). T-DNA Binary Vectors and Systems. Plant Physiol. 146, 325-332. doi: 10.1104/pp.107.113001
87. Li, G., Zhang, Q., Zhang, J., Bi, Y., and Shan, L. (2002). Establishment of multiple shoot clumps from maize (Zea mays L.) and regeneration of herbicide-resistant transgenic plantlets. Sci. China C Life Sci. 45, 40-49. doi: 10.1360/02yc9005
88. Li, X., and Nicholl, D. (2005). Development of PPO inhibitor-resistant cultures and crops. Pest Manag. Sci. 61, 277-285. doi: 10.1002/ps.1011
89. Li, X., Sandy, L., Volrath, S. L., Nicholl, D. B. G., Chilcott, C. E., Johnson, M. A., et al. (2003). Development of protoporphyrinogen oxidase as an efficient selection marker for Agrobacterium tumefaciens-mediated transformation of maize. Plant Physiol. 133, 736-747. doi: 10.1104/pp.103.026245
90. Li, Z., Moon, B. P., Xing, A., Liu, Z.-B., McCardell, R. P., Damude, H. G., et al. (2010). Stacking multiple transgenes at a selected genomic site via repeated recombinase-mediated DNA cassette exchanges. Plant Physiol. 154, 622-631. doi: 10.1104/pp.110.160093
91. Li, Z., Xing, A., Moon, B. P., McCardell, R. P., Mills, K., and Falco, S. C. (2009). Site-specific integration of transgenes in soybean via recombinase-mediated DNA cassette exchange. Plant Physiol. 151, 1087-1095. doi: 10.1104/pp.109.137612
92. Liang, Z., Zhang, K., Chen, K., and Gao, C. (2014). Targeted mutagenesis in Zea mays using TALENs and the CRISPR/Cas system. J. Genet. Genomics 41, 63-68. doi: 10.1016/j.jgg.2013.12.001
93. Liu, Y.-G., Shirano, Y., Fukaki, H., Yanai, Y., Tasaka, M., Tabata, S., et al. (1999). Complementation of plant mutants with large genomic DNA fragments by a transformation-competent artificial chromosome vector accelerates positional cloning. Proc. Natl. Acad. Sci. U.S.A. 96, 6535-6540. doi: 10.1073/pnas.96.11.6535
94. Lowe, K., Bowen, B., Hoerster, G., Ross, M., Bond, D., Pierce, D., et al. (1995). Germline transformation of maize following manipulation of chimeric shoot meristems. Biotechnology 13, 677-682. doi: 10.1038/nbt0795-677
95. Lowe, K., Prakash, N. S., Way, M., Mann, M. T., Spencer, T. M., and Boddupalli, R. S. (2009). Enhanced single copy integration events in corn via particle bombardment using low quantities of DNA. Transgenic Res. 18, 831-840. doi: 10.1007/s11248-009-9265-0
96. Luerhsen, K., and Walbot, V. (1994). The impact of AUG start codon context on maize gene expression in vivo. Plant Cell Rep. 13, 454-458.
97. Lyznik, L. A., Gordon-Kamm, W. J., and Tao, Y. (2003). Site-specific recombination for genetic engineering in plants. Plant Cell Rep. 21, 925-932. doi: 10.1007/s00299-003-0616-7
98. Lyznik, L. A., Ryan, R. D., Ritchie, S. W., and Hodges, T. K. (1989). Stable cotransformation of maize protoplasts with gusA and neo genes. Plant Mol. Biol. 13, 151-161. doi: 10.1007/BF00016134
99. Martineau, B., Voelker, T. A., and Sanders, R. A. (1994). On defining T-DNA. Plant Cel. 6, 1032-1033. doi: 10.1105/tpc.6.8.1032
100. May, B. P., Liu, H., Vollbrecht, E., Senior, L., Rabinowicz, P. D., Roh, D., et al. (2003). Maize-targeted mutagenesis: a knockout resource for maize. Proc. Natl. Acad. Sci. U.S.A. 100, 11541-11546. doi: 10.1073/pnas.1831119100
101. McCutchen, B. F., Hazel, C. B., Liu, D. L., Lu, A. L., Wayne, J. M., Olson, P. D., et al. (2007). Methods and Compositions for the Expression of a Polynucleotide of Interest. United States Patent Application Publication. US2007/0061917 A1.
102. McKnight, T. D., Lillis, M. T., and Simpson, R. B. (1987). Segregation of genes transferred to one plant cell from two separate Agrobacterium strains. Plant Mol. Biol. 8, 439-445. doi: 10.1007/BF00017989
103. Mets, L. J. (1993). Aerosol Beam Microinjector. United States Patent Number. 5,240,842
104. Meyer, P., and Saedler, H. (1996). Homology-dependent gene silencing in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 23-48. doi: 10.1146/annurev.arplant.47.1.23
105. Miller, M., Tagliani, L., Wang, N., Berka, B., Bidney, D., and Zhao, Z. Y. (2002). High efficiency transgene segregation in co-transformed maize plants using an Agrobacterium tumefaciens 2 T-DNA binary system. Transgenic Res. 11, 381-396. doi: 10.1023/A:1016390621482
106. Negrotto, D., Jolley, M., Beer, S., Wench, A. R., and 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. doi: 10.1007/s002999900187
107. O'Connor-Sánchez, A., Cabrera-Ponce, J. L., Valdez-Melara, M., Téllez-Rodríguez, P., Pons-Hernández, J. L., and Herrera-Estrella, L. (2002). Transgenic maize plants of tropical and subtropical genotypes obtained from calluses containing organogenic and embryogenic-like structures derived from shoot tips. Plant Cell Rep. 21, 302-312. doi: 10.1007/s00299-002-0502-8
108. Oltmanns, H., Frame, B., Lee, L.-Y., Johnson, S., Li, B., Wang, K., et al. (2010). Generation of backbone-free, low transgene copy plants by launching T-DNA from the Agrobacterium chromosome. Plant Physiol. 152, 1158-1166. doi: 10.1104/pp.109.148585
109. Ombori, O., Gitonga, N. M., and Machuka, J. (2008). Somatic embryogenesis and plant regeneration from immature embryos of tropical maize (Zea mays L.) inbred lines. Biotechnology 7, 224-232. doi: 10.3923/biotech.2008.224.232
110. Ombori, O., Muoma, J. V. O., and Machuka, J. (2013). Agrobacterium-mediated genetic transformation of selected tropical inbred and hybrid maize (Zea mays L.) lines. Plant Cell Tissue Organ Cult. 113, 11-23. doi: 10.1007/s11240-012-0247-1
111. Omirulleh, S., Abraham, M., Golovkin, M., Stefanov, I., Karabaev, M. K., Mustardy, L., et al. (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. doi: 10.1007/BF00028800
112. Park, S. H., Lee, B.-M., Salas, M. G., Srivatanakul, M., and Smith, R. H. (2000). Shorter T-DNA or additional virulence genes improve Agrobacterium-mediated transformation. Theor. Appl. Genet. 101, 1015-1020. doi: 10.1007/s001220051575
113. Puchta, H., Dujon, B., and Hohn, B. (1996). Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc. Natl. Acad. Sci. U.S.A. 93, 5055-5060. doi: 10.1073/pnas.93.10.5055
114. Puchta, H., and Fauser, F. (2014). Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J. 78, 727-741. doi: 10.1111/tpj.12338
115. Que, Q. (2006). Targeted Integration and Stacking of Dna Through Homologous Recombination. United States Patent Application Publication. US2006/0253918 A1.
116. Que, Q., Chilton, M.-D. M., de Fontes, C. M., He, C., Nuccio, M., Zhu, T., et al. (2010). Trait stacking in transgenic crops: challengs and opportunities. GM Crops 1, 220-229. doi: 10.4161/gmcr.1.4.13439
117. Que, Q., and Nicholl, D. (2012). Enhanced Transformation of Recalcitrant Monocots. United States Patent Application Publication. US2012/0278950 A1.
118. Register, J. C. III. Peterson, D. J., Bell, P. J., Bullock, W. P., Evans, I. J., Frame, B., et al. (1994). Structure and function of selectable and non-selectable transgenes in maize after introduction by particle bombardment. Plant Mol. Biol. 25, 951-961. doi: 10.1007/BF00014669
119. Rhodes, C. A., Lowe, K. S., and Ruby, K. L. (1988b). Plant regeneration from protoplasts isolated from embryogenic maize cell cultures. Biotechnology 6, 56-60.
120. Rhodes, C. A., Pierce, D. A., Mettler, I. J., Mascarenhas, D., and Detmer, J. J. (1988a). Genetically transformed maize plants from protoplasts. Science 240, 204-207.
121. Rout, J. R., Lowe, B. A., Purcell, J., Spelletich, A., Spencer, M., and Way, M. (2013). Method of Rapidly Transforming Monocots. United States Patent Publication. 8,395,020.
122. Sadelain, M., Papapetrou, E. P., and Bushman, F. D. (2012). Safe harbours for the integration of new DNA in the human genome. Nat. Rev. Cancer 12, 51-58. doi: 10.1038/nrc3179
123. Sadowski, P. (1986). Site-specific recombinases: changing partners and doing the twist. J. Bacteriol. 165, 341-347.
124. Sairam, R. V., Parani, M., Franklin, G., Lifeng, Z., Smith, B., MacDougall, J., et al. (2003). Shoot meristem: an ideal explant for Zea mays L. transformation. Genome 46, 323-329. doi: 10.1139/g02-120
125. Sheng, J., and Citovsky, V. (1996). Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8, 1699-1710. doi: 10.1105/tpc.8.10.1699
126. She, W., Lin, W., Zhu, Y., Chen, Y., Jin, W., Yang, Y., et al. (2010). The gypsy insulator of Drosophila melanogaster, together with its binding protein suppressor of Hairy-Wing, facilitate high and precise expression of transgenes in Arabidopsis thaliana. Genetics 185, 1141-1150. doi: 10.1534/genetics.110.117960
127. Shillito, R. D., Carswell, G. K., Johnson, C. M., DiMaio, J. J., and Harms, C. T. (1989). Regeneration of fertile plants from protoplasts of elite inbred maize. Biotechnology 7, 581-587. doi: 10.1038/nbt0689-581
128. Shukla, V. K., Doyon, Y., Miller, J. C., DeKelver, R. C., Moehle, E. A., Worden, S. E., et al. (2009). Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature 459, 437-441. doi: 10.1038/nature07992
129. Sidorov, V., Gilbertson, L., Addae, P., and Duncan, D. (2006). Agrobacterium-mediatd transformation of seedling-derived maize callus. Plant Cell Rep. 25, 320-328. doi: 10.1007/s00299-005-0058-5
130. Silvanovich, A., Bannon, G., and McClain, S. (2009). The use of E-score to determine the quality of protein alignments. Regul. Toxicol. Pharmacol. 54, S26-S31. doi: 10.1016/j.yrtph.2009.02.004
131. Simoens, C., Alliotte, T., Mendel, R., Muller, A., Schiemann, J., Van Lijsebettens, M., et al. (1986). A binary vector for transferring genomic libraries to plants. Nucleic Acids Res. 14, 8073-8090. doi: 10.1093/nar/14.20.8073
132. Singer, S. D., Cox, K. D., and Liu, Z. (2011). Enhancer-promoter interference and its prevention in transgenic plants. Plant Cell Rep. 30, 723-731. doi: 10.1007/s00299-010-0977-7
133. Sivamani, E., DeLong, R. K., and Qu, R. (2009). Protamine-mediated DNA coating remarkably improves bombardment transformation efficiency in plant cells. Plant Cell Rep. 28, 213-221. doi: 10.1007/s00299-008-0636-4
134. Songstad, D. D., Armstrong, C. L., and Peterson, W. L. (1991). AgNO3 increases type II callus production from immature embryos of maize inbred B73 and its derivatives. Plant Cell Rep. 9, 699-702. doi: 10.1007/BF00235361
135. Songstad, D. D., Armstrong, C. L., Peterson, W. L., Hairston, B., and Hinchee, M. A. W. (1996). Production of transgenic maize plants and progeny by bombardment of Hi-II immature embryos. In Vitro Cell Dev. Biol. Plant 32, 179-183. doi: 10.1007/BF02822763
136. Spencer, T. M., Gordon-Kamm, W. J., Daines, R. J., Start, W. G., and Lemaux, P. G. (1990). Bialaphos selection of stable transformants from maize cell culture. Theor. Appl. Genet. 79, 625-631. doi: 10.1007/BF00226875
137. Srivastava, V., Ariza-Nieto, M., and Wilson, A. J. (2004). Cre-mediated site-specific gene integration for consistent transgene expression in rice. Plant Biotechnol. J. 2, 169-179. doi: 10.1111/j.1467-7652.2003.00061.x
138. Srivastava, V., and Ow, D. W. (2001). Single copy primary transformants of maize obtained through the co-introduction of a recombinase-expressing construct. Plant Mol. Biol. 46, 561-566. doi: 10.1023/A:1010646100261
139. Stuiver, M. H., Ponstein, A. S., Ohl, S. A., Goddijn, O. J. M., Simons, L. H., Dekker, B. M. M., et al. (2000). Plasmids for Plant Transformation and Method for Using the Same. United States Patent Publication. 7,029,908.
140. Sugita, K., Kasahara, T., Matsunaga, E., and Ebinuma, H. (2000). A transformation vector for the production of marker-free transgenic plants containing a single copy transgene at high frequency. Plant J. 22, 461-469. doi: 10.1046/j.1365-313X.2000.00745.x
141. Sundar, I. K., and Sakthivel, N. (2008). Advances in selectable marker genes for plant transformation. J. Plant Physiol. 165, 1698-1716. doi: 10.1016/j.jplph.2008.08.002
142. Suttie, J. L., Chilton, M. D., and Que, Q. (2008). Lambda Integrase Mediated Recombination in Plants. United States Patent Publication. 7,351,877.
143. Swanda, A. P., Starr, R. A., and Jamruszka-Lewis, A. M. (2013). Automated System and Method for Separating and Sigulating Plant Embryos. United States Patent Application Publication. US2013/0167438 A1.
144. Till, B. J., Reynolds, S. H., Weil, C., Springer, N., Burtner, C., Young, K., et al. (2004). Discovery of induced point mutations in maize genes by TILLING. BMC Plant Biol. 4:12. doi: 10.1186/1471-2229-4-12
145. Timmis, R., Hirahara, E., Folster, H. G., and Surerus-Lopez, H. (2004). Automated System and Method for Harvesting and Multi-Stage Screening of Plant Embryos. United States Patent Application Publication. US2004/0267457 A1.
146. Tinland, B., Schoumacher, F., Gloeckler, V., Bravo-Angel, A. M., and Hohn, B. (1995). The Agrobacterium tumefaciens virulence D2 protein is responsible for precise integration of T-DNA into the plant genome. EMBO J. 14, 3585-3595.
147. Tisserat, B., and Vandercook, C. (1985). Development of an automated plant culture system. Plant Cell Tissue Organ Cult. 5, 107-117. doi: 10.1007/BF00040307
148. Vain, P., McMullen, M. D., and Finer, J. J. (1993). Osmotic treatment enhances particle bombardment-mediated transient and stable transformaiton of maize. Plant Cell Rep. 12, 84-88. doi: 10.1007/BF00241940
149. Valdez-Ortiz, A., Merdina-Godoy, S., Valverde, M. E., and Paredes-Lo'pez, O. (2007). A transgenic tropical maize line generated by the direct transformation of the embryo-scutellum by A. tumefaciens. Plant Cell Tissue Organ Cult. 91, 201-214. doi: 10.1007/s11240-007-9286-4
150. Vega, J. M., Yu, W., Kennon, A. R., Chen, X., and Zhang, Z. J. (2008). Improvement of Agrobacterium-mediated transformation in Hi-II maize (Zea mays) using standard binary vectors. Plant Cell Rep. 27, 297-305. doi: 10.1007/s00299-007-0463-z
151. Voytas, D. F. (2013). Plant genome engineering with sequence-specific nucleases. Annu. Rev. Plant Biol. 64, 327-350. doi: 10.1146/annurev-arplant-042811-105552
152. Walters, D., Vetsch, C., Potts, D., and Lundquist, R. (1992). Transformation and inheritance of a hygromycin phosphotransferase gene in maize plants. Plant Mol. Biol. 18, 189-200. doi: 10.1007/BF00034948
153. Wan, Y., Widholm, J. M., and Lemaux, P. G. (1995). Type I callus as a bombardment target for generating fertile transgenic maize (Zea mays L.). Planta 196, 7-14. doi: 10.1007/BF00193211
154. Wang, A. S., Evans, R. A., Altendorf, P. R., Hanten, J. A., Doyle, M. C., and Rosichan, J. L. (2000). A mannose selection system for production of fertile transgenic maize plants from protoplasts. Plant Cell Rep. 19, 654-660. doi: 10.1007/s002999900181
155. Wang, K., Frame, B., Ishida, Y., and Komari, T. (2009). "Maize transformation, " in Handbook of Maize: Genetics and Genomics, eds J. L. Bennetzen and S. Hake (Springer Science + Business Media LLC), 609-639. doi: 10.1007/978-0-387-77863-1
156. Wang, Y., Yau, Y. Y., Perkins-Balding, D., and Thomson, J. G. (2011). Recombinase technology: applications and possibilities. Plant Cell Rep. 30, 267-285. doi: 10.1007/s00299-010-0938-1
157. Wright, M., Dawson, J., Dunder, E., Suttie, J., Reed, J., Kramer, C., et al. (2001). Efficient biolistic transformation of maize (Zea mays L.) and wheat (Triticum aestivum L.) using the phosphomannose isomerase gene, pmi, as the selectable marker. Plant Cell Rep. 20, 429-436. doi: 10.1007/s002990100318
158. Wright, T. R., Shan, G. M., Walsh, T. A., Lira, J. M., Cui, C., Song, P., et al. (2010). Robust crop resistance to broadleaf and grass herbicides provided by aryloxyalkanoate dioxygenase transgenes. Proc. Natl. Acad. Sci. U.S.A. 107, 20240-20245. doi: 10.1073/pnas.1013154107
159. Xiayi, K., Xiuwen, Z., Heping, S., and Baojian, L. (1996). Electroporation of immature maize zygotic embryos and regeneration of transgenic plants. Transgenic Res. 5, 219-221. doi: 10.1007/BF01969713
160. Ye, X., Williams, E. J., Shen, J., Esser, J. A., Nichols, A. M., Petersen, M. W., et al. (2008). Plant development inhibitory genes in binary vector backbone improve quality event efficiency in soybean transformation. Transgenic Res. 17, 827-838. doi: 10.1007/s11248-008-9169-4
161. Ye, X., Williams, E. J., Shen, J., Johnson, S., Lowe, B., Radke, S., et al. (2011). Enhanced production of single copy backbone-free transgenic plants in multiple crop species using binary vectors with a pRi replication origin in Agrobacterium tumefaciens. Transgenic Res. 20, 773-786. doi: 10.1007/s11248-010-9458-6
162. Yu, G.-R., Liu, Y., Du, W.-P., Song, J., Lin, M., Xu, L.-S., et al. (2013). Optimization of Agrobacterium tumefaciens-mediated immature embryo transformation system and transformation of glyphosate-resistantg ene 2mG2-EPSPS in maize (Zea mays L.). J. of Integrative Agricult. 12, 2134-2142
163. Zhang, S., Williams-Carrier, R., and Lemaux, P. G. (2002). Transformation of recalcitrant maize elite inbreds using in vitro shoot meristematic cultures induced from germinated seedlings. Plant Cell Rep. 21, 263-270. doi: 10.1007/s00299-002-0513-5
164. Zhang, W.-J., Dewey, R. E., Boss, W., Phillippy, B. Q., and Qu, R. (2013). Enhanced Agrobacterium-mediated transformation efficiencies in monocot cells is associated with attenuated defense responses. Plant Mol. Biol. 81, 273-286. doi: 10.1007/s11103-012-9997-8
165. Zhang, W., Subbarao, S., Addae, P., Shen, A., Armstrong, C., Peschke, V., et al. (2003). Cre/lox-mediated marker gene excision in transgenic maize (Zea mays L.) plants. Theor. Appl. Genet. 107, 1157-1168. doi: 10.1007/s00122-003-1368-z
166. Zhao, C.-H., Zhang, L.-J., Ge, C., and Hu, K. (2008). Establishment and optimization of the regeneration system of mature embryos of maize (Zea mays L.). Agricult. Sci. China 7, 1046-1051. doi: 10.1016/S1671-2927(08)60145-5 doi: 10.1016/S1671-2927(08)60145-5
167. Zhao, Z-Y., Gu, W., Cai, T., Tagliani, L., Hondred, D., Bond, D., et al. (2001). High throughput genetic transformation mediated by Agrobacterium tumefaciens in maize. Mol. Breed. 8, 323-333. doi: 10.1023/A:1015243600325
168. Zhong, H., Sun, B., Warkentin, D., Zhang, S., Wu, R., Wu, T., et al. (1996). The competence of maize shoot meristems for integrative transformation and inherited expression of transgenes. Plant Physiol. 110, 1097-1107.
169. Zhu, T., Mettenburg, K., Peterson, D. J., Tagliani, L., and Baszczynski, C. L. (2000). Engineering herbicide-resistant maize using chimeric RNA/DNA oligonucleotides. Nat. Biotechnol.18, 556-558. doi: 10.1038/75435
170. Zhu, T., Peterson, D. J., Tagliani, L., St. Clari, G., Baszczynski, C. L., and Bowen, B. (1999). Targeted manipulation of maize genes in vivo using chimeric RNA/DNA oligonucleotides. Proc. Natl. Acad. Sci. U.S.A. 96, 8768-8773. doi: 10.1073/pnas.96.15.8768
171. Ziemienowicz, A., Shim, Y.-S., Matsuoka, A., Eudes, F., and Kovalchuk, I. (2012). A novel method of transgene delivery into Triticale plants using the Agrobacterium transferred DNA-derived nano-complex. Plant Physiol. 158, 1503-1513. doi: 10.1104/pp.111.192856
172. Zuo, J., Niu, Q. W., Moller, S. G., and Chua, N. H. (2001). Chemical-regulated, site-specific DNA excision in transgenic plants. Nat. Biotechnol. 19, 157-161. doi: 10.1038/84428