Advertisement

Recent Developments in Generation of Marker-Free Transgenic Plants

  • Rupesh Kumar SinghEmail author
  • Lav Sharma
  • Nitin Bohra
  • Sivalingam Anandhan
  • Eliel Ruiz-May
  • Francisco Roberto Quiroz-Figueroa
Chapter

Abstract

A plant modified through artificial insertion of a foreign DNA into its genome is referred to as “genetically modified plant” or a “transgenic” plant. The selection of the transgenic tissues during the genetic transformation process is based on the constitutively expressed marker gene(s) coding for reporters, such as those conferring resistance against antibiotics and/or herbicides. In this direction, Agrobacterium-mediated genetic co-transformation is arguably the most commonly used technique to transfer the gene(s) of interest as well as the marker gene(s). However, the latter is purposeless once a transgenic tissue has been selected. Although these marker genes are important for screening purposes, they exhibit safety concerns for the environment as well as among consumers. At times, commercial transgenic plants transfer these gene(s) to the weeds or other organisms, leading to the development of resistance among nontarget plants. Moreover, the escape of such gene could affect the wild relatives or land races via gene flow. Therefore, in order to maintain sustainability, removing the marker gene(s) from a transgenic crop is of utmost importance, prior to its commercialization. Hitherto, several methodologies have been evolved for the development of a marker-free transgenic crop. In the present summary, we discuss the merits and the shortcomings of the Agrobacterium-mediated genetic co-transformation. In addition, we review the recent developments among other approaches and their impacts and suggest directions for their maximum utilization in the near future.

Keywords

Marker-free Transgenic plant Agrobacterium-mediated genetic co-transformation Gene flow 

Notes

Acknowledgments

The authors would like to acknowledge the support from Projeto NORTE-01-0145-FEDER000017- INTERACT/ VitalityWINE, cofinanced by FEDER/Programa NORTE 2020, and Plataforma de inovação da vinha e do vinho-innovine&wine, Norte-01-0145-FEDER000038. Postdoctoral research grant (BPD/UTAD/INNOVINE&WINE/ 424/2016) to RKS is also acknowledged. Financial support (PEst-OE/QUI/UI0616/2014) provided to the Research Unit in Vila Real by Fundaçãopara a Ciência e Tecnologia (FCT), Portugal, and COMPETE is also acknowledged. Assistances from the project UID/AGR/04033/2013 and National Funds by FCT (Portuguese Foundation for Science and Technology) and the European Investment Funds by FEDER/COMPETE/POCI Operacional Competitiveness and Internationalization Programme under the Project POCI-01-0145-FEDER-006958 are also recognized. Chemistry center of Vila Real (CQ-VR) is gratefully acknowledged.

Conflict of Interest

The authors declare that there are no conflicts of interest.

References

  1. Ahmed MMS, Bian S, Wang M, Zhao J, Zhang B, Liu Q, Zhang C, Tang S, Gu M, Yu H (2017) RNAi-mediated resistance to rice black-streaked dwarf virus in transgenic rice. Transgenic Res 26:197–207PubMedCrossRefGoogle Scholar
  2. Bertalan I, Munder MC, Weiß C, Kopf J, Fischer D, Johanningmeier U (2015) A rapid, modular and marker-free chloroplast expression system for the green alga Chlamydomonas reinhardtii. J Biotechnol 195:60–66PubMedCrossRefGoogle Scholar
  3. Bevan MW, Flavell RB, Chilton MD (1983) A chimeric antibiotic resistance gene as a selectable marker for plant cell transformation. Nature 304:184–187CrossRefGoogle Scholar
  4. Breitler JC, Meynard D, Van Boxtel J, Royer M, Bonnot F, Cambillau L, Guiderdoni E (2004) A novel 2 T-DNA binary vector allows efficient generation of marker-free transgenic plants in three elite cultivars of rice (Oryza sativa L.). Transgenic Res 13:271–287PubMedCrossRefGoogle Scholar
  5. Chakraborti D, Sarkar A, Mondal HA, Schuermann D, Hohn B, Sarmah BK, Das S (2008) Cre/lox system to develop selectable marker free transgenic tobacco plants conferring resistance against sap sucking homopteran insect. Plant Cell Rep 27:1623–1633PubMedCrossRefGoogle Scholar
  6. Chiang YC, Kiang YT (1988) Genetic analysis of mannose-6-phosphate isomerase in soybeans. Genome 30:808–811CrossRefGoogle Scholar
  7. Costa DL, Piazza S, Campa M, Flachowsky H, Hanke MV, Malnoy M (2016) Efficient heat-shock removal of the selectable marker gene in genetically modified grapevine. Plant Cell Tissue Organ Cult 124:471–481CrossRefGoogle Scholar
  8. Cotsaftis O, Sallaud C, Breitler JC, Meynard D, Greco R, Pereira A, Guiderdoni E (2002) Transposon-mediated generation of T-DNA- and marker-free rice plants expressing a Bt endotoxin gene. Mol Breed 10:165–180CrossRefGoogle Scholar
  9. Dale EC, Ow DW (1991) Gene transfer with subsequent removal of the selection gene from the host genome. Proc Natl Acad Sci U S A 88:10558–10562PubMedPubMedCentralCrossRefGoogle Scholar
  10. Dale PJ, Clarke B, Fontes MG (2002) Potential for the environmental impact of transgenic crops. Nat Biotechnol 20:567–574PubMedCrossRefPubMedCentralGoogle Scholar
  11. Darbani B, Eimanifar A, Stewart CN, Camargo WN (2007) Methods to produce marker-free transgenic plants. Biotechnol J 2:83–90PubMedCrossRefPubMedCentralGoogle Scholar
  12. Darwish NA, Khan RS, Ntui VO, Nakamura I, Mii M (2014) Generation of selectable marker-free transgenic eggplant resistant to Alternariasolani using the R/RS site-specific recombination system. Plant Cell Rep 33:411–421PubMedCrossRefPubMedCentralGoogle Scholar
  13. De Block M, Debrouwer D (1991) Two T-DNA’s cotransformed into Brassica napus by a double Agrobacterium tumefaciens infection are mainly integrated at the same locus. Theor Appl Genet 82:257–263PubMedCrossRefPubMedCentralGoogle Scholar
  14. De Block M, Botterman J, Vandewiele M, Dockx J, Thoen C, Gosselé V, Movva NR, Thompson C, Montagu MV, Leemans J (1987) Engineering of herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J 6:2513–2518PubMedPubMedCentralCrossRefGoogle Scholar
  15. De Oliveira ML, Stover E, Thomson JG (2015) The codA gene as a negative selection marker in citrus. Springer Plus 17:p264CrossRefGoogle Scholar
  16. Depicker A, Herman L, Jacobs A, Schell J, Montague MV (1985) Frequencies of simultaneous transformation with different T-DNAs and their relevance to the agrobacterium plant cell interaction. Mol Gen Genet 201:477–484CrossRefGoogle Scholar
  17. Dutt M, Zambon FT, Erpen L, Soriano L, Grosser J (2018) Embryo-specific expression of a visual reporter gene as a selection system for citrus transformation. PLoS One 13:e0190413PubMedPubMedCentralCrossRefGoogle Scholar
  18. Ebinuma H, Komamine A (2001) Mat (Multi-Auto-Transformation) vector system. The oncogenes of Agrobacterium as positive markers for regeneration and selection of marker-free transgenic plants. In Vitro Cell Dev Biol Plant 37:103–113CrossRefGoogle Scholar
  19. Ebinuma H, Sugita K, Matsunaga E, Yamakado M (1997) Selection of marker-free transgenic plants using the isopentenyl transferase gene. Proc Natl Acad Sci U S A 94:2117–2121PubMedPubMedCentralCrossRefGoogle Scholar
  20. Erikson O, Hertzberg M, Nasholm T (2004) A conditional marker gene allowing both positive and negative selection in plants. Nat Biotechnol 22:455–458PubMedCrossRefPubMedCentralGoogle Scholar
  21. Éva C, Téglás F, Zelenyánszki H, Tamás C, Juhász A, Mészáros K, Tamás L (2018) Cold inducible promoter driven Cre-lox system proved to be highly efficient for marker gene excision in transgenic barley. J Biotechnol 265:15–24PubMedCrossRefPubMedCentralGoogle Scholar
  22. FAO, Food and Agriculture Organization/World Health Organization (2000) Safety aspects of genetically modified foods of plant origin. Report of a joint FAO/WHO consultation on foods derived from biotechnology. World Health Organization, GenevaGoogle Scholar
  23. Feng D, Wang Y, Wu J, Lu T, Zhang Z (2017) Development and drought tolerance assay of marker-free transgenic rice with OsAPX2 using biolistic particle-mediated co-transformation. Crop J 5:271–281CrossRefGoogle Scholar
  24. Ganguly S, Ghosh G, Purohit A, Sreevathsa R, Chaudhuri RK, Chakraborti D (2018) Effective screening of transgenic pigeonpea in presence of negative selection agents. Proc Natl Acad Sci India Sect B 88:1565CrossRefGoogle Scholar
  25. García-Almodóvar RC, Petri C, Padilla IMG, Burgos L (2014) Combination of site-specific recombination and a conditional selective marker gene allows for the production of marker-free tobacco plants. Plant Cell Tissue Organ Cult 116:205–215CrossRefGoogle Scholar
  26. Ghulam KAP, Na’imatulapidah AM (2018) Green fluorescent protein as a visual selection marker for oil palm transformation. Ind Crop Prod 115:134–145CrossRefGoogle Scholar
  27. Gilbertson LA, Huang S, Malver T (2018) Recombinant DNA constructs employing site – specific recombination United States Patent 9856485Google Scholar
  28. Gleave AP, Mitra DS, Mudge SR, Morris BA (1999) Selectable marker-free transgenic plants without sexual crossing: transient expression of Cre recombinase and use of the conditional lethal dominant gene. Plant Mol Biol 40:223–235PubMedCrossRefPubMedCentralGoogle Scholar
  29. Goldsbrough AP, Lastrella CN, Yoder JI (1993) Transposition mediated re-positioning and subsequent elimination of marker genes from transgenic tomato. Nat Biotechnol 11:1286–1292CrossRefGoogle Scholar
  30. Goldsworthy A, Street HE (1965) The carbohydrate nutrition of tomato roots: VIII. The mechanism of the inhibition by D-mannose of the respiration of excised roots. Ann Botany-London 29:45–58CrossRefGoogle Scholar
  31. Goodwin J, Pastori G, Davey M, Jones H (2004) Transgenic plants: methods and protocols. Method Mol Biol 286:191–202Google Scholar
  32. Gorbunova V, Levy AA (1999) How plants make ends meet: DNA double-strand break repair. Trends Plant Sci 4:263–269PubMedCrossRefGoogle Scholar
  33. Hare PD, Chua NH (2002) Excision of selectable marker genes from transgenic plants. Nat Biotechnol 20:575–580PubMedCrossRefGoogle Scholar
  34. He Y, Zhu M, Wang L, Wu J, Wang Q, Wang R, Zhao Y (2018) Programmed self-elimination of the CRISPR/Cas9 construct greatly accelerates the isolation of edited and transgene-free rice plants. Mol Plant 11:1210–1213PubMedCrossRefGoogle Scholar
  35. Herrera-Estrella L, De Block M, Messens E, Hernalsteens JP, Montagu MV, Schell J (1983) Chimeric genes as dominant selectable markers in plant cells. EMBO J 2:987–995PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hoelscher M, Tiller N, Teh AYH, Wu GZ, Ma JKC, Bock R (2018) High-level expression of the HIV entry inhibitor griffithsin from the plastid genome and retention of biological activity in dried tobacco leaves. Plant Mol Biol 97:357–370PubMedPubMedCentralCrossRefGoogle Scholar
  37. Holkar SK, Mandal B, Jain RK (2018) Development and validation of marker-free constructs based on nucleocapsid protein gene of watermelon bud necrosis orthotospovirus in watermelon. Curr Sci 114:1742–1747CrossRefGoogle Scholar
  38. Hu L, Li H, Qin R, Xu R, Li J, Li L, Wei P, Yang J (2016) Plant phosphomannose isomerase as a selectable marker for rice transformation. Sci Rep 6:25921PubMedPubMedCentralCrossRefGoogle Scholar
  39. Jaiwal PK, Sahoo L, Singh ND, Singh RP (2002) Strategies to deal with the concern about marker genes in transgenic plants: some environmentally friendly approaches. Curr Sci 83:128–136Google Scholar
  40. Jang JC, Sheen J (1997) Sugar sensing in higher plants. Trends Plant Sci 2:208–214CrossRefGoogle Scholar
  41. Jianru Z, Niu Q, Ikeda Y, Chua N (2002) Marker-free transformation: increasing transformation frequency by the use of regeneration-promoting genes. Curr Opin Biotechnol 13:173–180CrossRefGoogle Scholar
  42. Jo KR, Kim CJ, Kim SJ, Kim TY, Bergervoet M, Jongsma M, Visser RGF, Jacobsen E, Vossen JH (2014) Development of late blight resistant potatoes by cisgene stacking. BMC Biotechnol 14:50PubMedPubMedCentralCrossRefGoogle Scholar
  43. Joersbo M, Donaldson I, Kreiberg J, Petersen SG, Brunstedt J, Okkels FT (1998) Analysis of mannose selection used for transformation of sugar beet. Mol Breed 4:111–117CrossRefGoogle Scholar
  44. Kasai Y, Matsuzaki K, Ikeda F, Yoshimitsu Y, Harayama S (2017) Precise excision of a selectable marker gene in transgenic Coccomyxa strains by the piggyBac transposase. Algal Res 27:152–161CrossRefGoogle Scholar
  45. Kay E, Vogel TM, Bertolla F, Nalin R, Simonet P (2002) In situ transfer of antibiotic resistance genes from transgenic (transplastomic) tobacco plants to bacteria. Appl Environ Microbiol 68:3345–3351PubMedPubMedCentralCrossRefGoogle Scholar
  46. Khidr YA, Nasr MI (2018) Generation of transgenic marker-free cucumber plants by co-transformation strategy. Egyptian J Genet Cytol 47:29–43Google Scholar
  47. Kopertekh L, Krebs E, Guzmann F (2018) Improvement of conditional Cre-lox system through application of the regulatory sequences from cowpea mosaic virus. Plant Biotechnol Rep 12:127–137CrossRefGoogle Scholar
  48. Kuan YC, Thiruvengadam V, Lin JS, Liu JH, Chen TJ, Wu HM, Wang WC (2018) Broad-specificity amino acid racemase, a novel non-antibiotic selectable marker for transgenic plants. Plant Biotechnol Rep 12:27–38CrossRefGoogle Scholar
  49. Loughman BC (1966) The mechanism of absorption and utilization of phosphate by barley plants in relation to subsequent transport to the shoot. New Phytol 65:388–397CrossRefGoogle Scholar
  50. Lucca P, Ye X, Potrykus I (2001) Effective selection and regeneration of transgenic rice plants with mannose as selective agent. Mol Breed 7:43–49CrossRefGoogle Scholar
  51. Malca I, Endo RM, Long MR (1967) Mechansim of glucose counteraction of inhibition of root elongation by galactose, mannose and glucosamine. Phytopathology 57:272–278Google Scholar
  52. Maruta T, Yonemitsu M, Yabuta Y, Tamoi M, Ishikawa T, Shigeoka S (2008) Arabidopsis phosphomannose isomerase 1, but not phosphomannose isomerase 2, is essential for ascorbic acid biosynthesis. J Biol Chem 283:28842–28851PubMedPubMedCentralCrossRefGoogle Scholar
  53. McKnight TD, Lillis MT, Simpson RB (1987) Segregation of genes transferred to one plant cell from two separate Agrobacterium strains. Plant Mol Biol 8:439–445PubMedCrossRefGoogle Scholar
  54. Mentewab A, Stewart CNJ (2005) Overexpression of an Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nat Biotechnol 23:1177–1180PubMedCrossRefPubMedCentralGoogle Scholar
  55. Mészáros K, Éva C, Kiss T, Bányai J, Kiss E, Téglás F, Láng L, Karsai I, Tamás L (2015) Generating marker-free transgenic wheat using minimal gene cassette and cold-inducible Cre/lox system. Plant Mol Biol Report 33:1221–1231CrossRefGoogle Scholar
  56. Miflin BJ, Lea PJ (1977) Amino acid metabolism. Annu Rev Plant Physiol 28:299–329CrossRefGoogle Scholar
  57. Mikami T, Saeki Y, Hirai S, Shimokawa M, Umeyama Y, Kuroda Y, Kodama H (2018) Transformation efficiency and transgene expression level in marker-free RDR6-knockdown transgenic tobacco plants. Plant Biotechnol Rep 12:389–397CrossRefGoogle Scholar
  58. 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 36:1477–1491PubMedPubMedCentralCrossRefGoogle Scholar
  59. National Research Council (US) Committee on Genetically Modified Pest-Protected Plants (2000) ‘Genetically modified pest-protected plants: science and regulation’, Washington D.C: National Academy Press, p 1–246Google Scholar
  60. Negrotto D, Jolly 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 19:798–803PubMedCrossRefGoogle Scholar
  61. Nielsen KM, Bones AM, Smalla K, Elsas JDV (1998) Horizontal gene transfer from transgenic plants to terrestrial bacteria–a rare event? FEMS Microbiol Rev 22:79–103PubMedCrossRefGoogle Scholar
  62. Nishizawa-Yokoi A, Endo M, Ohtsuki N, Saika H, Toki S (2015) Precision genome editing in plants via gene targeting and piggyBac-mediated marker excision. Plant J 81:160–168PubMedCrossRefGoogle Scholar
  63. Nishizawa-Yokoi A, Endo M, Osakabe K, Saika H, Toki S (2016) Precise marker excision system using an animal-derived piggyBac transposon in plants. Plant J 77:454–463CrossRefGoogle Scholar
  64. Okennedey MM, Burger JT, Botha FC (2004) Pearl millet transformation system using the positive selectable marker gene phosphomannose isomerase. Plant Cell Rep 22:684–690CrossRefGoogle Scholar
  65. Oliva N, Chadha-Mohanty P, Poletti S, Abrigo E, Atienza G, Torrizo L, Garcia R, Dueñas CJ, Poncio MA, Balindong J, Manzanilla M, Montecillo F, Zaidem M, Barry G, Hervé P, Shou H, Slamet-Loedin IH (2014) Large-scale production and evaluation of marker-free indica rice IR64 expressing phytoferritin genes. Mol Breed 33:23–37PubMedCrossRefGoogle Scholar
  66. Osakabe K, Nishizawa-Yokoi A, Ohtsuki N, Osakabe Y, Toki S (2014) A mutated cytosine deaminase gene, codA (D314A), as an efficient negative selection marker for gene targeting in rice. Plant Cell Physiol 55:658–665PubMedCrossRefGoogle Scholar
  67. Palomo-Ríos E, Quesada MA, Matas AJ, Pliego-Alfaro F, Mercado JA (2018) The history and current status of genetic transformation in berry crops. In: Hytönen T, Graham J, Harrison R (eds) The genomes of rosaceous berries and their wild relatives. Compendium of Plant Genomes. Springer, East Malling, pp 139–160CrossRefGoogle Scholar
  68. Pego JV, Weisbeek PJ, Smeekens SCM (1999) Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiol 119:1017–1024PubMedPubMedCentralCrossRefGoogle Scholar
  69. Pérez-Bernal M, Delgado M, Cruz A, Abreu D, Valdivia O, Armas R (2017) Marker-free transgenic rice lines with a defensin gene are potentially active against phytopathogenic fungus Sarocladiumoryzae. Acta Phytopathologica et Entomologica Hungarica 52:135–144CrossRefGoogle Scholar
  70. Perl A, Galili S, Shaul O, Ben-Tzvi I, Galili G (1993) Bacterial dihydrodipicolinate synthase and desensitized aspartate kinase: two novel selectable markers for plant transformation. Nat Biotechnol 11:715–718CrossRefGoogle Scholar
  71. Petri C, López-Noguera S, Wang H, García-Almodóvar C, Alburquerque N, Burgos L (2012) A chemical-inducible Cre-LoxP system allows for elimination of selection marker genes in transgenic apricot. Plant Cell Tissue Organ Cult 110:337–346CrossRefGoogle Scholar
  72. Poliner E, Takeuchi T, Du ZY, Benning C, Farré EM (2018) Nontransgenic marker-free gene disruption by an episomal CRISPR system in the oleaginous microalga, Nannochloropsis oceanica. ACS Synth Biol 7:962–968PubMedCrossRefGoogle Scholar
  73. Proudfoot AEI, Payton MA, Wells TNC (1994) Purification and characterization of fungal and mammalian phosphomannose isomerases. J Protein Chem 13:619–627PubMedCrossRefGoogle Scholar
  74. Puchta H (2000) Removing selectable marker genes: taking the shortcut. Trends Plant Sci 5:273–274PubMedCrossRefGoogle Scholar
  75. Rajadurai G, Kalaivani A, Varanavasiyappan S, Balakrishnan N, Udayasuriyan V, Sudhakar D, Natarajan N (2018) Generation of insect resistant marker-free transgenic rice with a novel cry2AX1 gene. Electron J Plant Breeding 9:723–732CrossRefGoogle Scholar
  76. Ran Y, Patron N, Kay P, Wong D, Buchanan M, Cao Y, Sawbridge T, Davies JP, Mason J, Webb SR, Spangenberg G, Ainley WM, Walsh TA, Hayden MJ (2018) Zinc finger nuclease-mediated precision genome editing of an endogenous gene in hexaploid bread wheat (Triticumaestivum) using a DNA repair template. Plant Biotechnol J 16:2088–2101PubMedPubMedCentralCrossRefGoogle Scholar
  77. Rao MVR, Parameswari C, Sripriya R, Veluthambi K (2011) Transgene stacking and marker elimination in transgenic rice by sequential Agrobacterium-mediated co-transformation with the same selectable marker gene. Plant Cell Rep 30:1241–1252CrossRefGoogle Scholar
  78. Reed J, Privalle L, Powell ML, Meghji M, Dawson J, Dunder E, Sutthe J, Wenck A, Launis K, Kramer C, Chang YF, Hansen G, Wright M (2001) Phosphomannose isomerase: an efficient selectable marker for plant transformation. In Vitro Cell Dev Biol Plant 37:127–132CrossRefGoogle Scholar
  79. Righetti L, Djennane S, Berthelot P, Cournol R, Wilmot N, Loridon K, Vergne E, Chevreau E (2014) Elimination of the nptIImarker gene in transgenic apple and pear with a chemically inducible R/Rs recombinase. Plant Cell Tissue Organ Cult 117:335–348CrossRefGoogle Scholar
  80. Royal Society (1998) Genetically modified plants for food use. The Royal Society, LondonGoogle Scholar
  81. Schubbert R, Hohlweg U, Renz D, Doerfler W (1998) On the fate of orally ingested foreign DNA in mice: chromosomal association and placental transmission to the fetus. Mol Gen Genet 259:569–576PubMedCrossRefGoogle Scholar
  82. Shah P, Singh NK, Khare N, Rathore M, Anandhan S, Arif M, Singh RK, Das SC, Ahmed Z, Kumar N (2008) Agrobacterium mediated genetic transformation of summer squash (Cucurbita pepo L. cv. Australian green) with cbf-1using a two vector system. Plant Cell Tissue Organ Cult 95:363–371CrossRefGoogle Scholar
  83. Shao M, Michno JM, Hotton SK, Blechl A, Thomson J (2015) A bacterial gene codA encoding cytosine deaminase is an effective conditional negative selectable marker in Glycine max. Plant Cell Rep 34:1707–1716PubMedCrossRefGoogle Scholar
  84. Shimatani Z, Yokoi AN, Endo M, Toki S, Terada R (2015) Positive–negative-selection-mediated gene targeting in rice. Front Plant Sci 5:748PubMedPubMedCentralCrossRefGoogle Scholar
  85. Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K, Ezura H, Nishida K, Ariizumi T, Kondo A (2017) Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol 35:441–443PubMedCrossRefGoogle Scholar
  86. Shimatani Z, Fujikura U, Ishii H, Matsui Y, Suzuki M, Ueke Y, Taoka KI, Terada R, Nishida K, Kondo A (2018) Inheritance of co-edited genes by CRISPR-based targeted nucleotide substitutions in rice. Plant Physiol Biochem 131:78–83PubMedCrossRefGoogle Scholar
  87. Sonntag K, Wang Y, Wallbraun M (2004) A transformation method for obtaining marker-free plants based on phosphomannose isomerase. Acta Universitatis Latviensis Biol 676:223–226Google Scholar
  88. Sripriya R, Raghupathy V, Veluthambi K (2008) Generation of selectable marker-free sheath blight resistant transgenic rice plants by efficient co-transformation of a cointegrate vector T-DNA and a binary vector T-DNA in one Agrobacterium tumefaciens strain. Plant Cell Rep 27:1635–1644PubMedCrossRefPubMedCentralGoogle Scholar
  89. Srivastava V, Underwood JL, Zhao S (2017) Dual-targeting by CRISPR/Cas9 for precise excision of transgenes from rice genome. Plant Cell Tissue Org Cult 129:153–160CrossRefGoogle Scholar
  90. Tabatabaei I, Bosco CD, Bednarska M, Ruf S, Meurer J, Bock R (2018) A highly efficient sulfadiazine selection system for the generation of transgenic plants and algae. Plant Biotechnol J 7(3):638–649CrossRefGoogle Scholar
  91. Terada R, Nagahara M, Furukawa K, Shimamoto M, Yamaguchi K, Iida S (2010) Cre-lox mediated marker elimination and gene reactivation at waxy locus created in the rice genome based on strong positive-negative selection. Plant Biotechnol J 27:29–37CrossRefGoogle Scholar
  92. Verruto J, Francis K, Wang Y, Low MC, Greiner J, Tacke S, Kuzminov F, Lambert W, McCarren J, Ajjawi I, Bauman N, Kalb R, Hannum G, Moellering ER (2018) Unrestrained markerless trait stacking in Nannochloropsis gaditana through combined genome editing and marker recycling technologies. Proc Natl Acad Sci U S A 115:7015–7022CrossRefGoogle Scholar
  93. Wakita Y, Otani M, Iba K, Shimada T (1998) Co-integration, co-expression and co-segregation of an unlinked selectable marker gene and NtFAD3 gene in transgenic rice plants produced by particle bombardment. Genes Genet Syst 73:219–226PubMedCrossRefPubMedCentralGoogle Scholar
  94. Wang XH, Zhang S, Hu D, Zhao X, Li Y, Liu T, Wang J, Hou X, Li Y (2014a) BcPMI2, isolated from non-heading Chinese cabbage encoding phosphomannoseisomerase, improves stress tolerance in transgenic tobacco. Mol Biol Rep 41:2207–2216PubMedCrossRefPubMedCentralGoogle Scholar
  95. Wang Y, Zhang L, Li Y, Liu Y, Han L, Zhu Z, Wang F, Peng Y (2014b) Expression of Cry1Ab protein in a marker-free transgenic Bt rice line and its efficacy in controlling a target pest, Chilo suppressalis (Lepidoptera: Crambidae). Environ Entomol 43:528–536PubMedCrossRefPubMedCentralGoogle Scholar
  96. Wang K, Liu H, Du L, Ye X (2017) Generation of marker-free transgenic hexaploid wheat via an Agrobacterium-mediated co-transformation strategy in commercial Chinese wheat varieties. Plant Biotechnol J 15:614–623PubMedCrossRefPubMedCentralGoogle Scholar
  97. Woo HJ, Qin Y, Park SY, Park SK, Cho YG, Shin KS, Lim MH, Cho HS (2015) Development of selectable marker-free transgenic rice plants with enhanced seed tocopherol content through FLP/FRT-mediated spontaneous auto-excision. PLoS One 10:e0132667PubMedPubMedCentralCrossRefGoogle Scholar
  98. Wright M, Dawson J, Dunder E, Suttie J, Reed J, Kramer C, Chang Y, Novitzky R, Wang H, Artim-Moore L (2001) Efficient biolistic transformation of maize (Zea mays L.) using the phosphomannoseisomerase gene, pmi, as the selectable marker. Plant Cell Rep 20:429–436PubMedCrossRefPubMedCentralGoogle Scholar
  99. Xu M, Zhao S, Zhang Y, Yin H, Peng X, Cheng Z, Yang Z, Zheng J (2017) Production of marker-free transgenic rice (Oryza sativa L.) with improved nutritive quality expressing AmA1. Iran J Biotechnol 15:102–110PubMedPubMedCentralCrossRefGoogle Scholar
  100. Youssef D, Nihou A, Partier A, Tassy C, Paul W, Rogowsky PM, Beckert M, Barret P (2018) Induction of targeted deletions in transgenic bread wheat (Triticumaestivum L.) using customized meganuclease. Plant Mol Biol Report 36:71–81CrossRefGoogle Scholar
  101. Zhang Y, Liang Z, Zong Y, Wang Y, Liu J, Chen K, Qiu JL, Gao C (2016) Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. Nat Commun 7:12617PubMedPubMedCentralCrossRefGoogle Scholar
  102. Zhu Q, Yu S, Zeng D, Liu H, Wang H, Yang Z, Xie X, Shen R, Tan J, Li H, Zhao X, Zhang Q, Chen Y, Guo J, Chen L, Liu YG (2017) Development of “purple endosperm rice” by engineering anthocyanin biosynthesis in the endosperm with a high-efficiency transgene stacking system. Mol Plant 10:918–929PubMedCrossRefPubMedCentralGoogle Scholar
  103. Zou X, Peng A, Xu L, Liu X, Lei T, Yao L, He Y, Chen S (2013) Efficient auto-excision of a selectable marker gene from transgenic citrus by combining the Cre/loxP system and ipt selection. Plant Cell Rep 32:1601–1613PubMedCrossRefPubMedCentralGoogle Scholar
  104. Zubko E, Scutt C, Meyer P (2000) Intrachromosomal recombination between attP regions as a tool to remove selectable marker genes from tobacco transgenes. Nat Biotechnol 18:442–445PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Rupesh Kumar Singh
    • 1
    Email author
  • Lav Sharma
    • 2
  • Nitin Bohra
    • 3
    • 4
  • Sivalingam Anandhan
    • 5
  • Eliel Ruiz-May
    • 6
  • Francisco Roberto Quiroz-Figueroa
    • 7
  1. 1.Centro de Química de Vila Real (CQ-VR), Universidade de Trás-os-Montes e Alto DouroVila RealPortugal
  2. 2.CITAB – Centre for the Research and Technology of Agro-Environmental and Biological Sciences, University of Trás-os-Montes and Alto Douro, UTADVila RealPortugal
  3. 3.School of Genetics and Biotechnology, University of Trás-os-Montes and Alto Douro, UTADVila RealPortugal
  4. 4.Department of BiotechnologyNational Institute of TechnologyWarangalIndia
  5. 5.ICAR- Directorate of Onion and Garlic Research, RajgurunagarPuneIndia
  6. 6.Red de Estudios Moleculares Avanzados, Instituto de Ecología A. C., ClusterBioMimic®XalapaMexico
  7. 7.Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Sinaloa (CIIDIR-IPN Unidad Sinaloa), Laboratorio de Fitomejoramiento MolecularGuasaveMéxico

Personalised recommendations