Visual marker and Agrobacterium-delivered recombinase enable the manipulation of the plastid genome in greenhouse-grown tobacco plants

Plant Journal

Volumn 70, Issue 4, 2012, Pages 717-725

  Tungsuchat Huang, Tarinee ^a   Maliga, Pal ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Agrobacterium injection; marker free plastids; Nicotiana tabacum; phage recombinases; technical advance; tobacco; visual plastid markers

Indexed keywords

AGROBACTERIUM; MARKER-FREE PLASTIDS; NICOTIANA TABACUM; RECOMBINASES; TECHNICAL ADVANCES; VISUAL PLASTID MARKERS;

CELL CULTURE; GENES; GREENHOUSES; MOLECULAR BIOLOGY; TISSUE; TOBACCO;

SEED;

BACTERIAL DNA; BACTERIOPHAGE RECEPTOR; DNA POLYMERASE; GENTAMICIN; PROTEIN SYNTHESIS INHIBITOR; SITE SPECIFIC RECOMBINASE; SITE-SPECIFIC RECOMBINASE; T DNA; T-DNA;

AGRICULTURE; ARTICLE; BACTERIOPHAGE; DRUG RESISTANCE; ENZYMOLOGY; GENE INACTIVATION; GENETIC MARKER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHODOLOGY; MICROCLIMATE; PIGMENTATION; PLANT; PLANT GENE; PLANT LEAF; PLANT SEED; PLASTID GENOME; RHIZOBIUM; TOBACCO; TRANSGENIC PLANT;

AGRICULTURE; AGROBACTERIUM; ATTACHMENT SITES, MICROBIOLOGICAL; BACTERIOPHAGES; DNA NUCLEOTIDYLTRANSFERASES; DNA, BACTERIAL; DRUG RESISTANCE; ENVIRONMENT, CONTROLLED; GENE KNOCKOUT TECHNIQUES; GENES, PLANT; GENETIC MARKERS; GENOME, PLASTID; GENTAMICINS; PIGMENTATION; PLANT LEAVES; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN SYNTHESIS INHIBITORS; SEEDS; TOBACCO;

AGROBACTERIUM; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; RHIZOBIUM;

EID: 84861338083     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04918.x     Document Type: Article

References (41)

1. Cardi, T., Lenzi, P., and, Maliga, P., (2010) Chloroplasts as expression platforms for plant-produced vaccines. Expert Rev Vaccines, 9, 893-911.
2. Carrer, H., Staub, J.M., and, Maliga, P., (1990) Gentamycin resistance in Nicotiana conferred by AAC(3)-I, a narrow substrate specificity acetyl transferase. Plant Mol. Biol. 17, 301-303.
3. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
4. Corneille, S., Lutz, K., Svab, Z., and, Maliga, P., (2001) Efficient elimination of selectable marker genes from the plastid genome by the CRE-lox site-specific recombination system. Plant J. 72, 171-178.
5. Corneille, S., Lutz, K.A., Azhagiri, A.K., and, Maliga, P., (2003) Identification of functional lox sites in the plastid genome. Plant J. 35, 753-762.
6. Davarpanah, S.J., Jung, S.H., Kim, Y.J., Park, Y.I., Min, S.R., Liu, J.R., and, Jeong, W.J., (2009) Stable plastid transformation in Nicotiana benthamiana. J Plant Biol. 52, 244-250.
7. Day, A., and, Goldschmidt-Clermont, M., (2011) The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol. J. 9, 540-553.
8. Desfeux, C., Clough, S.J., and, Bent, A.F., (2000) Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol. 123, 895-904.
9. Dufourmantel, N., Pelissier, B., Garcon, F., Peltier, G., Ferullo, J.M., and, Tissot, G., (2004) Generation of fertile transplastomic soybean. Plant Mol. Biol. 55, 479-489.
10. Finer, J.J., Vain, P., Jones, M.W., and, McMullen M.D., (1992) Development of the particle inflow gun for DNA delivery to plant cells. Plant Cell Rep. 11, 323-328.
11. Hajdukiewicz, P.T.J., Gilbertson, L., and, Staub, J.M., (2001) Multiple pathways for Cre/lox-mediated recombination in plastids. Plant J. 27, 161-170.
12. Iamtham, S., and, Day, A., (2000) Removal of antibiotic resistance genes from transgenic tobacco plastids. Nat. Biotechnol. 18, 1172-1176.
13. Kanamoto, H., Yamashita, A., Asao, H., Okumura, S., Takase, H., Hattori, M., Yokota, A., and, Tomizawa, K., (2006) Efficient and stable transformation of Lactuca sativa L. cv. Cisco (lettuce) plastids. Transgenic Res. 15, 205-217.
14. Kittiwongwattana, C., Lutz, K.A., Clark, M., and, Maliga, P., (2007) Plastid marker gene excision by the phiC31 phage site-specific recombinase. Plant Mol. Biol. 64, 137-143.
15. Klaus, S.M.J., Huang, F.C., Eibl, C., Koop, H.U., and, Golds, T.J., (2003) Rapid and proven production of transplastomic tobacco plants by restoration of pigmentation and photosynthesis. Plant J. 35, 811-821.
16. Klaus, S.M.J., Huang, F.C., Golds, T.J., and, Koop, H.-U., (2004) Generation of marker-free plastid transformants using a transiently cointegrated selection gene. Nat. Biotechnol. 22, 225-229.
17. Kode, V., Mudd, E., Iamtham, S., and, Day, A., (2006) Isolation of precise plastid deletion mutants by homology-based excision: a resource for site-directed mutagenesis, multi-gene changes and high-throughput plastid transformation. Plant J. 46, 901-909.
18. Liu, C.W., Lin, C.C., Chen, J.J., and, Tseng, M.J., (2007) Stable chloroplast transformation in cabbage (Brassica oleracea L. var. capitata L.) by particle bombardment. Plant Cell Rep. 26, 1733-1744.
19. Lutz, K.A., and, Maliga, P., (2007) Construction of marker-free transplastomic plants. Curr. Opin. Biotechnol. 18, 107-114.
20. Lutz, K., Corneille, S., Azhagiri, A.K., Svab, Z., and, Maliga, P., (2004) A novel approach to plastid transformation utilizes the phiC31 phage integrase. Plant J. 37, 906-913.
21. Lutz, K.A., Bosacchi, M.H., and, Maliga, P., (2006a) Plastid marker gene excision by transiently expressed CRE recombinase. Plant J. 45, 447-456.
22. Lutz, K.A., Svab, Z., and, Maliga, P., (2006b) Construction of marker-free transplastomic tobacco using the Cre-loxP site-specific recombination system. Nat Protoc. 1, 900-910.
23. Maliga, P., (2004) Plastid transformation in higher plants. Annu Rev Plant Biol. 55, 289-313.
24. Maliga, P., and, Bock, R., (2011) Plastid biotechnology: food, fuel and medicine for the 21st century. Plant Physiol. 155, 1501-1510.
25. Maliga, P., and, Svab, Z., (2011) Engineering the plastid genome of Nicotiana sylvestris, a diploid model species for plastid genetics. In Plant Chromosome Engineering: Methods and Protocols (, Birchler, J.J., ed.). New York: Springer Science+Business Media, LLC, pp. 37-50.
26. Murray, M.G., Palmer, J.D., Cuellar, R.E., and, Thompson, W.F., (1979) Deoxyribonucleic acid sequence organization in the mung bean genome. Biochemistry, 18, 5259-5266.
27. O'Neill, C., Horvath, G.V., Horvath, E., Dix, P.J., and, Medgyesy, P., (1993) Chloroplast transformation in plants: polyethylene glycol (PEG) treatment of protoplasts is an alternative to biolistic delivery systems. Plant J. 3, 729-738.
28. Poethig, S., (1989) Genetic mosaics and cell lineage analysis in plants. Trends Genet. 5, 273-277.
29. Raubeson, L.A., and, Jansen, R.K., (2005) Chloroplast genomes of plants. In Diversity and Evolution of Plants-Genotypic and Phenotypic Variation in Higher Plants (, Henry, R.J., ed.). Wallingford, UK: CABI Publishing, pp. 45-68.
30. Ruf, S., Hermann, M., Berger, I.J., Carrer, H., and, Bock, R., (2001) Stable genetic transformation of tomato plastids: foreign protein expression in fruit. Nat. Biotechnol. 19, 870-875.
31. Ruhlman, T., Verma, D., Samson, N., and, Daniell, H., (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol. 152, 2088-2104.
32. Sanford, J.C., Smith, F.D., and, Russell, J.A., (1993) Optimizing the biolistic process for different biological applications. Methods Enzymol. 217, 483-509.
33. Singh, A.K., Verma, S.S., and, Bansal, K.C., (2010) Plastid transformation in eggplant (Solanum melongena L.). Transgenic Res. 19, 113-119.
34. Svab, Z., and, Maliga, P., (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc. Natl Acad. Sci. USA, 90, 913-917.
35. Tungsuchat-Huang, T., Sinagawa-Garcia, S.R., Paredes-Lopez, O., and, Maliga, P., (2010) Study of plastid genome stability in tobacco reveals that the loss of marker genes is more likely by gene conversion than by recombination between 34-bp loxP repeats. Plant Physiol. 153, 252-259.
36. Tungsuchat-Huang, T., Slivinski, K.M., Sinagawa-Garcia, S.R., and, Maliga, P., (2011) Visual spectinomycin resistance gene for facile identification of transplastomic sectors in tobacco leaves. Plant Mol. Biol. 76, 453-461.
37. Valkov, V.T., Gargano, D., Manna, C., Formisano, G., Dix, P.J., Gray, J.C., Scotti, N., and, Cardi, T., (2011) High efficiency plastid transformation in potato and regulation of transgene expression in leaves and tubers by alternative 5' and 3' regulatory sequences. Transgenic Res. 20, 137-151.
38. Wei, Z., Liu, Y., Lin, C., Wang, Y., Cai, Q., Dong, Y., and, Xing, S., (2011) Transformation of alfalfa chloroplasts and expression of green fluorescent protein in a forage crop. Biotechnol. Lett. 33, 2487-2494.
39. Ye, G.N., Colburn, S., Xu, C.W., Hajdukiewicz, P.T.J., and, Staub, J.M., (2003) Persistance of unselected transgenic DNA during a plastid transformation and segregation approach to herbicide resistance. Plant Physiol. 133, 402-410.
40. Ye, G.N., Daniell, H., and, Sanford, J.C., (1990) Optimization of delivery of foreign DNA into higher-plant chloroplasts. Plant Mol. Biol. 15, 809-819.
41. Zubko, M.K., Zubko, E.I., van Zuilen, K., Mayer, P., and, Day, A., (2004) Stable transformation of petunia plastids. Transgenic Res. 13, 523-530.