Generation of selectable marker-free transgenic tomato resistant to drought, cold and oxidative stress using the Cre/loxP DNA excision system

Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Curr Opin Biotechnol 13:146–150. doi:10.1016/S0958-1669(02)00298-7 Badawi GH, Kawano N, Yamauchi Y, Shimada E, Sasaki R, Kubo A, Tanaka K (2004) Over-expression of ascorbate peroxidase in tobacco chloroplasts enhances the tolerance to salt stress and water deficit. Physiol Plant 121(2):231–238. doi:10.1111/j.0031-9317.2004.00308.x Becker D, Kemper E, Schell J, Masterson R (1992) New plant binary vectors with selectable markers located proximately to the left T-DNA border. Plant Mol Biol 20:1195–1197. doi:10.1007/BF00028908 Benfey PN, Ellis J, Pelletier G (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J 9:1677–1684 Berridge MJ (1997) Elementary and global aspects of calcium signaling. J Physiol 499:291–306 Breitler JC, Meynard D, Boxtel JV, Royer M, Cambillau L, Guiderdoni E (2004) A novel two T-DNA binary vector allows efficient generation of marker-free transgenic plants in three elite cultivars of rice (Oryza sativa L.). Transgenic Res 13:271–287. doi:10.1023/B:TRAG.0000034626.22918.0a Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi:10.1046/j.1365-313x.1998.00343.x Communi D, Vanweyenberg V, Erneux C (1995) Molecular study and regulation of d-myo-inositol 1, 4, 5-trisphosphate 3-kinase. Cell Signal 7:643–650. doi:10.1016/0898-6568(95)00035-N Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19. doi:10.1007/BF02712670 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 37:103–113. doi:10.1007/s11627-001-0021-2 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(6):2117–2121. doi:10.1073/pnas.94.6.2117 Ebinuma H, Sugita K, Matsunaga E, Endo S, Kasahara T (2000) Selection of marker-free transgenic plants using the oncogenes (IPT, ROLA, B, C) of Agrobacterium as selectable markers. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants II. Kluwer, Dordrecht, pp 25–46 Endo S, Sugita K, Sakai M, Tanaka H, Ebinuma H (2002) Single-step transformation for generating marker-free transgenic rice using the type MAT vector system. Plant J 30:115–122. doi:10.1046/j.1365-313X.2002.01272.x 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 a conditional lethal dominant gene. Plant Mol Biol 40:223–235. doi:10.1023/A:1006184221051 Higgins JD, Newbury HJ, Barbara DJ, Muthumeenakshi S (2006) The production of marker-free genetically engineered broccoli with sense and antisense ACC synthase 1 and ACC oxidase 1 and 2 to extend shelf-life. Mol Breed 17:7–20. doi:10.1007/s11032-005-0237-7 Huang S, Gilbertson LA, Adams TH, Malloy KP, Reisenbigler EK, Birr DH, Snyder MW, Zhang Q, Luethy MH (2004) Generation of marker-free transgenic maize by regular two-border Agrobacterium transformation vectors. Transgenic Res 13:451–461. doi:10.1007/s11248-004-1453-3 Ishige F, Takaichi M, Foster R, Chua NH, Oeda K (1999) A G-box motif (GCCACGTGCC) tetramer confers high-level constitutive expression in dicot and monocot plants. Plant J 18:443–448. doi:10.1046/j.1365-313X.1999.00456.x Khan RS, Chin DP, Nakamura I, Mii M (2006) Production of marker-free transgenic Nierembergia caerulea using MAT vector system. Plant Cell Rep 25:914–919. doi:10.1007/s00299-006-0125-6 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. doi:10.1046/j.1365-313X.1996.10010165.x Li B, Wei AY, Song CX, Li N, Zhang JR (2008) Heterologous expression of the TsVP gene improves the drought resistance of maize. Plant Biotechnol J 6:146–159. doi:10.1111/j.1467-7652.2007.00301.x Liu H, Wang QQ, Yu MM, Zhang YY, Wu YB, Zhang HX (2008) Transgenic salt-tolerant sugar beet (Beta vulgaris L.) constitutively expressing an Arabidopsis thaliana vacuolar Na+/H+ antiporter gene, AtNHX3, accumulate more soluble sugar but less salt in storage roots. Plant Cell Environ 31:1325–1334. doi:10.1111/j.1365-3040.2008.01838.x Lloyd AM, Davis RW (1994) Functional expression of the yeast FLP/FRT site-specific recombination system in Nicotiana tabacum. Mol Gen Genet 242(6):653–657. doi:10.1007/BF00283419 Lv SL, Yang AF, Zhang JR (2007) Increase of glycinebetaine synthesis improves drought tolerance in cotton. Mol Breed 20:233–248. doi:10.1007/s11032-007-9086-x McKersie BD, Chen Y, Beus M, Bowley SR, Bowler C, Inze D, D’Halluin K, Botterman J (1993) Superoxide dismutase enhances tolerance of freezing stress in transgenic Alfalfa (Medicago sativa L.). Plant Physiol 103:1155–1163. doi:10.1104/pp.103.4.1155 Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497 Park SH, Li JS, Pittman JK, Berkowitz GA, Yang HB, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci USA 102(52):18830–18835. doi:10.1073/pnas.0509512102 Qin M, Bayley C, Stockton T, Ow DW (1994) Cre recombinase-mediated site-specific recombination between plant chromosomes. Proc Natl Acad Sci USA 91(5):1706–1710. doi:10.1073/pnas.91.5.1706 Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327. doi:10.1046/j.1365-313x.2000.00787.x Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 1–3, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor Sawahel WA (1994) Transgenic plants: performance, release and containment. World J Microbiol Biotechnol 10:139–144. doi:10.1007/BF00360874 Sreekala C, Wu J, Gu K, Wang D, Tian D, Yin Z (2005) Excision of a selectable marker in transgenic rice (Oryza sativa L.) using a chemically regulated Cre/loxP system. Plant Cell Rep 24:86–94. doi:10.1007/s00299-004-0909-5 Stevenson-Paulik J, Odom AR, York JD (2002) Molecular and biochemical characterization of two plant inositol polyphosphate 6-/3-/5-kinases. J Biol Chem 277:42711–42718. doi:10.1074/jbc.M209112200 Sugita K, Matsunaga E, Ebinuma H (1999) Effective selection system for generating maker-free transgenic plants independent of sexual crossing. Plant Cell Rep 8:94l–947 Sugita K, Kasahara T, Matsunaga E, Ebinuma H (2000) A transformation vector for the production of marker-free transgenic plants containing a single copy transgenic at hi-frequency. Plant J 22:461–469. doi:10.1046/j.1365-313X.2000.00745.x Wang Y, Chen B, Hu Y, Li J, Lin Z (2005) Inducible excision of selectable marker gene from transgenic plants by the Cre/lox site-specific recombination system. Transgenic Res 14:605–614. doi:10.1007/s11248-005-0884-9 Xia HJ, Brearley C, Elge S, Kaplan B, Fromm H, Mueller-Roeber B (2003) Arabidopsis inositol polyphosphate 6-/3-kinase is a nuclear protein that complements a yeast mutant lacking a functional ArgR-Mcm1 transcription complex. Plant Cell 15:449–463. doi:10.1105/tpc.006676 Xu J, Brearley CA, Lin WH, Wang Y, Ye R, Mueller-Roeber B, Xu ZH, Xue HW (2005) A role of Arabidopsis inositol polyphosphate kinase AtIpk2α, in pollen germination and root growth. Plant Physiol 137:94–103. doi:10.1104/pp.104.045427 Yang L, Tang RJ, Zhu JQ, Liu H, Mueller-Roeber B, Xia HJ, Zhang HX (2008) Enhancement of stress tolerance in transgenic tobacco plants constitutively expressing AtIpk2β, an inositol polyphosphate 6-/3-kinase from Arabidopsis thaliana. Plant Mol Biol 66:329–343. doi:10.1007/s11103-007-9267-3 Yoshimura K, Miyao K, Gaber A, Takeda T, Kanaboshi H, Miyasaka H, Shigeoka S (2004) Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J 37:21–33. doi:10.1046/j.1365-313X.2003.01930.x Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768. doi:10.1038/90824 Zhang W, Subbarao S, Addae P, Shen A, Armstrong C, Peschke V, Gilbertson L (2003) Cre/lox-mediated marker-free transgenic plant. J Agric Biotechnol 12:589–596 Zhang YY, Li HX, Ouyang B, Lu YG, Ye ZB (2006) Chemical-induced autoexcision of selectable markers in elite tomato plants transformed with a gene conferring resistance to lepidopteran insects. Biotechnol Lett 28:1247–1253. doi:10.1007/s10529-006-9081-z Zhang ZB, Guang Y, Arana F, Chen Z, Li Y, Xia HJ (2007) Arabidopsis inositol polyphosphate 6-/3-Kinase (AtIpk2b) is involved in axillary shoot branching via auxin signaling. Plant Physiol 144:942–951. doi:10.1104/pp.106.092163 Zuo J, Niu QW, Chua NH (2000) An estrogen receptor-based transactivator XVE mediated highly inducible gene expression in transgenic plants. Plant J 24(2):265–273. doi:10.1046/j.1365-313x.2000.00868.x Zuo J, Niu QW, Simon GM, Chua NH (2001) Chemical-regulated, site-specific DNA excision in transgenic plants. Nat Biotechnol 19:157–161. doi:10.1038/84428