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Inheritance and field performance of transgenic Korean Bt rice lines resistant to rice yellow stem borer

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Transgenic Korean rice plants containing the cry1Ab gene were developed for resistance against yellow stem borer (Scirpophaga incertulas, YSB). More than 100 independent transgenic lines from three Korean varieties (P-I, P-II and P-III) were generated. The amount of Cry1Ab in transgenic T0 plants was as high as 2.88% of total soluble proteins. These levels were sufficient to cause 100% mortality of YSB larvae. The majority of T1 transgenic lines originated from the varieties P-I and P-II followed a Mendelian fashion of segregation. Deviation from the expected segregation ratio was observed in a small number of the transgenic lines of P-I and P-II origins. However, this deviation was primarily observed in the P-III originated lines. Segregation analysis of the T1 generation indicated that 1–3 copies of the cry1Ab gene were integrated into the genome of the majority of the transgenic lines originating from varieties P-I and P-II. Stunted and semi-fertile mutants were observed in some transgenic lines. These aberrations were either independent or closely linked to the introduced cry1Ab gene loci in different transgenic lines. Reduction in GUS expression levels and loss of toxicity against YSB larvae were found in some transgenic lines. The transgenic T3 and T4 lines causing 100% mortality of third instar YSB larvae in the lab were completely protected in the field. Analysis of important yield components on nine selected transgenic lines indicated that stem length, panicle length, grain number per panicle, and seed setting rates were reduced in transgenic plants compared to those in non-transgenic parental rice lines. Number of panicles per cluster, however, was significantly higher in transgenic plants. The numerical value of the average yield was in general greater in the controls than in all the transgenic lines, indicating some ‘yield drag’. Since some selected lines were highly resistant to the YSB with good yielding potential, they offer effective potential for use in insect resistance management programs.

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References

  • Alinia F, Cohen MB, Gould F (1999) Heritability of tolerance to the Cry1Ab toxin of Bacillus thuringiensis in Chilo suppressalis (Lepidoptera: Crambidae). J Econ Entomol 93:14–17

    Google Scholar 

  • Andreadis SS, Alvarez-Alfageme F, Sanchez-Ramos I, Stodola TJ, Andow DA, Milonas PG, Savopoulou-Soultani M, Castanera P (2007) Frequency of resistance to Bacillus thuringiensis toxin Cry1Ab in Greek and Spanish populations of Sesamia nonagrioides (Lepidoptera: Noctuidae). J Econ Entomol 100:195–201

    Article  PubMed  CAS  Google Scholar 

  • Butaye KMJ, Cammue BPA, Delaure SL, De Bolle MFC (2005) Approaches to minimize variation of transgene expression in plants. Mol Breed 16:79–91

    Article  Google Scholar 

  • Chen L, Zhang S, Beachy RN, Fauquet CM (1998) A protocol for consistent, large-scale production of fertile transgenic rice plants. Plant Cell Rep 18:25–31

    Article  Google Scholar 

  • Cheng XY, Sardana R, Kaplan H, Altosaar I (1998) Agrobacterium-transformed rice plants expressing synthetic cryIA(b) and cryIA(c) genes are highly toxic to striped stem borer and yellow stem borer. Proc Natl Acad Sci USA 95:2767–2772

    Article  PubMed  CAS  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349

    Article  PubMed  CAS  Google Scholar 

  • Enriquez-Obregon GA, Prieto-Samsonov DL, de la Riva GA, Perez M, Selman-Housein G, Vazquez-Padron RI (1999) Agrobacterium-mediated Japonica rice transformation: a procedure assisted by an antinecrotic treatment. Plant Cell Tissue Organ Cult 59:159–168

    Article  CAS  Google Scholar 

  • Fearing PL, Brown D, Vlachos D, Meghji M, Privalle L (1997) Quantitative analysis of CryIA(b) expression in Bt maize plants, tissues and silage, and stability of expression over successive generations. Mol Breed 3:169–176

    Article  CAS  Google Scholar 

  • Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93:7783–7788

    Article  PubMed  CAS  Google Scholar 

  • Huang FN, Buschman LL, Higgins RA (1999) Susceptibility of different instars of European corn borer (Lepidoptera: Crambidae) to diet containing Bacillus thuringiensis. J Econ Entomol 92:547–550

    Google Scholar 

  • James VA, Worland B, Snape JW, Vain P (2004) Strategies for precise quantification of transgene expression levels over several generations in rice. J Exp Bot 55:1307–1313

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Lee S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim SI, An G (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22:561–570

    Article  PubMed  CAS  Google Scholar 

  • Kathuria H, Giri J, Tyagi H, Tyagi AK (2007) Advances in transgenic rice biotechnology. Crit Rev Plant Sci 26:65–103

    Article  CAS  Google Scholar 

  • Khanna HK, Raina SK (2002) Elite indica transgenic rice plants expressing modified Cry1Ac endotoxin of Bacillus thuringiensis show enhanced resistance to yellow stem borer (Scirpophaga incertulas). Transgenic Res 11:411–423

    Article  PubMed  CAS  Google Scholar 

  • Kim CS, Lee SN, Pak KC (1996) Sreening of rice germplasms resistant to Yellow Stem Borer (YSB) insect pest. Proc Acad Agric Sci 35:8–13

    Google Scholar 

  • Koziel MG, Beland GL, Bowman C, Carozzi NB, Crenshaw R, Crossland L, Dawson J, Desai N, Hill M, Kadwell S, Launis K, Lewis K, Maddox D, Mcpherson K, Meghji MR, Merlin E, Rhodes R, Warren GW, Wright M, Evola SV (1993) Field performance of elite transgenic maize plants expressing an insecticidal protein derived from Bacillus thuringiensis. Bio/Technology 11:194–200

    Article  CAS  Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation, a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214

    Article  Google Scholar 

  • Lee SH, Lee DG, Woo HS, Lee KW, Kim DH, Kwak SS, Kim JS, Kim H, Ahsan N, Choi MS, Yang JK, Lee BH (2006) Production of transgenic orchardgrass via Agrobacterium-mediated transformation of seed-derived callus tissues. Plant Sci 171:408–414

    Article  CAS  Google Scholar 

  • Li L, Li R, Fei S, Qu R (2005) Agrobacterium-mediated transformation of common bermudagrass (Cynodon dactylon). Plant Cell Tissue Organ Cult 83:223–229

    Article  Google Scholar 

  • Lin YJ, Zhang QF (2005) Optimising the tissue culture conditions for high efficiency transformation of indica rice. Plant Cell Rep 23:540–547

    Article  PubMed  CAS  Google Scholar 

  • Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana t-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  PubMed  CAS  Google Scholar 

  • Maqbool SB, Christou P (1999) Multiple traits of agronomic importance in transgenic indica rice plants: analysis of transgene integration patterns, expression levels and stability. Mol Breed 5:471–480

    Article  Google Scholar 

  • Matzke MA, Mette MF, Matzke AJM (2000) Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol Biol 43:401–415

    Article  PubMed  CAS  Google Scholar 

  • Mehlo L, Mazithulela G, Twyman RM, Boulton MI, Davies JW, Christou P (2000) Structural analysis of transgene rearrangements and effects on expression in transgenic maize plants generated by particle bombardment. Maydica 45:277–287

    Google Scholar 

  • Mishra KK, Handa AK (2005) Meiotic re-establishment of post-transcriptional gene silencing is regulated by aberrant RNA formation in tomato (Lycopersicon esculentum cv. Mill.). Mol Breed 16:139–149

    Article  CAS  Google Scholar 

  • Rommens CMT, Rudenko GN, Dijkwel PP, Vanhaaren MJJ, Ouwerkerk PBF, Blok KM, Nijkamp HJJ, Hille J (1992) Characterization of the Ac/Ds behavior in transgenic tomato plants using plasmid rescue. Plant Mol Biol 20:61–70

    Article  PubMed  CAS  Google Scholar 

  • Sallaud C, Gay C, Larmande P, Bes M, Piffanelli P, Piegu B, Droc G, Regad F, Bourgeois E, Meynard D, Perin C, Sabau X, Ghesquiere A, Glaszmann JC, Delseny M, Guiderdoni E (2004) High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. Plant J 39:450–464

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Shu QY, Ye GY, Cui HR, Cheng XY, Xiang YB, Wu DX, Gao MW, Xia YW, Hu C, Sardana R, Altosaar I (2000) Transgenic rice plants with a synthetic cry1Ab gene from Bacillus thuringiensis were highly resistant to eight lepidopteran rice pest species. Mol Breed 6:433–439

    Article  CAS  Google Scholar 

  • Shu QY, Cui HR, Ye GY, Wu DX, Xia YW, Gao MW, Altosaar I (2002) Agronomic and morphological characterization of Agrobacterium-transformed Bt rice plants. Euphytica 127:345–352

    Article  CAS  Google Scholar 

  • Spencer TM, Obrien JV, Start WG, Adams TR, Gordonkamm WJ, Lemaux PG (1992) Segregation of transgenes in maize. Plant Mol Biol 18:201–210

    Article  PubMed  CAS  Google Scholar 

  • Svitashev S, Ananiev E, Pawlowski WP, Somers DA (2000) Association of transgene integration sites with chromosome rearrangements in hexaploid oat. Theor Appl Genet 100:872–880

    Article  CAS  Google Scholar 

  • Travella S, Ross SM, Harden J, Everett C, Snape JW, Harwood WA (2005) A comparison of transgenic barley lines produced by particle bombardment and Agrobacterium-mediated techniques. Plant Cell Rep 23:780–789

    Article  PubMed  CAS  Google Scholar 

  • Upadhyaya NM, Surin B, Ramani K, Gaudron J, Schunmann PHD, Taylor W, Waterhouse PM, Wang M-B (2000) Agrobacterium-mediated transformation of Australian rice cultivars Jarrah and Amaroo using modified promoter and selectable markers. Aust J Plant Physiol 27:201–210

    CAS  Google Scholar 

  • Vain P, James VA, Worland B, Snape JW (2002) Transgene behaviour across two generations in a large random population of transgenic rice plants produced by particle bombardment. Theor Appl Genet 105:878–889

    Article  PubMed  CAS  Google Scholar 

  • Valderrama AM, Velasquez N, Rodriguez E, Zapata A, Zaidi MA, Altosaar I, Arango R (2007) Resistance to Tecia solanivora (Lepidoptera : Gelechiidae) in three transgenic Andean varieties of potato expressing Bacillus thuringiensis Cry1Ac protein. J Econ Entomol 100:172–179

    Article  PubMed  Google Scholar 

  • van Lijsebetens M, Vanderhaeghen R, van Montagu M (1991) Insertional mutagenesis in Arabidopsis thaliana: isolation of a TDNA-linked mutation that alters leaf morphology. Theor Appl Genet 81:277–284

    Article  Google Scholar 

  • Wassenegger M, Pelissier T (1998) A model for RNA-mediated gene silencing in higher plants. Plant Mol Biol 37:349–362

    Article  PubMed  CAS  Google Scholar 

  • Weng LX, Deng HH, Xu JL, Li Q, Wang LH, Jiang ZD, Zhang HB, Li QW, Zhang LH (2006) Regeneration of sugarcane elite breeding lines and engineering of stem borer resistance. Pest Manage Sci 62:178–187

    Article  CAS  Google Scholar 

  • Wu G, Cui H, Ye G, Xia Y, Sardana R, Cheng X, Li Y, Altosaar I, Shu Q (2002) Inheritance and expression of the cry1Ab gene in Bt (Bacillus thuringiensis) transgenic rice. Theor Appl Genet 104:727–734

    Article  PubMed  CAS  Google Scholar 

  • Wunn J, Kloti A, Burkhardt PK, Biswas GCG, Launis K, Iglesias VA, Potrykus I (1996) Transgenic Indica rice breeding line IR58 expressing a synthetic cryIA(b) gene from Bacillus thuringiensis provides effective insect pest control. Bio/Technology 14:171–176

    Article  PubMed  CAS  Google Scholar 

  • Ye GY, Shu QY, Cui HR, Hu C, Gao MW, Xia YW, Cheng X, Altosaar I (2000) A leaf-section bioassay for evaluating rice stem borer resistance in transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner. Bull Entomol Res 90:179–182

    Article  PubMed  CAS  Google Scholar 

  • Ye GY, Shu QY, Yao HW, Cui HR, Cheng XY, Hu C, Xia YW, Gao MW, Altosaar I (2001) Field evaluation of resistance of transgenic rice containing a synthetic cry1Ab gene from Bacillus thuringiensis Berliner to two stem borers. J Econ Entomol 94:271–276

    Article  PubMed  CAS  Google Scholar 

  • Zaidi MA, Mohammadi M, Postel S, Masson L, Altosaar I (2005) The Bt gene cry2Aa2 driven by a tissue specific ST-LS1 promoter from potato effectively controls Heliothis virescens. Transgenic Res 14:289–298

    Article  PubMed  CAS  Google Scholar 

  • Zaidi MA, Narayanan M, Sardana R, Taga I, Postel S, Johns R, McNulty M, Mottiar Y, Mao J, Loit E, Altosaar I (2006) Optimizing the tissue culture media for efficient transformation of different indica rice genotypes. Agron Res 4:563–575

    Google Scholar 

  • Zaidi MA, Cheng X, Altosaar I (2007) Characterization of left-border flanking sequences of T-DNA integration in transgenic rice (Oryza sativa L) expressing cry1Ab. Cereal Res Commun 35(3):1375–1383

    Article  CAS  Google Scholar 

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Acknowledgements

This work was funded by grants from The Rockefeller Foundation and Natural Sciences and Engineering Research Council of Canada to IA. We are thankful to Dr Jefferson, CAMBIA, Australia for kindly providing the plant expression vector pCAMBIA1305.1. We are also grateful to Dr Upadhyaya, CSIRO, Australia for his scientific advice.

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Correspondence to Illimar Altosaar.

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Kim, S., Kim, C., Li, W. et al. Inheritance and field performance of transgenic Korean Bt rice lines resistant to rice yellow stem borer. Euphytica 164, 829–839 (2008). https://doi.org/10.1007/s10681-008-9739-9

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  • DOI: https://doi.org/10.1007/s10681-008-9739-9

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