Reduced generation time of apple seedlings to within a year by means of a plant virus vector: A new plant-breeding technique with no transmission of genetic modification to the next generation

Plant Biotechnology Journal

Volumn 12, Issue 1, 2014, Pages 60-68

  Yamagishi, Noriko ^a   Kishigami, Ryusuke ^a   Yoshikawa, Nobuyuki ^a  

^a IWATE UNIVERSITY   (Japan)

Author keywords

Apple latent spherical virus vector; Apple seedling; Early flowering; New breeding technique; Reduction in generation time

Indexed keywords

APPLE LATENT SPHERICAL VIRUS; ARABIDOPSIS; MALUS; MALUS X DOMESTICA;

APPLE LATENT SPHERICAL VIRUS VECTOR; APPLE SEEDLING; ARTICLE; EARLY FLOWERING; FLOWER; GENE EXPRESSION REGULATION; GENETICS; MALUS; NEW BREEDING TECHNIQUE; PHYSIOLOGY; PLANT VIRUS; REDUCTION IN GENERATION TIME; SEEDLING; TRANSGENIC PLANT;

APPLE LATENT SPHERICAL VIRUS VECTOR; APPLE SEEDLING; EARLY FLOWERING; NEW BREEDING TECHNIQUE; REDUCTION IN GENERATION TIME;

FLOWERS; GENE EXPRESSION REGULATION, PLANT; MALUS; PLANT VIRUSES; PLANTS, GENETICALLY MODIFIED; SEEDLING;

EID: 84891165419     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12116     Document Type: Article

References (44)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., Ichinoki, H., Notaguchi, M., Goto, K. and Araki, T. (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science, 309, 1052-1056.
2. Bäurle, I. and Dean, C. (2006) The timing of developmental transitions in plants. Cell, 125, 655-664.
3. Böhlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H. and Nilsson, O. (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science, 312, 1040-1043.
4. Bradlley, D., Ratcliffe, O., Vincent, C., Carpenter, R. and Coen, E. (1997) Inflorescence commitment and architecture in Arabidopsis. Science, 275, 80-83.
5. Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C. and Coupland, G. (2007) FT protein movement contributes to long-distance signalling in floral induction of Arabidopsis. Science, 316, 1030-1033.
6. Crosby, J.A., Janick, J., Pecknold, P.C., Korban, S.S., O'Connon, P.A., Ries, S.M., Goffreda, J. and Voordeckers, A. (1992) Breeding apples for scab resistance: 1945-1990. Fruit Var. J. 46, 145-166.
7. Crosby, J.A., Janick, J. and Pecknold, P.C. (1994) 'GoldRush' apple. HortSci. 29, 827-828.
8. Endo, T., Shimada, T., Fujii, H., Kobayashi, Y., Araki, T. and Omura, M. (2005) Ectopic expression of an FT homolog from Citrus confers an early flowering phenotype on trifoliate orange (Poncirus trifoliate L. Raf). Transgenic Res. 14, 703-712.
9. Esumi, T., Tao, R. and Yonemori, K. (2005) Isolation of LEAFY and TERMINAL FLOWER 1 homologues from six fruit tree species in the subfamily Maloideae of the Rosaceae. Sex. Plant Reprod. 17, 277-287.
10. Fischer, C. (1994) Shortening of the juvenile period in apple breeding. In Developments in Plant Breeding: Progress in Temperate Fruit Breeding (Schmidt, H. and Kellerhals, M., eds), pp. 161-164. London: Kluwer Academic Publishers.
11. Flachowsky, H., Hanke, M.-V., Peil, A., Strauss, S.H. and Fladung, M. (2009) A review on transgenic approaches to accelerate breeding of woody plants. Plant Breed. 128, 217-226.
12. Flachowsky, H., Le Roux, P.M., Peil, A., Patocchi, A., Richter, K. and Hanke, M.-V. (2011) Application of a high-speed breeding technology to apple (Malus x domestica) based on transgenic early flowering plants and marker-assisted selection. New Phytol. 192, 364-377.
13. Flachowsky, H., Szankowski, I., Waidmann, S., Peil, A., Tränkner, C. and Hanke, M.-V. (2012) The MdTFL1 gene of apple (Malus x domestica Borkh.) reduces vegetative growth and generation time. Tree Physiol. 32, 1288-1301.
14. Freiman, A., Shlizerman, L., Golobovitch, S., Yablovitz, Z., Korchinsky, R., Cohen, Y., Samach, A., Chevreau, E., Le Roux, P.-M., Patocchi, A. and Flaishman, M.A. (2012) Development of transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2. Planta, 235, 1239-1251.
15. Gleba, Y., Marillonnet, S. and Klimyuk, V. (2004) Engineering viral expression vectors for plants: the 'full virus' and the 'deconstructed virus' strategies. Curr. Opin. Plant Biol. 7, 182-188.
16. Hättach, C., Flachowsky, H., Kapturska, D. and Hanke, M.-V. (2008) Isolation of flowering genes and seasonal changes in their transcript levels related to flower induction and initiation in apple (Malus x domestica). Tree Physiol. 28, 1459-1466.
17. Hecht, V., Laurie, R.E., Vander Schoor, J.K., Ridge, S., Knowles, C.L., Liew, L.C., Sussmilch, F.C., Murfet, I.C., Macknight, R.C. and Weller, J.L. (2011) The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell, 23, 147-161.
18. Hsu, C.-Y., Liu, Y., Luthe, D.S. and Yuceer, C. (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. The Plant Cell, 18, 1846-1861 doi: 10.1105/tpc.106.041038.
19. Huijser, P. and Schmid, M. (2011) The control of developmental phase transitions in plants. Development, 138, 4117-4129.
20. Igarashi, A., Yamagata, K., Sugai, T., Takahashi, Y., Sugawara, E., Tamura, A., Yaegashi, H., Yamagishi, N., Takahashi, T., Isogai, M., Takahashi, H. and Yoshikawa, N. (2009) Apple latent spherical virus vectors for reliable and effective virus-induced gene silencing among a broad range of plants including tobacco, tomato, Arabidopsis thaliana, cucurbits, and legumes. Virology, 386, 407-416.
21. Imamura, T., Nakatsuka, T., Higuchi, A., Nishihara, M. and Takahashi, H. (2011) The gentian orthorogs of the FT/TFL1 gene family control floral initiation in Gentiana. Plant Cell Physiol. 52, 1031-1041.
22. Kong, F., Liu, B., Xia, Z., Sato, S., Kim, B., Watanabe, S., Yamada, T., Tabata, S., Kanazawa, A., Harada, K. and Abe, J. (2010) Two coordinately regulated homologs of FLOWERING LOCUS T are involved in the control of photoperiodic flowering in soybean. Plant Physiol. 154, 1220-1231.
23. Kotoda, N. and Wada, M. (2005) MdTFL1, a TFL1-like gene of apple, retards the transition from the vegetative to reproductive phase in transgenic Arabidopsis. Plant Sci. 168, 95-104.
24. Kotoda, N., Iwanami, H., Takahashi, S. and Abe, K. (2006) Antisense expression of MdTFL1, a TFL1-like gene, reduce the juvenile phase in apple. J. Am. Soc. Hort. Sci. 131, 74-81.
25. Kotoda, N., Hayashi, H., Suzuki, M., Igarashi, M., Hatsuyama, Y., Kidou, S.-I., Igasaki, T., Nishiguchi, M., Yano, K., Shimizu, T., Takahashi, S., Iwanami, H., Moriya, S. and Abe, K. (2010) Molecular characterization of FLOWERING LOCUS T-like genes of apple (Malus x domestica Borkh.). Plant Cell Physiol. 51, 561-575.
26. Le Roux, P.-M., Flachowsky, H., Hanke, M.-V., Gesseler, C. and Patocchi, A. (2012) Use of transgenic early flowering approach in apple (Malus x domestica Borkh.) to introgress fire blight resistance from cultivar Evereste. Mol. Breeding, 30, 857-874.
27. Li, C., Sasaki, N., Isogai, M. and Yoshikawa, N. (2004) Stable expression of foreign proteins in herbaceous and apple plants using Apple latent spherical virus RNA2 vectors. Arch. Virol. 149, 1541-1558.
28. Lv, L., Duan, J., Xie, J.H., Wei, C.B., Liu, Y.G., Liu, S.H. and Sun, G.M. (2012) Isolation and characterization of a FLOWERING LOCUS T homolog from pineapple (Ananas comosus (L.) Merr). Gene, 505, 368-373.
29. Matsuda, N., Ikeda, K., Kurosaka, M., Takashina, T., Isuzugawa, K., Endo, T. and Omura, M. (2009) Early flowering phenotype in transgenic pears (Pyrus communis L.) expressing the CiFT gene. J. Japan Soc. Hort. Sci. 78, 410-416.
30. Mimida, N., Kotoda, N., Ueda, T., Igarashi, M., Hatsuyama, Y., Iwanami, H., Moriya, S. and Abe, K. (2009) Four TFL1/CEN-like genes on distinct linkage groups show different expression patterns to regulate vegetative and reproductive development in apple (Malus x domestica Borkh.). Plant Cell Physiol. 50, 394-412.
31. Mimida, N., Ureshino, A., Tanaka, N., Shigeta, N., Sato, N., Moriya-Tanaka, Y., Iwanami, H., Honda, C., Suzuki, A., Komori, S. and Wada, M. (2011) Expression patterns of several floral genes during flower initiation in the apical buds of apple (Malus x domestica Borkh.) revealed by in situ hybridization. Plant Cell Rep. 30, 1485-1492.
32. Nakamura, K., Yamagishi, N., Isogai, M., Komori, S., Ito, T. and Yoshikawa, N. (2011) Seed and pollen transmission of Apple latent spherical virus in apple. J. Gen. Plant Pathol. 77, 48-53.
33. Notaguchi, M., Abe, M., Kimura, T., Daimon, Y., Kobayashi, T., Yamaguchi, A., Tomita, Y., Dohi, K., Mori, M. and Araki, T. (2008) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol. 49, 1645-1658.
34. Purkayastha, A. and Dasgupta, I. (2009) Virus-induced gene silencing: a versatile tool for discovery of gene function in plants. Plant Physiol. Biochem. 47, 967-976.
35. Ratcliffe, O.J., Amaya, I., Vincent, C.A., Rothstein, S., Carpenter, R., Coen, E.S. and Bradley, D.J. (1998) A common mechanism controls the life cycle and architecture of plants. Development, 125, 1609-1615.
36. Ratcliffe, O.J., Bradley, D.J. and Coen, E.S. (1999) Separation of shoot and floral identity in Arabidopsis. Development, 126, 1109-1120.
37. Sasaki, S., Yamagishi, N. and Yoshikawa, N. (2011) Efficient virus-induced gene silencing in apple, pear, and Japanese pear using Apple latent spherical virus vectors. Plant Methods, 7, 15.
38. Srinivasan, C., Dardick, C., Callahan, A. and Scorza, R. (2012) Plum (Prunus domestica) trees transformed with poplar FT1 result in altered architecture, dormancy requirement, and continuous flowering. PLoS ONE, 7, e40715.
39. Tamaki, S., Matsuo, S., Wong, H.L., Yokoi, S. and Shimamoto, K. (2007) Hd3a protein is a mobile flowering signal in rice. Science, 316, 1033-1036.
40. Tränkner, C., Lehmann, S., Hoenicka, H., Hanke, M.-V., Fladung, M., Lenhardt, D., Dunemann, F., Gau, A., Schlangen, K., Malony, M. and Flachowsky, H. (2010) Over-expression of an FT-homologous gene of apple induces early flowering in annual and perennial plants. Planta, 232, 1309-1324.
41. Wang, J.-W., Park, M.Y., Wang, L.-J., Koo, Y., Chen, X.-Y., Weigel, D. and Poethig, R.S. (2011) MiRNA control of vegetative phase change in trees. PLoS Genet. 7, e1002012.
42. Yamagishi, N., Sasaki, S. and Yoshikawa, N. (2010) Highly efficient inoculation method of apple viruses to apple seedlings. Julius-Kuhn-Archiv. 427, 226-229 (http://icvf.jki.bund.de).
43. Yamagishi, N., Sasaki, S., Yamagata, K., Komori, S., Nagase, M., Wada, M., Yamamoto, T. and Yoshikawa, N. (2011) Promotion of flowering and reduction of a generation time in apple seedlings by ectopical expression of the Arabidopsis thaliana FT gene using the Apple latent spherical virus vector. Plant Mol. Biol. 75, 193-204.
44. Zhang, H., Harry, D.E., Ma, C., Yuceer, C., Hsu, C.-Y., Vikram, V., Shevchenko, O., Etherington, E. and Strauss, S.H. (2010) Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J. Expt. Botany, 61, 2549-2560.