In Vitro Cellular & Developmental Biology - Plant

, Volume 42, Issue 6, pp 482–490 | Cite as

Invited review: Transformation of strawberry: The basis for translational genomics in Rosaceae

  • Kevin M. Folta
  • Amit Dhingra


Translational genomics is defined as the application of molecular-genetic principles derived from model systems to species of experimental or economic interest. The past 20 years of research in plant model systems such as Arabidopsis thaliana have relinquished vast amounts of information regarding gene function, the integration of genetic components into pathways, and the interrelationships between pathways to control form and function in plants and plant-products alike. At present, the challenge is to relate these paradigms to other species of economic or scientific interest. Apart from being an important and valuable crop, strawberry (Fragaria spp.) is a member of the Rosaceae, a plant family containing fruit, nut, ornamental and wood-bearing species. Strawberry is unique within the Rosaceae in that it is a rapidly growing herbaceous perennial with a small genome and the ability to thrive in a laboratory setting. Strawberry species may also be transformed and regenerated in a time scale of weeks or months instead of years. For these reasons, strawberry has been recognized as the translational genomics model for the Rosaceae family. This review summarizes and synthesizes the technical reports of strawberry regeneration and transformation, consolidating the large body of information regarding genetic modification of this important genus.

Key words

Fragaria Rosaceae strawberry transformation/regeneration transgenic translational genomics 


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  1. Akiyama, Y.; Yamamoto, Y.; Ohmido, N.; Oshima, M.; Fukui, K. Estimation of the nuclear DNA content of strawberries (Fragaria spp.) compared with Arabidopsis thaliana by using dual-stem flow cytometry. Cytologia 66:431–436; 2001.Google Scholar
  2. Alsheikh, M. K.; Suso, H. P.; Robson, M.; Battey, N. H.; Wetten, A. Appropriate choice of antibiotic and Agrobacterium strain improves transformation of antibiotic-sensitive Fragaria vesca and F.v. semperflorens. Plant Cell Rep. 20:1173–1180; 2002.CrossRefGoogle Scholar
  3. Barcelo, M.; El-Mansouri, I.; Mercado, J. A.; Quesada, M. A.; Alfaro, F. P. Regeneration and transformation via Agrobacterium tumefaciens of the strawberry cultivar Chandler. Plant Cell Tiss. Organ Cult. 54:29–36; 1998.CrossRefGoogle Scholar
  4. Chalavi, V.; Tabaeizadeh, Z.; Thibodeau, P. Enhanced resistance to Verticillium dahliae in transgenic strawberry plants expressing a Lycopersicon chilense chitinase gene. J. Am. Soc. Hort. Sci. 128:747–753; 2003.Google Scholar
  5. Dale, E. C.; Ow, D. W. Gene-transfer with subsequent removal of the selection gene from the host genome. Proc. Natl. Acad. Sci. USA 88:10558–10562; 1991.PubMedCrossRefGoogle Scholar
  6. Davis, T. M.; Yu, H. A linkage map of the diploid strawberry, Fragaria vesca. J. Heredity 88:215–221; 1997.Google Scholar
  7. Debnath, S. C. Strawberry sepal: another explant for thidiazuron-induced advantitious shoot regeneration. In Vitro Cell. Dev. Biol.—Plant 41:671–676; 2005.CrossRefGoogle Scholar
  8. de Mesa, M. C.; Jimenez-Bermudez, S.; Pliego-Alfaro, F.; Quesada, M. A.; Mercado, J. A. Agrobacterium cells as microprojectile coating: a novel approach to enhance stable transformation rates in strawberry. Aust. J. Plant Physiol. 27:1093–1100; 2000.Google Scholar
  9. Dirlewanger, E.; Graziano, E.; Joobeur, T.; Garriga-Caldere, F.; Cosson, P.; Howad, W.; Arus, P. Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc. Natl Acad. Sci. USA 101:9891–9896; 2004.PubMedCrossRefGoogle Scholar
  10. ElMansouri, I.; Mercado, J. A.; Valpuesta, V.; LopezAranda, J. M.; PliegoAlfaro, F.; Quesada, M. A. Shoot regeneration and Agrobacterium-mediated transformation of Fragaria vesca L. Plant Cell Rep. 15:642–646; 1996.CrossRefGoogle Scholar
  11. Folta, K. M.; Davis, T. M. Strawberry genes and genomics. Crit. Rev. Plant Sci. 25:1–17; 2006.CrossRefGoogle Scholar
  12. Folta, K. M.; Dhingra, A.; Howard, L.; Stewart, P.; Chandler, C. K. Characterization of LF9, an octoploid strawberry genotype selected for rapid regeneration and transformation. Planta (in press); 2006.Google Scholar
  13. Foucault, C.; Letouze, R. In vitro: regeneration de plantes de Fraisier a partir de fragmentes de petiole et de bourgeons floraux. Biol. Plant. 29:409–414; 1987.Google Scholar
  14. Graham, J.; McNicol, R. J.; Greig, K. Towards genetic based insect resistance in strawberry using the Cowpea trypsin inhibitor gene. Ann. Appl. Biol. 127:163–173; 1995.CrossRefGoogle Scholar
  15. Graham, J.; McNicol, R. J.; Kumar, A. Use of the gus gene as a selectable marker for Agrobacterium-mediated transformation of Rubus. Plant Cell Tiss. Organ Cult. 20:35–39; 1990.CrossRefGoogle Scholar
  16. Gruchala, A.; Korbin, M.; Zurawicz, E. Conditions of transformation and regeneration of ‘Induka’ and ‘Elista’ strawberry plants. Plant Cell Tiss. Organ Cult. 79:153–160; 2004.CrossRefGoogle Scholar
  17. Hancock, J. F. Strawberries. New York, NY: CABI Publishing; 1999.Google Scholar
  18. Haymes, K. M.; Davis, T. M. Agrobacterium-mediated transformation of ‘Alpine’ Fragaria vesca, and transmission of transgenes to R1 progeny. Plant Cell Rep. 17:279–283; 1998.CrossRefGoogle Scholar
  19. Hokanson, S. C.; Maas, J. L. Strawberry biotechnology. In: Plant breeding reviews. New York: John Wiley and Sons, Inc. 2001:139–180.Google Scholar
  20. Houde, M.; Dallaire, S.; N’Dong, D.; Sarhan, F. Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol. J. 2:381–387; 2004.PubMedCrossRefGoogle Scholar
  21. Huetteman, C. A.; Preece, J. E. Thidiazuron— a potent cytokinin for woody plant-tissue culture. Plant Cell Tiss. Organ Cult. 33:105–119; 1993.CrossRefGoogle Scholar
  22. James, D. J.; Passey, A. J.; Barbara, D. J. Agrobacterium-mediated transformation of the cultivated strawberry (Fragaria × anannassa Duch) using disarmed binary vectors. Plant Sci. 69:79–94; 1990.CrossRefGoogle Scholar
  23. Jemmali, A.; Boxus, P.; Dekegel, D.; Vanheule, G. Occurrence of spontaneous shoot regeneration on leaf stipules in relation to hyperflowering response in micropropagated strawberry plantlets. In Vitro Cell. Dev. Biol.— Plant 30P:192–195; 1994.Google Scholar
  24. Jiménez-Bermúdez, S.; Redondo-Nevado, J.; Muñoz-Blanco, J.; Caballero, J. L.; Lopez-Aranda, J. M.; Valpuesta, V.; Pliego-Alfaro, F.; Quesada, M. A.; Mercado, J. A. Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiol. 128:551–759; 2002.CrossRefGoogle Scholar
  25. Landi, L.; Mezzetti, B. TDZ, auxin and genotype effects on leaf organogenesis in Fragaria. Plant Cell Rep. 25:281–288; 2006.PubMedCrossRefGoogle Scholar
  26. Liu, Z. R.; Sanford, J. C. Plant-regeneration by organogenesis from strawberry leaf and runner tissue. HortScience 23:1057–1059; 1988.Google Scholar
  27. Lunkenbein, S.; Coiner, H.; de Vos, C. H. R.; Schaart, J. G.; Boone, M. J.; Krens, F. A.; Schwab, W.; Salentijn, E. M. J. Molecular characterization of a stable antisense chalcone synthase phenotype in strawberry (Fragaria × ananassa). J. Agric. Food Chem. 54:2145–2153; 2006.PubMedCrossRefGoogle Scholar
  28. Makvandi-Nejad, S.; McLean, M. D.; Hirama, T.; Almquist, K. C.; MacKenzie, C. R.; Hall, J. C. Transgenic tobacco plants expressing a dimeric single-chain variable fragment (scFv) antibody against Salmonella enterica serotype paratyphi B. Transgenic Res. 14:785–792; 2005.PubMedCrossRefGoogle Scholar
  29. Marcotrigiano, M.; McGlew, S. P.; Hackett, G.; Chawla, B. Shoot regeneration from tissue-cultured leaves of the American cranberry (Vaccinium macrocarpon). Plant Cell Tiss. Organ Cult. 44:195–199; 1996.CrossRefGoogle Scholar
  30. Mathews, H.; Dewey, V.; Wagoner, W.; Bestwick, R. K. Molecular and cellular evidence of chimaeric tissues in primary transgenics and elimination of chimaerism through improved selection protocols. Transgenic Res. 7:123–129; 1998.CrossRefGoogle Scholar
  31. Mathews, H.; Wagoner, W.; Kellogg, J.; Bestwick, R. Genetic-transformation of strawberry—stable integration of a gene to control biosynthesis of ethylene. In Vitro Cell. Dev. Biol.—Plant 31:36–43; 1995.CrossRefGoogle Scholar
  32. Mok, M. C.; Mok, D. W. S.; Armstrong, D. J.; Shudo, K.; Isogai, Y.; Okamoto, T. Cytokinin activity of N-phenyl-N′-1,2,3-thiadiazol-5-urea (thidiazuron). Phytochemistry 21:1509–1511; 1982.CrossRefGoogle Scholar
  33. Monet, R.; Guye, A.; Roy, M.; Dachary, N. Peach Mendelian genetics: a short review and new results. Agronomie 16:321–329; 1996.Google Scholar
  34. Mullen, C. A.; Kilstrup, M.; Blaese, R. M. Transfer of the bacterial gene for cytosine deaminase to mammalian-cells confers lethal sensitivity to 5-fluorocytosine—a negative selection system. Proc. Natl Acad. Sci. USA 89(1):33–37; 2002.CrossRefGoogle Scholar
  35. Murashige, T.; Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15:473–497; 1962.CrossRefGoogle Scholar
  36. Murthy, B. N. S.; Singh, R. P.; Saxena, P. K. Induction of high-frequency somatic embryogenesis in geranium (Pelargonium × hortorum Bailey cv. Ringo Rose) cotyledonary cultures. Plant Cell Rep. 15:423–426; 1996.CrossRefGoogle Scholar
  37. Nehra, N. S.; Chibbar, R. N.; Kartha, K. K.; Datla, R. S. S.; Crosby, W. L.; Stushnoff, C. Agrobacterium-mediated transformation of strawberry calli and recovery of transgenic plants. Plant Cell Rep. 9:10–13; 1990a.Google Scholar
  38. Nehra, N. S.; Chibbar, R. N.; Kartha, K. K.; Datla, R. S. S.; Crosby, W. L.; Stushnoff, C. Genetic-transformation of strawberry by Agrobacterium tumefaciens using a leaf disk regeneration system. Plant Cell Rep. 9:293–298; 1990b.Google Scholar
  39. Nehra, N. S.; Stushnoff, C.; Kartha, K. K. Direct shoot regeneration from strawberry leaf-disks. J. Am. Soc. Hort. Sci. 114:1014–1018; 1989.Google Scholar
  40. Nyman, M.; Wallin, A. Plant-regeneration from strawberry (Fragaria × ananassa) mesophyll protoplasts. J. Plant Physiol. 133:375–377; 1988.Google Scholar
  41. Nyman, M.; Wallin, A. Transient gene expression in strawberry (Fragaria × ananassa Duch) protoplasts and the recovery of transgenic plants. Plant Cell Rep. 11:105–108; 1992.CrossRefGoogle Scholar
  42. Oosumi, T.; Gruszewski, H. A.; Blischak, L. A.; Baxter, A. J.; Wadl, P. A.; Shuman, J. L.; Veilleux, R. E.; Shulaev, V. High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta 223:1219–1230; 2006.PubMedCrossRefGoogle Scholar
  43. Owen, H. R.; Miller, A. R. Haploid plant regeneration from anther cultures of three North American cultivars of strawberry (Fragaria × ananassa Duch). Plant Cell Rep. 15:905–909; 1996.CrossRefGoogle Scholar
  44. Owens, C. L.; Thomashow, M. F.; Hancock, J. F.; Iezzoni, A. F. CBF1 orthologs in sour cherry and strawberry and the heterologous expression of CBF1 in strawberry. J. Am. Soc. Hort. Sci. 127:489–494; 2002.Google Scholar
  45. Passey, A. J.; Barrett, K. J.; James, D. J. Adventitious shoot regeneration from seven commercial strawberry cultivars (Fragaria × ananassa Duch.) using a range of explant types. Plant Cell Rep. 21:397–401; 2003.PubMedGoogle Scholar
  46. Poirier, Y.; Ventre, G.; Nawrath, C. High-frequency linkage of co-expressing T-DNA in transgenic Arabidopsis thaliana transformed by vacuum-infiltration of Agrobacterium tumefaciens. Theor. Appl. Genet. 100:487–493; 2000.CrossRefGoogle Scholar
  47. Puchta, H. Marker-free transgenic plants. Plant Cell Tiss. Organ Cult. 74:123–134; 2003.CrossRefGoogle Scholar
  48. Qin, Y. H.; Zhang, S. L.; Asghar, S.; Zhang, L. X.; Qin, Q. P.; Chen, K. S.; Xu, C. J. Regeneration mechanism of Toyonoka strawberry under different color plastic films. Plant Sci. 168:1425–1431; 2005.CrossRefGoogle Scholar
  49. Ricardo, V. G.; Coll, Y.; Castagnaro, A.; Ricci, J. C. D. Transformation of a strawberry cultivar using a modified regeneration medium. Hortscience 38:277–280; 2003.Google Scholar
  50. Rosin, F. M.; Aharoni, A.; Salentijn, E. M. J.; Schaart, J. G.; Boone, M. J.; Hannapel, D. J. Expression patterns of a putative homolog of AGAMOUS, STAG1, from strawberry. Plant Sci. 165:959–968; 2003.CrossRefGoogle Scholar
  51. Rugini, E.; Orlando, R. High-efficiency shoot regeneration from calluses of strawberry (Fragaria × ananassa-Duch) stipules of In-vitro shoot cultures. J. Hort. Sci. 67:577–582; 1992.Google Scholar
  52. Sargent, D. J.; Clarke, J.; Simpson, D. W.; Tobutt, K. R.; Arus, P.; Monfort, A.; Vilanova, S.; Denoyes-Rothan, B.; Rousseau, M.; Folta, K. M.; Bassil, N. V.; Battey, N. H. An enhanced microsatellite map of diploid Fragaria. Theor. Appl. Genet. 112:1349–1359; 2006.PubMedCrossRefGoogle Scholar
  53. Sargent, D. J.; Davis, T. M.; Tobutt, K. R.; Wilkinson, M. J.; Battey, N. H.; Simpson, D. W. A genetic linkage map of microsatellite, gene-specific and morphological markers in diploid Fragaria. Theor. Appl. Genet. 109:1385–1391; 2004.PubMedCrossRefGoogle Scholar
  54. Schaart, J. G.; Krens, F. A.; Pelgrom, K. T. B.; Mendes, O.; Rouwendal, G. J. A. Effective production of marker-free transgenic strawberry plants using inducible site-specific recombination and a bifunctional selectable marker gene. Plant Biotech. J. 2:233–240; 2004.CrossRefGoogle Scholar
  55. Schaart, J. G.; Salentijn, E. M. J.; Krens, F. A. Tissue-specific expression of the beta-glucuronidase reporter gene in transgenic strawberry (Fragaria × ananassa) plants. Plant Cell Rep. 21:313–319; 2002.CrossRefGoogle Scholar
  56. Sorvari, S.; Ulvinen, S.; Hietaranta, T.; Hiirsalmi, H. Preculture medium promotes direct shoot regeneration from micropropagated strawberry leaf disks. HortScience 28:55–57; 1993.Google Scholar
  57. Stacey, G.; VandenBosch, K. ‘Translational’ legume biology. Models to crops. Plant Physiol. 137:1173; 2005.PubMedCrossRefGoogle Scholar
  58. Staudt, G. The species of Fragaria, their taxonomy and geographic distribution. Acta Hort. 265:23–33; 1989.Google Scholar
  59. Vellicce, G. R.; Ricci, J. C. D.; Hernandez, L.; Castagnaro, A. P. Enhanced resistance to Botrytis cinerea mediated by the transgenic expression of the chitinase gene ch5B in strawberry. Transgenic Res. 15:57–68; 2006.PubMedCrossRefGoogle Scholar
  60. Visser, C.; Qureshi, J. A.; Gill, R.; Saxena, P. K. Morphoregulatory role of thidiazuron—substitution of auxin and cytokinin requirement for the induction of somatic embryogenesis in geranium hypocotyl cultures. Plant Physiol. 99:1704–1707; 1992.PubMedCrossRefGoogle Scholar
  61. Wang, J. L.; Ge, H. B.; Peng, S. Q.; Zhang, H. M.; Chen, P. L.; Xu, J. R. Transformation of strawberry (Fragaria ananassa Duch.) with late embryogenesis abundant protein gene. J. Hort. Sci. Biotechnol. 79:735–738; 2004.Google Scholar
  62. Zhao, Y.; Liu, Q. Z.; Davis, R. E. Transgene expression in strawberries driven by a heterologous phloem-specific promoter. Plant Cell Rep. 23:224–230; 2004.PubMedCrossRefGoogle Scholar
  63. Zhu, H.; Choi, H. K.; Cook, D. R.; Shoemaker, R. C. Bridging model and crop legumes through comparative genomics. Plant Physiol. 137:1189–1196; 2005.PubMedCrossRefGoogle Scholar

Copyright information

© Society for In Vitro Biology 2006

Authors and Affiliations

  1. 1.Horticultural Sciences Department and the Plant Molecular and Cellular Biology ProgramUniversity of FloridaGainesville

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