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

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Summary

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.

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References

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Davis, T. M.; Yu, H. A linkage map of the diploid strawberry, Fragaria vesca. J. Heredity 88:215–221; 1997.

    CAS  Google Scholar 

  • Debnath, S. C. Strawberry sepal: another explant for thidiazuron-induced advantitious shoot regeneration. In Vitro Cell. Dev. Biol.—Plant 41:671–676; 2005.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Folta, K. M.; Davis, T. M. Strawberry genes and genomics. Crit. Rev. Plant Sci. 25:1–17; 2006.

    Article  CAS  Google Scholar 

  • 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.

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hancock, J. F. Strawberries. New York, NY: CABI Publishing; 1999.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hokanson, S. C.; Maas, J. L. Strawberry biotechnology. In: Plant breeding reviews. New York: John Wiley and Sons, Inc. 2001:139–180.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Huetteman, C. A.; Preece, J. E. Thidiazuron— a potent cytokinin for woody plant-tissue culture. Plant Cell Tiss. Organ Cult. 33:105–119; 1993.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Landi, L.; Mezzetti, B. TDZ, auxin and genotype effects on leaf organogenesis in Fragaria. Plant Cell Rep. 25:281–288; 2006.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Z. R.; Sanford, J. C. Plant-regeneration by organogenesis from strawberry leaf and runner tissue. HortScience 23:1057–1059; 1988.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Monet, R.; Guye, A.; Roy, M.; Dachary, N. Peach Mendelian genetics: a short review and new results. Agronomie 16:321–329; 1996.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Murashige, T.; Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15:473–497; 1962.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • Nyman, M.; Wallin, A. Plant-regeneration from strawberry (Fragaria × ananassa) mesophyll protoplasts. J. Plant Physiol. 133:375–377; 1988.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Puchta, H. Marker-free transgenic plants. Plant Cell Tiss. Organ Cult. 74:123–134; 2003.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Stacey, G.; VandenBosch, K. ‘Translational’ legume biology. Models to crops. Plant Physiol. 137:1173; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Staudt, G. The species of Fragaria, their taxonomy and geographic distribution. Acta Hort. 265:23–33; 1989.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

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  1. Horticultural Sciences Department and the Plant Molecular and Cellular Biology Program, University of Florida, 1301 Fifield Hall, 32611, Gainesville, FL

    Kevin M. Folta & Amit Dhingra

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  1. Kevin M. Folta
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Correspondence to Kevin M. Folta.

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Folta, K.M., Dhingra, A. Invited review: Transformation of strawberry: The basis for translational genomics in Rosaceae . In Vitro Cell.Dev.Biol.-Plant 42, 482–490 (2006). https://doi.org/10.1079/IVP2006807

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