GMO Strawberry: Methods, Risk and Benefits

  • Bruno Mezzetti
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 6)

The potential for profitable applications of biotechnology to many fruits and vegetables, tree fruits and nuts, can be limited by the high cost of research, development and regulatory approval combined with the small plantations and the diversity of varieties. Further, experimentation with perennials such as fruit trees, berry and nuts and is comparatively expensive (because the experimental unit is larger and takes more time), and it is costly and not easy to bring into new plantations or replacing and existing orchards with a new variety. For these reasons biotech application in horticultural crops are quite limited at research level and commercialization is almost completely absent. Horticultural crops use much less land but their production is of much higher value. Upon this situation, the development of biotechnology applications in horticultural crops and the achievement of market acceptance can be expected, in the near future, mainly for those crops with a broader importance in cultivation and market.


Strawberry Fruit Strawberry Plant Expansin Gene rolC Gene Strawberry Cultivar 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Agius F, Gonzalez-Lamothe R, Caballero JL, Munoz-Blanco J, Botella MA, and Valpuesta V (2003) Engineering increased vitamin C levels in plants by over-expression of a D- galacturonic acid reductase. Nat Biotechnol 21: 177–81.CrossRefPubMedGoogle Scholar
  2. Ahroni A, van Tunen AJ, Rosin FM, and Hannapel DJ (1999) Isolation of an AGAMOUS cDNA (STAG1) from Strawberry (Fragaria x ananassa cv. Elsanta) (Accession No. AF168468). (PGR99-153) Plant Physiol 121: 686.Google Scholar
  3. Aharoni A, Keizer LCP, Bouwmeester HJ, Sun-Zhong K, Alvarez-Huerta M, Verhoeven HA, Blaas J, Houwelingen AMML van, Vos-RCH de, Voet H van-der, Jansen RC, Guis M, Mol J, Davis RW, Schena-M, Tunen AJ van, O’-Connell AP, and van-der-Voet-H (2000) Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12(5): 647–661.CrossRefPubMedGoogle Scholar
  4. Almeida JRM, D’Amico E, Preuss A, Carbone F, Ric de Vos CH, and Deiml B (2007) Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria×ananassa). Arch Biochem Biophys 465: 61–71.CrossRefPubMedGoogle Scholar
  5. Alsheikh MK, Suso HP, Robson M, Battey NH, and Wetten A (2002) Appropriate choice of antibiotic and Agrobacterium strain improves transformation of antibiotic-sensitive Fragaria vesca and F.v. sepmerflorens. Plant Cell Rep 20:1173–1180.CrossRefGoogle Scholar
  6. Asao HG, Nishizawa Y, Arai S, Sato T, Hirai M, and Yoshida K (1997) Enhanced resistance against a fungal pathogen Sphaerotheca fumuli in transgenic strawberry expressing a rice chitinase gene. Plant Biotechnol 14:145–149.Google Scholar
  7. Asao HG, Arai S, and Nishizawa Y (2003) Environmental risk evaluation of transgenic strawberry expressing a rice chitinase gene. Seibutsu Kogakkaishi 81:57–63 (in Japanese with English Abstract).Google Scholar
  8. Bachelier C, Graham J, Machray G, Manoir J du, Roucou JF, McNicol RJ, Davies H, Du-Manoir J, Scheer HAT. vander, Lieten F, and Dijkstra J (Ed.) (1997) Integration of an invertase gene to control sucrose metabolism in strawberry cultivars. Proceedings of the third international strawberry symposium, Veldhoven, Netherlands, 29 April-4 May 1996. Volume I. Acta Horticulturae 439: 161–163.Google Scholar
  9. Balokhina NV, Kaliayeva MA, and Buryanov Ya I (2000) The elaboration of a shoot regeneration system for the genetic transformation of the wild strawberry (Fragaria vesca L.). Biotekhnologiya 16: 46–51.Google Scholar
  10. Barcélo M, El Mansouri I, Mercado JA, Quesada MA, and Alfaro FP (1998) Regeneration and transformation via Agrobacterium tumefaciens of the strawberry cultivar Chandler. Plant Cell Tiss Org Cult 54: 29–36.CrossRefGoogle Scholar
  11. Bhagwat B, and Lane WD (2004) In vitro shoot regenerations from leaves of sweet cherry (Prunus avium) ‘Lapins’ and ‘Sweetheart’. Plant Cell Tiss Org Cult 78: 173–181.CrossRefGoogle Scholar
  12. Bingham ET (1989) Registration of regen-S Alfa germplasm useful in tissue culture and transformation research. Crop Sci 29:1095–1096.CrossRefGoogle Scholar
  13. Casanova E, Trillas MI, Moysset L, and Vainstein A (2005) Influence of rol genes in floriculture. Biotechnol Adv 23(1):3–39.CrossRefPubMedGoogle Scholar
  14. Chalavi V, Tabaeizadeh Z, and Thibodeau P (2003) Enhanced resistance to Verticillium dahliae in transgenic strawberry plants expressing a Lycopersicon chilense chitinase gene. J Am Soc Hortic Sci 128:747–753.Google Scholar
  15. Civello PM, Powell ALT, Sabehat A, and Bennett AB (1999) An expansin gene expressed in ripening strawberry fruit. Plant Physiol 121(4): 1273–1279.CrossRefPubMedGoogle Scholar
  16. Davis TM, and Yu H (1997) A linkage map of the diploid strawberry, Fragaria vesca. J Hered 88:215–221.Google Scholar
  17. Davuluri GR, Van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Bramely PM, Pennings HJ, and Bowler C (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoids content in tomatoes. Nat Biotechnol 23: 890–895.CrossRefPubMedGoogle Scholar
  18. El Mansouri L, Mercadi JA, Valpuesta V, Lopez-Aranda JM, Pliegi-Alfaro F, and Quesada MA (1996) Shoot regeneration and Agrobacterium-mediated trasformation of Fragaria vesca L. Plant Cell Rep. 15: 642–646.CrossRefGoogle Scholar
  19. Finstad K, Martin RR, Ramsdell DC, and Barba M (1995) Transformation of strawberry for virus resistance. VII th International symposium on small fruit virus diseases. Acta Hort No. 385: 86–90.Google Scholar
  20. Folta KM, Dhingra A, Howard L, Stewart PJ, and Chandler CK (2006) Characterization of LF9 an octoploid strawberry genotype selected for rapid regeneration and transformation. Planta 224:1058–1067.CrossRefPubMedGoogle Scholar
  21. Foucault C, and Letouze R (1987) In vitro: regeneration des plant de Fraisier a partir de fragmentes de petiole et de bourgeons floraux. Biol. Plantarum 29: 409–414.CrossRefGoogle Scholar
  22. Gardner N, Melberg T, George M, and Smith AG (2006) Differential expression of rolC results in unique plant phenotypes. J Am Soc Horticult Sci 131(1): 82–88.Google Scholar
  23. Gilberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, and Giuliano G (2005) Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol 137:199–208.CrossRefGoogle Scholar
  24. Graham J, McNicol RJ, and Greig K (1995) Transgenic apples and strawberries: advances in transformation, introduction of genes for insect resistance and field studies of tissue cultured plants. Ann Appl Biol 127: 163–173.CrossRefGoogle Scholar
  25. Graham J, Gordon SC, and McNicol RJ (1997a) The effect of the CpTi gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae). Ann Appl Biol 131(1): 133–139.Google Scholar
  26. Graham J, Machray G, Manoir J du, Roucou JF, McNicol RJ, Davies H, and Du Manoir J (1997b) Integration of an invertase gene to control sucrose metabolism in strawberry cultivars. Acta Hort 439: 161–163.Google Scholar
  27. Griesser M, Hoffmann T, Bellido ML, Rosati C, Fink B, Kurtzer R, Aharoni A, Muñoz-Blanco J, Schwab W (2008) Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit. Plant Physiol 146(4):1528–1539.CrossRefPubMedGoogle Scholar
  28. Gruchala A, Korbin M, and Zurawicz E (2004) Conditions of transformation and regeneration of Iduka and Elista strawberry plants. Plant Cell Tiss Organ Cult 79: 153–160.CrossRefGoogle Scholar
  29. Haymes KM, and Davis TM (1997) Agrobacterium – mediated transformation of ‘Alpine’ Fragaria vesca and transmission of transgenes to R1 progeny. Plant Cell Rep. 17: 279–283CrossRefGoogle Scholar
  30. Huetteman CA, and Preece JE (1993) Thidiazuron: a potent cytokinin for woody plant tissue culture. Plant Cell Tiss Org Cult 33: 105–119.CrossRefGoogle Scholar
  31. James DJ (1987) Cell and tissue culture technology for the genetic manipulation of temperate fruit trees. In: Biotechnol Genet Eng Rev. 5: 33–79. G.E. Russell (Ed.) Intercept, Newcastle-upon TyneGoogle Scholar
  32. James DJ, Passey AJ, and Barbara DJ (1990) Agrobacterium-mediated transformation of the cultivated strawberry (Fragaria x ananassa Duch.) using disarmed binary vectors. Plant Sci 69: 79–94.CrossRefGoogle Scholar
  33. Jimenez-Bermudez S, Redondo-Nevado J, Munoz-Blanco J, Caballero JL, Lopez-Aranda JM, Valpuesta V, Pliego-Alfaro F, Quesada MA, and Mercado JA (2002) Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiol 128: 751–759.CrossRefPubMedGoogle Scholar
  34. Kempin SA, Mandel MA, and Yanofsky MF (1993) Conversion of perianth into reproductive organs by ectopic expression oh the tobacco floral homeotic gene NAG1. Plant Physiol, 103:4 1041–1046.CrossRefPubMedGoogle Scholar
  35. Kumar S, Sharma P, and Pental D (1998) A Gentic approach to in vitro regeneration of non-regenerating cotton (Gossypium hirsutum L.) cultivars. Plant Cell Rep 15:59–63.CrossRefGoogle Scholar
  36. Lamproye A, Hofinger M, Berthon JY, and Gaspar T (1990) 3-(Benzo(b)selenienyl)acetic acid, a potent synthetic auxin in somatic embryogenesis. Comptes rendus Acad Sci Paris 311 (série III): 127–132.Google Scholar
  37. Landi L, and Mezzetti B (2006) TDZ, auxin and genotype effects on leaf organogenesis in Fragaria. Plant Cell Rep 25(4):281–8.CrossRefPubMedGoogle Scholar
  38. Liu ZR, and Sanford JC (1988) Plant regeneration by organogenesis from strawberry leaf and runner tissue. HortScience 23: 1057–1059.Google Scholar
  39. Llop-Tous I, Dominguez-Puigjaner E, Palomer X, and Vendrell M (1999) Characterization of two divergent endo-beta-1,4-glucanase cDNA clones highly expressed in the nonclimacteric strawberry fruit. Plant Physiol 119:(4): 1415–1421.CrossRefPubMedGoogle Scholar
  40. Manning K (1994) Changes in gene expression during strawberry fruit ripening and their regulation by auxin. Planta 194:(1): 62–68.CrossRefGoogle Scholar
  41. Mathews H, Wagoner W, Kellog J, and Bestwick R (1995). Genetic transformation of strawberry: stable integration of a gene to control biosynthesis of ethylene. In Vitro Cell Dev Biol Plant 31:36–43.CrossRefGoogle Scholar
  42. Mazzara M, Mezzetti B, James JD, and Negri P (1998) Il gene rolC in fragola. L’informatore Agrario 29:46–49.Google Scholar
  43. Meng RG, Chen THN, Finn CE, and Li YH (2004) Improving in vitro plant regeneration from leaf and petiole explants of ‘Marion’ blackberry. Hort Science 39: 316–320.Google Scholar
  44. Mezzetti B (2003) Genetic transformation in strawberry and raspberry. In: Plant Genetic Engineering, Vol. 6 Improvement of Fruit Crops. Eds. Pawan K Jaiwal and Rana P Singh. SCI Tech Publishing LLC, Houston, TXGoogle Scholar
  45. Mezzetti B, Costantini E, Cionchetti F, Landi L, Pandolfini T, and Spena A (2004a) Genetic transformation in strawberry and raspberry for improving plant productivity and fruit quality. Euroberry Symposium, Acta Hort (ISHS) 649:107–110.
  46. Mezzetti B, Landi L, Pandolfini T, and Spena A (2004b) The defH9-iaaM auxin-synthesizing gene increases plant fecundity and fruit production in strawberry and raspberry. BMC Biotechnol 4:4–6750/4/4.Google Scholar
  47. Mihály K, Ingrid MM, and Bánfalvi Z (2006) Generation of marker- and backbone-free transgenic potatoes by site-specific recombination and a bi-functional marker gene in a non-regular one-border Agrobacterium transformation vector. Transgenic Res 15:729–737.CrossRefGoogle Scholar
  48. Mitiouchkina TY, and Dolgov SV (2000) Modification of chrysanthemum plant and flower architecture by rolC gene from Agrobacterium rhizogenes introduction. Acta Hort 508: 163–169.Google Scholar
  49. Mizukami Y, and Ma H (1995) Separation of Ag function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA. Plant Mol Biol 28(5): 767–784;CrossRefPubMedGoogle Scholar
  50. Murashige T, and Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497.CrossRefGoogle Scholar
  51. Nam YW, Tichit L, Leperlier M, Cuerq B, Marty I, and Lelievre JM (1999) Isolation and characterization of mRNAs differentially expressed during ripening of wild strawberry (Fragaria vesca L.) fruits. Plant Mol Biol 39: 629–636.CrossRefPubMedGoogle Scholar
  52. Nehra NS, Stushnoff C, and Kartha KK (1989) Direct shoot regeneration from leaf discs. J Am Soc Horti Sci 114:1014–1018.Google Scholar
  53. Nehra NS, Chibbar RN, Kartha KK, Datla RSS, Crosby WL, and Stushnoff C (1990) Genetic transformation of strawberry by Agrobacterium tumefaciens using a leaf disk regeneration system. Plant Cell Rep 9: 293–298.Google Scholar
  54. Nilsson O, Moritz T, Sundberg B, Sandberg G, and Olsson O (1996) Expression of the Agrobacterium rhizogenes rolC gene in a deciduous forest tree alters growth and development and leads to stem fasciation. Plant Physiol 112(2):493–502.PubMedGoogle Scholar
  55. Oosumi T, Gruszewski HA, Blischak LA, Baxter AJ, Wadl PA, Shuman JL, Veilleux RE, and Shulaev V (2006) High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta 223(6):1219–30.CrossRefPubMedGoogle Scholar
  56. Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, and Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487.CrossRefPubMedGoogle Scholar
  57. Palomer X, Llop-Tous I, Vendrell M, Krens FA, Schaart JG, and Boone MJ (2006) Antisense down-regulation of strawberry endo-β-(1,4)-glucanase genes does not prevent fruit softening during ripening. Plant Sci 171: 640–646.CrossRefGoogle Scholar
  58. Park JI, Lee YK, Chung WI, Lee IH, Choi JH, and Lee WM (2006) Modification of sugar composition in strawberry fruit by antisense suppression of an ADP-glucose pyrophosphorylase. Mol Breed 17:269–279.CrossRefGoogle Scholar
  59. Passey AJ, Barrett KJ, and James DJ (2003) Adventitious shoot regeneration from seven commercial strawberry cultivars (Fragaria x ananassa Duch.) using a range of explant types. Plant Cell Rep 21: 397–401.PubMedGoogle Scholar
  60. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, and Lifschitz E (1994) Isolation of the tomato AGAMOUS gene TAg1 and analysis of its homeotic role in transgenic plants. Plant Cell 6(2): 163–173.CrossRefPubMedGoogle Scholar
  61. Ricardo VG, Coll Y, Castagnaro A, and Ricci JCD (2003) Transformation of a strawberry cultivars using a modified regeneration medium. Hort Science 38:277–280.Google Scholar
  62. Ricardo VG, Ricci JCD, Hernández L, and Castagnaro AP (2006) Enhanced resistance to Botrytis cinerea mediated by the transgenic expression of the chitinase gene ch5B in strawberry. Transgenic Res 15:57–68.CrossRefGoogle Scholar
  63. Rotino GL, Perri E, Zottini M, Sommer H, and Spena A (1997). Genetic engineering of parhenocarpic plants. Nat Biotechnol 15: 1398–1320.CrossRefPubMedGoogle Scholar
  64. Rugini E, and Orlando R (1992) High efficiency shoot regeneration from calluses of strawberry (Fragaria x ananassa Duch.) stipules of in vitro shoot cultures. J Hortic Sci 67: 577–582.Google Scholar
  65. Sargent DJ, Clarke J, Simpson DW, Tobutt KR, Arús P, Monfort A, Vilanova S, Denoyes-Rothan B, Rousseau M, Folta KM, Bassil NV, and Battey NH (2006) An enhanced microsatellite map of diploid Fragaria. Theor Appl Genet 112(7):1349–59.CrossRefPubMedGoogle Scholar
  66. Sargent DJ, Rys A, Nier S, Simpson DW, and Tobutt KR (2007) The development and mapping of functional markers in Fragaria and their transferability and potential for mapping in other genera. Theor Appl Genet 114(2):373–384.CrossRefPubMedGoogle Scholar
  67. Scalzo J, Battino M, Costantini E, and Mezzetti B (2005) Breeding and biotechnology for improving berry nutritional quality. Biofactors 23(4):213–20.CrossRefPubMedGoogle Scholar
  68. Schaart JG, Krens FA, Pelgrom KTB, Mendes O, and Rouwendal GJA (2004) Effective production of marker-free transgenic strawberry plants using inducible site-specific recombination and a bifunctional selectable marker gene. Plant Biotechnol J 2:233–240.CrossRefPubMedGoogle Scholar
  69. Schmulling T, Schell J, and Spena A (1988) Single genes from Agrobacterium rhizogenes influence plant development. EMBO J 7: 2621–2629.PubMedGoogle Scholar
  70. Schwarz-Sommer Z, Saedler H, Sommer H, Russo VEA, Brody S, Cove D, and Ottolenghi S (Ed) (1992) Homeotic genes in the genetic control of flower morphogenesis in Antirrhinum majus. Development: the molecular genetic approach. Springer Verlagm, Heidelberg, pp. 242–256.Google Scholar
  71. Sesmero R, Quesada MA, and Mercado JA (2007) Antisense inhibition of pectate lyase gene expression in strawberry fruit: characteristics of fruits processed into jam. J Food Eng 79: 194–199.CrossRefGoogle Scholar
  72. Simpson DW, James DJ, Passey AJ, Massiah A, and Sargent DJ (1999) Genetic modification of strawberry for enhanced resistance to Botrytis cinerea. Abstract meeting COST836, Integrated Research in Berries, INRA – Paris.Google Scholar
  73. Sorvari S, Ulvinen S, Hietarante T, and Hiirsalmi H (1993) Pre-culture medium promotes direct shoot regeneration from micropropagated strawberry leaf disks. HortScience 28: 55–57.Google Scholar
  74. Spena A, and Rotino GL (2001) Parthenocarpy: state of the art. In: Current trends in the embryology of Angiosperm. Eds. Bhojwani SS and Soh WY) Kluwers Academic Publishers, Dordrecht, pp. 435–450.Google Scholar
  75. Stougaard J (1993) Substrate-dependent negative selection in plants using a bacterial cytosine deaminase gene. Plant J 3:755–761.CrossRefGoogle Scholar
  76. Trainotti L, Spolaore S, Ravanello A, Baldan B, and Casadoro G (1999) A novel E-type endo-beta-1,4-glucanase with a putative cellulose-binding domain is highly expressed in ripening strawberry fruits. Plant Mol Biol 40(2): 323–332.CrossRefPubMedGoogle Scholar
  77. Uratsu SL, Ahmadu H, Bringust RS, and Dandekar AM, (1991) Relative virulence of Agrobacterium tumefaciens strains on strawberry. HortScience 26: 196–199.Google Scholar
  78. Welander M, and Zhu Li H (2006) Rol genes: molecular biology, physiology, morphology, breeding uses. Plant Bree Rev 26: 79–103.Google Scholar
  79. Wilkinson JQ, Lanahan MB, Conner TW, and Klee HJ (1995) Identification of mRNAs with enhanced expression in ripening strawberry fruit using polymerase chain reaction differential display. Plant Mol Biol 27(6): 1097–1108.CrossRefPubMedGoogle Scholar
  80. Winefield C, Lewis D, Arathoon S, and Deroles S (1999) Alteration of Petunia plant form through the introduction of the rolC gene from Agrobacterium rhizogenes. Mol Breed 5(6): 543–551.CrossRefGoogle Scholar
  81. Woolley LC, James DJ, and Manning K, 2001. Purification and properties of an endo-β-1,4-glucanase from strawberry and down-regulation of the corresponding gene, cel1. Planta 214:11–21.CrossRefPubMedGoogle Scholar
  82. Wurgler FE, Sobels FH, and Vogel E (1984) Drosophila as an assay system for detecting genetic changes. In: Hanbook of Mutagenicity Test Procedures, 2nd edn, Kildey BJ, Legator M, Nichols W, and Ramel C (Eds). Elsevier Science, Amsterdam, pp. 551–602.Google Scholar
  83. Zuker A, Tzfira T, Scovel G, Ovadis M, Shklarman E, Itzhaki H, and Vainstein A (2001) RolC-transgenic carnation with improved horticultural traits: quantitative and qualitative analysis of greenhouse-grown plants. J Am Soc Hort Sci 126:13–18.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Bruno Mezzetti
    • 1
  1. 1.Dipartimento di Scienze Ambientali e delle Produzioni Vegetali – Marche Polytechnic UniversityAnconaItaly

Personalised recommendations