Abstract
Cultivated strawberry (Fragaria × ananassa) and Rubus berries, raspberry and blackberry, are small fruits highly appreciated by consumers and worldwide cultivated. The polyploidy nature of these species, their high heterozygosity, and the lack of natural resistance to several pests are the main constraints to the development of improved genotypes by conventional breeding. In recent years, genetic transformation has demonstrated to be a powerful tool to overcome these limitations. In this chapter, the current state of genetic transformation technology in Fragaria and Rubus spp. is reviewed. The feasibility of strawberry to regenerate in vitro has allowed the development of efficient transformation protocols for both cultivated and the wild strawberry Fragaria vesca. Important traits such as photoperiod requirements for flowering, fungal tolerance, biotic stress tolerance, and fruit shelf life have been manipulated in transgenic strawberry plants through the introduction of different genes. Furthermore, tools for the development of intragenic plants, containing chimeric genes from the own species and devoid of marker genes, have been generated. By contrast, the recalcitrance of Rubus tissues to regenerate in vitro has impeded the development of robust transformation protocols in these species, although a few number of studies have successfully obtained transgenic plants carrying genes of interest. Main achievements, limitations, and future prospects of genetic transformation in both genera are discussed.
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References
Abdal-Aziz SA, Pliego-Alfaro F, Quesada MA, Mercado JA (2006) Evidence of frequent integration of non-T-DNA vector backbone sequences in transgenic strawberry plant. J Biosci Bioeng 101:508–510
Alsheikh MK, Suso H-P, Robson M, Battey NH, Wetten A (2002) Appropriate choice of antibiotic and Agrobacterium strain improves transformation of antibiotic-sensitive Fragaria vesca and F. v. semperflorens. Plant Cell Rep 20:1173–1180
Araki M, Ishii T (2015) Towards social acceptance of plant breeding by genome editing. Trends Plant Sci 20:145–149
Asao H, Nishizawa Y, Arai S, Sato T, Hirai M, Yoshida K, Shinmyo A, Hibi T (1997) Enhanced resistance against a fungal pathogen Sphaerotheca humuli in transgenic strawberry expressing a rice chitinase gene. Plant Biotech 14:145–149
Asao H, Arai S, Nishizawa Y (2003) Environmental risk evaluation of transgenic strawberry expressing a rice chitinase gene. Seibutsu-Kogaku Kaishi 81:57–63
Barceló M, El Mansouri I, Mercado JA, Quesada MA, Pliego-Alfaro F (1998) Regeneration and transformation via Agrobacterium tumefaciens of the strawberry cultivar Chandler. Plant Cell Tissue Organ Cult 54:29–36
Basson CE, Groenewald JH, Kossmann J, Cronjé C, Bauer R (2011) Upregulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in strawberry. Transgenic Res 20:925–931
Beachy RN, Lapidot M, Gafny R (1999) Resistance to virus infection using modified viral movement protein. US Patent 5,898,097, 27 Apr 1999
Birch RG (1997) Plant transformation: problem and strategies for practical application. Annu Rev Plant Physiol Plant Mol Biol 48:297–326
Biswas MK, Islam R, Hossain M (2007) Somatic embryogenesis in strawberry (Fragaria sp.) through callus culture. Plant Cell Tissue Organ Cult 90:49–54
Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340
Casado-Díaz A, Encinas-Villarejo S, de los Santos B, Schiliro E, Yubero-Serrano E-M, Amil-Ruíz F, Pocovi MI, Pliego-Alfaro F, Dorado G, Rey M, Romero F, Muñoz-Blanco J, Caballero JL (2006) Analysis of strawberry genes differentially expressed in response to Colletotrichum infection. Physiol Plant 128:633–650
Chalavi V, Tabaeizadeh Z, 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
Chu C, Wang C, Sun C, Hsu C, Yin K, Chu C, Bi F (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci Sin XVIII 5:659–668
Cockburn A (2002) Assuring the safety of genetically modified (GM) foods: the importance of an holistic, integrative approach. J Biotechnol 98:79–106
Cordero de Mesa M, Jiménez-Bermúdez S, Pliego-Alfaro F, Quesada MA, Mercado JA (2000) Agrobacterium cells as microprojectile coating: a novel approach to enhance stable transformation rates in strawberry. Aust J Plant Physiol 27:1093–1100
Cousineau JC, Donnelly DJ (1991) Adventitious shoot regeneration from leaf explants of tissue cultured and greenhouse-grown raspberry. Plant Cell Tissue Organ Cult 27:249–255
Dale A, Sjulin TM (1990) Few cytoplasms contribute to North American strawberry cultivars. HortScience 25:1341–1342
Dana MM, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142:722–730
De Faria MJSS, Donnelly DJ, Cousineau JC (1997) Adventitious shoot regeneration and Agrobacterium-mediated transformation of red raspberry. Braz Arch Biol Technol 40:518–529
Debnath SC (2005) Strawberry sepal: another explant for thidiazuron-induced adventitious shoot regeneration. In Vitro Cel Dev Biol Plant 41:671–676
Debnath SC (2006) Zeatin overcomes thidiazuron-induced inhibition of shoot elongation and promotes rooting in strawberry culture in vitro. J Hortic Sci Biotech 81:349–354
Debnath SC (2010) A scaled-up system for in vitro multiplication of thidiazuron-induced red raspberry shoots using bioreactor. J Hortic Sci Biotech 85:94–100
Donnoli R, Sunseri F, Martelli G, Greco I (2001) Somatic embryogenesis, plant regeneration and genetic transformation in Fragaria spp. Acta Hortic 560:235–239
du Plessis HJ, Brand RJ, Glyn-Woods C, Goedhart MA (1997) Efficient genetic transformation of strawberry (Fragaria x ananassa Duch.) cultivar Selekta. Acta Hortic 447:289–294
Dziadczyk P, Bolibok H, Tyrka M, Hortyński JA (2003) In vitro selection of strawberry (Fragaria × ananassa Duch.) clones tolerant to salt stress. Euphytica 132:49–55
El Mansouri I, Mercado JA, Valpuesta V, López-Aranda JM, Pliego-Alfaro F, Quesada MA (1996) Shoot regeneration and Agrobacterium-mediated transformation of Fragaria vesca L. Plant Cell Rep 15:642–646
Finstad K, Martin RR (1995) Transformation of strawberry for virus resistance. Acta Hortic 385:86–90
Fiola JA, Hassan MA, Swartz HJ, Bors RH, McNicols R (1990) Effect of thidiazuron, light fluence rates and kanamycin on in vitro shoot organogenesis from excised Rubus cotyledons and leaves. Plant Cell Tissue Organ Cult 20:223–228
Fischer TC, Mirbeth B, Rentsch J, Sutter C, Ring L, Flachowsky H, Habegger R, Hoffman T, Hanke M-V, Schawb W (2014) Premature and ectopic anthocyanin formation by silencing of anthocyanidin reductase in strawberry (Fragaria × ananassa). New Phytol 201:440–451
Folta KM, Dhingra A, Howard L, Stewart PJ, Chandler CK (2006) Characterization of LF9, an octoploid strawberry genotype selected for rapid regeneration and transformation. Planta 224:1058–1067
Gajdošová A, Vujović T, Súkeníková M, Libiaková G (2015) Improvement of adventitious organogenesis for regeneration of transgenic plants in blackberry. Genetika 47:599–608
Garrido C, Carbú M, Fernández-Acero FJ, González-Rodríguez VE, Cantoral JM (2011) New insights in the study of strawberry fungal pathogens. In: Husaini AM, Mercado JA (eds) Genomics, transgenics, molecular breeding and biotechnology of strawberry. Global Science Books, pp 24–39
George EF (1993) Plant propagation by tissue culture. Part 1. The technology. Exegetics Ltd., Edington, England, pp 3–36
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442
Gough B (2008) An encyclopedia of small fruit. CRC Press, Taylor and Francis Group
Graham J (2005) Fragaria strawberry. In: Litz RE (ed) Biotechnology of fruit and nut crops. CABI Publishing, pp 456–474
Graham J, McNicol RJ, Greig K (1995) Towards genetic based insect resistance in strawberry using the Cowpea trypsin inhibitor gene. Ann Appl Biol 127:163–173
Graham J, Gordon SC, McNicol RJ (1997a) The effect of the CpTi gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae). Ann Appl Biol 131:133–139
Graham J, Iasi L, Millm S (1997b) Genotype-specific regeneration from a number of Rubus cultivars. Plant Cell Tissue Organ Cult 48:167–173
Graham J, Gordon SC, Smith K, McNicol RJ, McNicol JW (2002) The effect of the cowpea trypsin inhibitor in strawberry on damage by vine weevil under field conditions. J Hortic Sci Biotech 77:33–40
Gruchala A, Korbin M, Zurawicz E (2004) Conditions of transformation and regeneration of ‘Induka’ and ‘Elista’ strawberry plants. Plant Cell Tissue Organ Cult 79:153–160
Gu X, Gao Z, Zhuang W, Qiao Y, Wang X, Mi L, Zhang Z, Lin Z (2013) Comparative proteomic analysis of rd29A:RdreB1BI transgenic and non-transgenic strawberries exposed to low temperature. J Plant Phyiol 170:696–706
Guidarelli M, Baraldi E (2015) Transient transformation meets gene function discovery: the strawberry fruit case. Front Plant Sci 6:444
Gupta S, Mahalaxmi V (2009) In vitro high frequency direct plant regeneration from whole leaves of blackberry. Sci Hortic 120:22–26
Haddadi F, Aziz MA, Abdullah SNA, Tan SG, Kamaladini H (2015) An efficient Agrobacterium-mediated transformation of strawberry cv. Camarosa by a dual plasmid system. Molecules 20:3647–3666
Hanhineva KJ, Kärenlampi SO (2007) Production of transgenic strawberries by temporary immersion bioreactor system and verification by TAIL-PCR. BMC Biotechnol 7:11
Hanhineva K, Kokko H, Kärenlampi S (2005) Shoot regeneration from leaf explants of five strawberry (Fragaria × ananassa) cultivars in temporary immersion bioreactor system. In Vitro Cel Dev Biol Plant 41:826–831
Hanhineva K, Kokko H, Siljanen H, Rogachev I, Aharoni A, Kärenlampi SO (2009) Stilbene synthase gene transfer caused alterations in the phenylpropanoid metabolism of transgenic strawberry (Fragaria × ananassa). J Exp Bot 60:2093–2106
Hannum SM (2004) Potential impact of strawberries on human health: a review of the science. Crit Rev Food Sci Nutr 44:1–17
Hassan MA, Swartz HJ, Inamine G, Mullineaux P (1993) Agrobacterium tumefaciens-mediated transformation of several Rubus genotypes and recovery of transformed plants. Plant Cell Tissue Organ Cult 33:9–17
Heh Ran C, Jae Park P, Kwon Lee H, Song Joong Y, Sok Lee I (2008) The identification of optimum condition for direct regeneration in black raspberry. J Plant Biotechnol 35:163–167
Hoffmann T, Kalinowski G, Schwab W (2006) RNAi-induced silencing of gene expression in strawberry fruit (Fragaria × ananassa) by agroinfiltration: a rapid assay for gene function analysis. Plant J 48:816–826
Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387
Huetteman CA, Preece JE (1993) Thidiazuron: a potent cytokinin for woody plant tissue culture. Plant Cell Tissue Organ Cult 33:105–119
Husaini AM (2010) Pre- and post-agroinfection strategies for efficient leaf disc transformation and regeneration of transgenic strawberry plants. Plant Cell Rep 29:97–110
Husaini AM, Abdin MZ (2007) Interactive effect of light, temperature and TDZ on the regeneration potential of leaf discs of Fragaria × ananassa Duch. In Vitro Cel Dev Biol Plant 43:576–584
Husaini AM, Abdin MZ (2008) Development of transgenic strawberry (Fragaria × ananassa Duch.) plants tolerant to salt stress. Plant Sci 174:446–455
Husaini AM, Srivastava DK (2006) Plant regeneration and Agrobacterium-mediated gene transfer studies in strawberry tissues (Fragaria × ananassa). Asian J Microbiol Biotech Environ Sci 8:671–678
Husaini AM, Aquil S, Bhat M, Qadri T, Kamaluddin Abdin MZ (2008) A high-efficiency direct somatic embryogenesis system for strawberry (Fragaria × ananassa Duch.) cultivar Chandler. J Crop Sci Biotechnol 11:107–110
Husaini AM, Mercado JA, Teixeira da Silva JA, Schaart JG (2011) Review of factors affecting organogenesis, somatic embryogenesis and Agrobacterium tumefaciens-mediated transformation of strawberry. In: Husaini AM, Mercado JA (eds) Genomics, transgenics, molecular breeding and biotechnology of strawberry. Global Science Books, p 1–11
Husaini AM, Abdin MZ, Khan S, Xu YW, Aquil S, Anis M (2012) Modifying strawberry for better adaptability to adverse impact of climate change. Curr Sci 102:1660–1673
Iannetta PPM, Laarhoven L-C, Medina-Escobar N, James EK, McManus MT, Davies HV, Harren FJM (2006) Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit. Physiol Plant 127:247–259
Information Systems for Biotechnology (2016) http://www.isb.vt.edu/data.aspx. Accessed 20 Oct 2016
James DJ, Passey AJ, Barbara DJ (1990) Agrobacterium-mediated transformation of the cultivated strawberry (Fragaria × ananassa Duch.) using disarmed binary vectors. Plant Sci 69:79–94
James DJ, Passey AJ, Eastebrook MA, Solomon MG, Barbara DJ (1992) Progress in the introduction of transgenes for pest and disease resistance into strawberries. Phytoparasitica 20:83–87
Jiménez-Bermúdez S, Redondo-Nevado J, Muñoz-Blanco J, Caballero JL, López-Aranda JM, Valpuesta V, Pliego-Alfaro F, Quesada MA, Mercado JA (2002) Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiol 128:751–759
Jiwan D, Roalson EH, Main D, Dhingra A (2013) Antisense expression of peach mildew resistance locus O (PpMlo1) gene confers cross-species resistance to powdery mildew in Fragaria × ananassa. Transgenic Res 22:1119–1131
Joint Research Centre (2016) GMO register. European Commission. http://gmoinfo.jrc.ec.europa.eu/Default.aspx. Accessed 20 Oct 2016
Jung S, Ficklin S, Lee T, Cheng C-H, Blenda A, Zheng P, Yu J, Bombarely A, Cho I, Ru S, Evans K, Peace C, Abbott AG, Mueller LA, Olmstead MA, Main D (2014) The genome database for Rosaceae (GDR): year 10 update. Nucl Acids Res 42:D1237–D1244
Kokko HI, Kärenlampi SO (1998) Transformation of artic bramble (Rubus articus L.) by Agrobacterium tumefaciens. Plant Cell Rep 17:822–826
Kordestani GK, Karami O (2008) Picloram-induced somatic embryogenesis in leaves of strawberry (Fragaria ananassa L.). Acta Biol Cracov Bot 50:69–72
Kortstee AJ, Khan SA, Helderman C, Trindade LM, Wu Y, Visser RGF, Brendolise C, Allan A, Schouten HJ, Jacobsen E (2011) Anthocyanin production as a potential visual selection marker during plant transformation. Transgenic Res 20:1253–1264
Koskela EA, Mouhu K, Albani MC, Kurokura T, Rantanen M, Sargent DJ, Battey NH, Coupland G, Elomaa P, Hytönen T (2012) Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol 159:1043–1054
Koskela EA, Sønsteby A, Flachowsky H, Heide OM, Hanke M-V, Elomaa P, Hytönen T (2016) TERMINAL FLOWER1 is a breeding target for a novel everbearing trait and tailored flowering responses in cultivated strawberry (Fragaria × ananassa Duch.). Plant Biotechnol J 14:1852–1861
Landi L, Mezzetti B (2006) TDZ, auxin and genotype effects on leaf organogenesis in Fragaria. Plant Cell Rep 25:281–288
Landi L, Capocasa F, Costantini E, Mezzetti B (2009) ROLC strawberry plant adaptability, productivity, and tolerance to soil-borne disease and mycorrhizal interactions. Transgenic Res 18:933–942
Lazić T, Ruzić D (2007) Organogenesis in vitro from the leaf of blackberry cv. ‘Cacanska bestrna’. Genetika 39:69–78
Lee YK, Kim I-J (2011) Modulation of fruit softening by antisense suppression of endo-β-1,4-glucanase in strawberry. Mol Breeding 27:375–383
Li Q, Ji K, Sun Y, Luo H, Wang H, Leng P (2013) The role of FaBG3 in fruit ripening and B. cinerea fungal infection of strawberry. Plant J 76:24–35
López-Aranda JM, Pliego-Alfaro F, López-Navidad I, Barceló-Muñoz M (1994) Micropropagation of strawberry (Fragaria x ananassa Duch.). Effect of mineral salts, benzyladenine levels and number of subcultures on the in vitro and field behaviour of the obtained microplants and the fruiting capacity of their progeny. J Hortic Sci 69:625–637
Lunkenbein S, Coiner H, Ric de Vos CH, Schaart JG, Boone MJ, Krens FA, Schwab W, Salentijn EMJ (2006a) Molecular characterization of a stable antisense chalcone synthase phenotype in strawberry (Fragaria × ananassa). J Agric Food Chem 54:2145–2153
Lunkenbein S, Salentijn EMJ, Coiner HA, Boone MJ, Krens FA, Schwab W (2006b) Up- and down-regulation of Fragaria × ananassa O-methyltransferase: impacts on furanone and phenylpropanoid metabolism. J Exp Bot 57:2445–2453
Maas JL (1998) Compendium of strawberry diseases. APS Press, St Paul
Martín RR, Mathews H, Keller K, Kellogg JA, Wagner R (2003) Development of resistance to raspberry bushy dwarf virus. US Patent 6,548,742, 15 Apr 2003
Martinelli A, Gaiani A, Cella R (1997) Agrobacterium-mediated transformation of strawberry cultivar Marmolada onebar. Acta Hortic 439:169–173
Mathews H, Wagoner W, Kellogg J, Bestwick R (1995a) Genetic transformation of strawberry: stable integration of a gene to control biosynthesis of ethylene. In Vitro Cel Dev Biol Plant 31:36–43
Mathews H, Wagoner W, Cohen C, Kellog J, Bestwick R (1995b) Efficient genetic transformation of red raspberry, Rubus ideaus L. Plant Cell Rep 14:471–476
Mathews H, Dewey V, Wagoner W, Bestwick RK (1998) Molecular and cellular evidence of chimaeric tissues in primary transgenics and elimination of chimaerism through improved selection protocols. Transgenic Res 7:123–129
McNicol RJ, Graham J (1990) In vitro regeneration of Rubus from leaf and stem segments. Plant Cell Tissue Organ Cult 21:45–50
Meng R, Chen THH, Finn CE, Li Y (2004) Improving in vitro plant regeneration from leaf and petiole explants of ‘Marion’ blackberry. HortScience 39:316–320
Mercado JA, Pliego-Alfaro F, Quesada MA (2007a) Strawberry. In: Pua EC, Davey MR (eds) Biotechnology in agriculture and forestry, vol 60. Transgenic crops V. Springer, Berlin Heidelberg, pp 309–328
Mercado JA, Martín-Pizarro C, Pascual L, Quesada MA, Pliego-Alfaro F, de los Santos B, Romero F, Gálvez J, Rey M, de la Viña G, Llobell A, Yubero-Serrano E-M, Muñoz-Blanco J, Caballero JL (2007b) Evaluation of tolerance to Colletotrichum acutatum in strawberry plants transformed with Trichoderma-derived genes. Acta Hortic 738:383–388
Mercado JA, Trainotti L, Jiménez-Bermúdez S, Santiago-Doménech N, Posé S, Donolli R, Barceló M, Casadoro G, Pliego-Alfaro F, Quesada MA (2010) Evaluation of the role of the endo-β-(1,4)-glucanase gene FaEG3 in strawberry fruit softening. Postharvest Biol Technol 55:8–14
Mercado JA, Pliego-Alfaro F, Quesada MA (2011) Fruit shelf life and potential for its genetic improvement. In: Jenks MA, Bebeli PJ (eds) Breeding for fruit quality. Wiley, Oxford, pp 81–104
Mercado JA, Barceló M, Pliego C, Rey M, Caballero JL, Muñoz-Blanco J, Ruano-Rosa D, López-Herrera C, de los Santos B, Romero-Muñoz F, Pliego-Alfaro F (2015) Expression of the β-1,3-glucanase gene bgn13.1 from Trichoderma harzianum in strawberry increases tolerance to crown rot diseases but interferes with plant growth. Transgenic Res 24:979–989
Mezzetti B, Savini G, Carnevali F, Moti D (1997) Plant genotype and growth regulators interaction affecting in vitro morphogenesis of blackberry and raspberry. Biol Plant 39:139–150
Mezzetti B, Landi L, Pandolfini T, Spena A (2004) The defH9-iaaM auxin-synthesizing gene increases plant fecundity and fruit production in strawberry and raspberry. BMC Biotechnol 4:4
Millan-Mendoza B, Graham J (1999) Organogenesis and micropropagation in red raspberry using forchlorfenuron (CPPU) of blackberry (Rubus fruticosus L.). Plant Cell Tissue Organ Cult 120:351–354
Monticelli S, Gentile A, Damiano C (2002) Regeneration and Agrobacterium-mediated transformation in stipules of strawberry. Acta Hortic 567:105–107
Morgan A, Baker CM, Chu JSF, Lee K, Crandall BA, Jose L (2002) Production of herbicide tolerant strawberry through genetic engineering. Acta Hortic 567:113–115
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nagamangala Kanchiswamy CN, Sargent DJ, Velasco R, Maffei ME, Malnoy M (2015) Looking forward to genetically edited fruit crops. Trends Biotechnol 33:62–64
Nehra NS, Stushnoff C, Kartha KK (1989) Direct shoot regeneration from strawberry leaf disks. J Am Soc Hortic Sci 114:1014–1018
Nehra NS, Chibbar RN, Kartha KK, Datla RSS, Crosby WL, Stushnoff C (1990) Genetic transformation of strawberry by Agrobacterium tumefaciens using a leaf disk regeneration system. Plant Cell Rep 9:293–298
Nehra NS, Kartha KK, Stushnoff C, Giles KL (1992) The influence of plant growth regulator concentrations and callus age on somaclonal variation in callus culture regenerants of strawberry. Plant Cell Tissue Organ Cult 29:257–268
Nyman M, Wallin A (1992a) Transient gene expression in strawberry (Fragaria × ananassa Duch.) protoplasts and the recovery of transgenic plants. Plant Cell Rep 11:105–108
Nyman M, Wallin A (1992b) Improved culture technique for strawberry (Fragaria × ananassa Duch.) protoplasts and the determination of DNA content in protoplast derived plants. Plant Cell Tissue Organ Cult 30:127–133
Oosumi T, Gruszewski HA, Blischak LA, Baxter AJ, Wadl PA, Shuman JL, Veilleux RE, Shulaev V (2006) High-efficiency transformation of the diploid strawberry (Fragaria vesca) for functional genomics. Planta 223:1219–1230
Oosumi T, Ruiz-Rojas JJ, Veilleux RE, Dickerman A, Shulaev V (2010) Implementing reverse genetics in Rosaceae: analysis of T-DNA flanking sequences of insertional mutant lines in the diploid strawberry, Fragaria vesca. Physiol Plant 140:1–9
Owens CL, Thomashow MF, Hancock JF, Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologous expression of CBF1 in strawberry. J Am Soc Hortic Sci 127:489–494
Owensy de Novoa C, Conner AJ (1992) Comparison of in vitro shoot regeneration protocols from Rubus leaf explants. New Zeal J Crop Hort Sci 20:471–476
Padilla IMG, Burgos L (2010) Aminoglycoside antibiotics: structure, functions and effects on in vitro plant culture and genetic transformation protocols. Plant Cell Rep 29:1203–1213
Palomer X, Llop-Tous I, Vendrell M, Krens FA, Schaart JG, Boone MJ, van der Valk E, Salentijn EMJ (2006) Antisense down-regulation of strawberry endo-β-(1,4)-glucanase genes does not prevent fruit softening during ripening. Plant Sci 171:640–646
Paniagua C, Blanco-Portales R, Barceló-Muñoz M, García-Gago JA, Waldron KW, Quesada MA, Muñoz-Blanco J, Mercado JA (2016) Antisense down-regulation of the strawberry β-galactosidase gene FaβGal4 increases cell wall galactose levels and reduces fruit softening. J Exp Bot 67:619–631
Pantazis CJ, Fisk S, Mills K, Flinn BS, Shulaev V, Veilleux RE, Dan Y (2013) Development of an efficient transformation method by Agrobacterium tumefaciens and high throughput spray assay to identify transgenic plants for woodland strawberry (Fragaria vesca) using NPTII selection. Plant Cell Rep 32:329–337
Park J-I, Lee Y-K, Chung W-I, Lee I-H, Choi J-H, Lee W-M, Ezura H, Lee S-P, Kim I-J (2006) Modification of sugar composition in strawberry fruit by antisense suppression of an ADP-glucose pyrophosphorylase. Mol Breeding 17:269–279
Passey AJ, Barrett KJ, James DJ (2003) Adventitious shoot regeneration from seven commercial strawberry cultivars (Fragaria × ananassa Duch.) using a range of explant types. Plant Cell Rep 21:397–401
Pineda H, Posé S, Paniagua C, García-Gago JA, Pliego-Alfaro F, Quesada MA, Mercado JA, Matas AJ (2013) A core collection of modified strawberry germplasm as a resource tool for funghi infection and fruit texture studies. In: International strawberry congress, 2nd edn, Antwerp, Belgium, 4–6 Sept 2013
Posé S, Kirby AR, Paniagua C, Waldron KW, Morris VJ, Quesada MA, Mercado JA (2015) The nanostructural characterization of strawberry pectins in pectate lyase or polygalacturonase silenced fruits elucidates their role in softening. Carbohydr Polym 132:134–145
Puite KJ, Schaart JG (1998) Agrobacterium-mediated transformation of the apple cultivars ‘Gala’, ‘Golden Delicious’ and ‘Elstar’, and the strawberry cultivars ‘Gariguette’, ‘Polka’ and ‘Elsanta’. Acta Hortic 484:547–556
Qin YH, Zhang SL, Asghar S, Zhang LX, Qin QP, Chen KS, Xu CJ (2005a) Regeneration mechanism of Toyonoka strawberry under different color plastic films. Plant Sci 168:1425–1431
Qin YH, Zhang SL, Zhang LX, Zhu DY, Syed A (2005b) Response of in vitro strawberry to silver nitrate (AgNO3). HortScience 40:747–751
Qin YH, Teixeira da Silva JA, Bi JH, Zhang SL, Hu GB (2011) Response of in vitro strawberry to antibiotics. Plant Growth Regul 65:183–193
Quesada MA, Martín-Pizarro C, García-Gago JA, Posé S, Santiago N, Sesmero R, Pliego-Alfaro F, Mercado JA (2007) Transgenic strawberry: current status and future perspectives. Transgenic Plant J 1:280–288
Quesada MA, Blanco-Portales R, Posé S, García-Gago JA, Jiménez-Bermúdez S, Muñoz-Serrano A, Caballero JL, Pliego-Alfaro F, Mercado JA, Muñoz-Blanco J (2009) Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiol 150:1022–1032
Reis L, Ayub RA (2015) Organogenesis and plant selection by kanamycin of strawberry in vitro aiming at genetic transformation. Semina: Ciências Agrárias 36:2443–2452
Ricardo VG, Coll Y, Castagnaro A, Diaz Ricci JC (2003) Transformation of a strawberry cultivar using a modified regeneration medium. HortScience 38:277–280
Rommens CM, Haring MA, Swords K, Davies HV, Belknap WR (2007) The intragenic approach as a new extension to traditional plant breeding. Trends Plant Sci 12:397–403
Saied AM, Keutgen AJ, Noga G (2005) The influence of NaCl salinity on growth, yield and fruit quality of strawberry cvs. ‘Elsanta’ and ‘Korona’. Sci Hortic 103:289–303
Schaart JG, Krens FA, Pelgrom KTB, Mendes O, 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
Schaart JG, Kjellsen TD, Mehli L, Heggem R, Iversen T-H, Schouten HJ, Krens FA (2011) Towards the production of genetically modified strawberries which are acceptable to consumers. In: Husaini AM, Mercado JA (eds) Genomics, transgenics, molecular breeding and biotechnology of strawberry. Global Science Books, pp 103–107
Schawb W, Hoffmann T, Kalinowski G, Preuß A (2011) Functional genomics in strawberry fruit through RNAi-mediated silencing. In: Husaini AM, Mercado JA (eds) Genomics, transgenics, molecular breeding and biotechnology of strawberry. Global Science Books, pp 91–101
Schestibratov KA, Dolgov SV (2005) Transgenic strawberry plants expressing a thaumatin II gene demonstrate enhanced resistance to Botrytis cinerea. Sci Hortic 106:177–189
Schouten HJ, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants. EMBO Rep 7:750–753
Sesmero R, Quesada MA, 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
Sesmero R, Mitchell JR, Mercado JA, Quesada MA (2009) Rheological characterisation of juices obtained from transgenic pectate lyase-silenced strawberry fruits. Food Chem 116:426–432
Shakhbazau AV, Kartel NA (2008) Chitinases in bioengineering research. Russ J Genet 44:881–889
Shaw DV, Gubler WD, Larson KD, Hansen J (1996) Genetic variation for field resistance to Verticillium dahliae evaluated using genotypes and segregating progenies of California strawberries. J Am Soc Hortic Sci 121:625–628
Silva KJP, Brunings A, Peres NA, Mou Z, Folta KA (2015) The Arabidopsis NPR1 gene confers broad-spectrum disease resistance in strawberry. Transgenic Res 24:693–704
Sjulin TM, Dale A (1987) Genetic diversity of North American strawberry cultivars. J Am Soc Hortic Sci 112:375–385
Skirvin RM, Motoike S, Coyner M, Norton MA (2005) Rubus spp. Cane fruit. In: Litz RE (ed) Biotechnology of fruit and nut crops. CABI Publishing, pp 566–582
Sorvari S, Ulvinen S, Hietaranta T, Hiirsalmi H (1993) Preculture medium promotes direct shoot regeneration from micropropagated strawberry leaf disks. HortScience 28:55–57
Spolaore S, Trainotti L, Casadoro G (2001) A simple protocol for transient gene expression in ripe fleshy fruit mediated by Agrobacterium. J Exp Bot 52:845–850
Súkeníková M, Libiaková G, Moravčíková J, Hricová A, Gajdošova A (2015) Agrobacterium tumefaciens-mediated transformation of blackberry (Rubus fruticosus L.). Plant Cell Tissue Organ Cult 120:351–354
Swartz HJ, Bors R, Mohamed F, Naess SK (1990) The effect of pretreatment on subsequent shoot organogenesis from Rubus and Malus leaves. Plant Cell Tissue Organ Cult 21:179–184
Szajdek A, Borowska EJ (2008) Bioactive compounds and health-promoting properties of berry fruits: a review. Plant Foods Hum Nutr 63:147–156
Tian M, Gu Q, Zhu M (2003) The involvement of hydrogen peroxide and antioxidant enzymes in the process of shoot organogenesis of strawberry callus. Plant Sci 165:701–707
Tian J, Cheng L, Z-y Han, Y-c Yao (2015) Tobacco rattle virus mediated gene silencing in strawberry plants. Plant Cell Tissue Organ Cult 120:1131–1138
Tsao CW, Reed BM (2002) Gelling agents, silver nitrate and sequestrene iron influence adventitious shoot and callus formation from Rubus leaves. In Vitro Cell Dev Biol Plant 38:29–32
Turk BA, Swartz HJ, Zimmerman RH (1994) Adventitious shoot regeneration from in vitro-cultured leaves of Rubus genotypes. Plant Cell Tissue Organ Cult 38:11–17
Untergasser A, Bijl GJM, Liu W, Bisseling T, Schaart JG, Geurts R (2012) One-step Agrobacterium mediated transformation of eight genes essential for Rhizobium symbiotic signaling using the novel binary vector system pHUGE. PLoS ONE 7:e47885
Veilleux RE, Mills KP, Baxter AJ, Upham KT, Ferguson TJ, Holt SH, Lu N, Ruiz-Rojas JJ, Pantazis CJ, Davis CM, Lindsay RC, Powell FL, Dan Y, Dickerman AW, Oosumi T, Shulaev V (2012) Transposon tagging in diploid strawberry. Plant Biotechnol J 10:985–994
Vellicce GR, Díaz Ricci JC, Hernández L, 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
Vujović T, Ružić D, Cerović R (2014) Adventitious organogenesis via intermediate callus formation in representatives of Prunus, Pyrus and Rubus genera. Rom Biotechnol Lett 19(3)
Wang DY, Wergin WP, Zimmerman RH (1984) Somatic embryogenesis and plant regeneration from immature embryos of strawberry. HortScience 19:71–72
Wang J, Ge H, Peng S, Zhang H, Chen P, Xu J (2004) Transformation of strawberry (Fragaria ananassa Duch.) with late embryogenesis abundant protein gene. J Hortic Sci Biotechnol 79:735–738
Wang F, Gao ZH, Qiao YS, Mi L, Li JF, Zhang Z (2014) RdreB1BI gene expression driven by the stress-induced promoter rd29A enhances resistance to cold stress in Benihope strawberry. Acta Hortic 1049:975–987
Watt K, Graham J, Gordon SC, Woodhead M, McNicol RJ (1999) Current and future transgenic control strategies to vine weevil and other insect resistance in strawberry. J Hort Sci Biotech 74:409–421
Wawrzynczak D, Sowik I, Michalczuk L (2000) Agrobacterium-mediated transformation of five strawberry genotypes. J Fruit Ornam Plant Res 8:1–8
Woolley LC, James DJ, 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
Yeh S-Y, Huang F-C, Hoffmann T, Mayershofer M, Schwab W (2014) FaPOD27 functions in the metabolism of polyphenols in strawberry fruit (Fragaria sp.). Front Plant Sci 5:518
Youssef SM, Jiménez-Bermúdez S, Luz Bellido M, Martín-Pizarro C, Barceló M, Abdal-Aziz SA, Caballero JL, López-Aranda JM, Pliego-Alfaro F, Muñoz J, Quesada MA, Mercado JA (2009) Fruit yield and quality of strawberry plants transformed with a fruit specific strawberry pectate lyase gene. Sci Hortic 119:120–125
Zakaria H, Hussein GM, Abdel-Hadi A-HA, Abdallah NA (2014) Improved regeneration and transformation protocols for three strawberry cultivars. GM Crops Food 5:27–35
Zawadzka M, Orlikowska T (2006) Factors modifying regeneration in vitro of adventitious shoots in five red raspberry cultivars. J Fruit Ornam Plant Res 14:105–115
Zhang Q, Folta KM, Davis TM (2014) Somatic embryogenesis, tetraploidy, and variant leaf morphology in transgenic diploid strawberry (Fragaria vesca subspecies vesca ‘Hawaii 4’). BMC Plant Biol 14:23
Zhou J, Wang G, Liu Z (2018) Efficient genome-editing of wild strawberry genes, vector development, and validation. Plant Biotechnol J. https://doi.org/10.1111/pbi.12922. (in press)
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We acknowledge the Ministerio de Economía y Competitividad of Spain and FEDER EU Funds (grant reference AGL2014-55784-C2-1-R) for financial support.
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Palomo-Ríos, E., Quesada, M.A., Matas, A.J., Pliego-Alfaro, F., Mercado, J.A. (2018). The History and Current Status of Genetic Transformation in Berry Crops. In: Hytönen, T., Graham, J., Harrison, R. (eds) The Genomes of Rosaceous Berries and Their Wild Relatives. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-76020-9_11
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