Advancements in plant regeneration and genetic transformation of grapevine (Vitis spp.)

doi:10.1016/S2095-3119(20)63586-9

摘要/Abstract

摘要：

葡萄是世界上最重要的经济作物之一，改善其主要农艺性状以适应不断变化的农业环境和消费者需求是非常重要的。随着现代生物技术的发展，尤其是分子遗传技术的应用，为选育高产、优质、抗逆和抗病性强的葡萄新品种提供了新方法。目前，通过基因枪和农杆菌介导法已成功将一些葡萄品种进行遗传转化，并通过建立的再生体系获得了转基因葡萄植株。然而，基因型，外植体类型以及培养基的组成成分能够影响葡萄植株再生效率；受体材料、菌株和浓度、筛选标记的选用也会影响其转化效率。本文归纳总结了近年来报道的葡萄植株再生和遗传转化的研究进展，存在的问题和未来的研究方向，以期为葡萄新品种改良提供参考。

Abstract:

Grapevine (Vitis spp.) is one of the most economically important fruit crops worldwide, and there is considerable interest in improving its major agronomic and enological traits in response to ever-changing agricultural environments and consumer demands. Molecular genetic techniques in particular, associated with rapid technological advancements, provide an attractive alternative to conventional breeding approaches for developing new grapevine varieties with enhanced yield performance, quality, stress tolerance and disease resistance. To date, several grapevine varieties have been transformed with genes associated with diverse functions through biolistic bombardment and/or Agrobacterium-mediated transformation, and transgenic grape lines have been obtained using established regeneration systems. Nevertheless, a wide range of factors, including genotype, explant source and culture medium, have been shown to affect the efficiency of plant regeneration. Moreover, the selection and use of acceptor materials, bacterial strain and cell density, selectable markers and selection methods also influence transformation efficiency. This paper provides an overview of recent advances in grapevine regeneration and genetic transformation and in-depth discussion of the major limiting factors, and discusses promising future strategies to develop robust plant regeneration and genetic transformation in grapevine.

Key words: grapevine , organogenesis , somatic embryogenesis , plant regeneration , genetic transformation

. [J]. Journal of Integrative Agriculture, 2021, 20(6): 1407-1434.

ZHANG Xiu-ming, WU Yi-fei, LI Zhi, SONG Chang-bing, WANG Xi-ping. Advancements in plant regeneration and genetic transformation of grapevine (Vitis spp.)[J]. Journal of Integrative Agriculture, 2021, 20(6): 1407-1434.

参考文献

Acanda Y, Prado M J, González M V, Rey M. 2013. Somatic embryogenesis from stamen filaments in grapevine (Vitis vinifera L. cv. Mencía): Changes in ploidy level and nuclear DNA content. In Vitro Cellular & Developmental Biology - Plant, 49, 276–284.
Agüero C B, Meredith C P, Dandekar A M. 2006. Genetic transformation of Vitis vinifera L. cvs. Thompson Seedless and Chardonnay with the pear PGIP and GFP encoding genes. Vitis, 45, 1–8.
Agüero C B, Uratsu S L, Greve C, Powell A L T, Labavitch J M, Meredith C P, Dandekar A M. 2005. Evaluation of tolerance to Pierce’s disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Molecular Plant Pathology, 6, 43–51.
Alavijeh M K, Ebadi A, Zarei A, Omidi M. 2016. Somatic Embryogenesis from anther, whole flower, and leaf explants of some grapevine cultivars. Plant Tissue Culture and Biotechnology, 26, 219–230.
Altpeter F, Baisakh N, Beachy R, Bock R, Capell T, Christou P, Daniell H, Datta K, Datta S, Dix P J, Fauquet C, Huang N, Kohli A, Mooibroek H, Nicholson L, Nguyen T T, Nugent G, Raemakers K, Romano A, Somers D A, et al. 2005. Particle bombardment and the genetic enhancement of crops: Myths and realities. Molecular Breeding, 15, 305–327.
Araya S, Prieto H, Hinrichsen P. 2008. An efficient buds culture method for the regeneration via somatic embryogenesis of table grapes ‘Red Globe’ and ‘Flame Seedless’. Vitis, 47, 251–252.
Ben-Amar A, Cobanov P, Buchholz G, Mliki A, Reustle G. 2013. In planta agro-infiltration system for transient gene expression in grapevine (Vitis spp.). Acta Physiologiae Plantarum, 35, 3147–3156.
Bertini E, Tornielli G B, Pezzotti M, Zenoni S. 2019. Regeneration of plants from embryogenic callus-derived protoplasts of Garganega and Sangiovese grapevine (Vitis vinifera L.) cultivars. Plant Cell, Tissue and Organ Culture, 138, 239–246.
Bornhoff B A, Harst M, Zyprian E, Töpfer R. 2005. Transgenic plants of Vitis vinifera cv. Seyval blanc. Plant Cell Reports, 24, 433–438.
Bouamama B, Mliki A, Ghorbel A. 2000. Efficiency of coupling biolistic and Agrobacterium in genetic transformation of Tunisian autochthonous grapes. Agricoltura Mediterranea, 130, 223–227.
Cadavid-Labrada A, Medina C, Martinelli L, Arce-Johnson P. 2008. Somatic embryogenesis and efficient regeneration of Vitis vinifera L. ‘Carménère’ plants. Vitis, 47, 73–74.
Cardoso H G, Campos M C, Pais M S, Peixe A. 2019. Somatic embryogenesis in Iberian grapevine (Vitis vinifera) cultivars using carpels as initial explants: Protocol establishment and histological evaluation. Journal of Agricultural Science and Technology, B9, 15–30.
Carimi F, Barizza E, Gardiman M, Lo Schiavo F. 2005. Somatic embryogenesis from stigmas and styles of grapevine. In Vitro Cellular & Developmental Biology - Plant, 41, 249–252.
Carra A, Sajeva M, Abbate L, Siragusa M, Pathirana R, Carimi F. 2016. Factors affecting somatic embryogenesis in eight Italian grapevine cultivars and the genetic stability of embryo-derived regenerants as assessed by molecular markers. Scientia Horticulturae, 204, 123–127.
de Carvalho D C, da Silva A L L, Schuck M R, Purcino M, Tanno G N, Biasi L A. 2013. Fox grape cv. Bordô (Vitis labrusca L.) and grapevine cv. Chardonnay (Vitis vinifera L.) cultivated in vitro under different carbohydrates, amino acids and 6-benzylaminopurine levels. Brazilian Archives of Biology and Technology, 56, 191–201.
de Carvalho D C, da Silva A L L, Tanno G N, Purcino M, Biasi L A. 2011. Organogenesis from leaf segments and internodes of grapevine cv. Merlot. Ciência e Agrotecnologia, 35, 108–114.
Chee R, Pool R M, Bucher D. 1984. A method for large scale in vitro propagation of Vitis. New York’s Food and Life Sciences Bulletin, 109, 1–9.
Cheng S, Xie X, Xu Y, Zhang C, Wang X, Zhang J, Wang Y. 2016. Genetic transformation of a fruit-specific, highly expressed stilbene synthase gene from Chinese wild Vitis quinquangularis. Planta, 243, 1041–1053.
Chu M, Quiñonero C, Akdemir H, Alburquerque N, Pedreño M Á, Burgos L. 2016. Agrobacterium-mediated transformation of Vitis cv. Monastrell suspension-cultured cells: Determination of critical parameters. Biotechnology Progress, 32, 725–734.
Clog E, Bass P, Walter B. 1990. Plant regeneration by organogenesis in Vitis rootstock species. Plant Cell Reports, 8, 726–728.
Colby S M, Juncosa A M, Meredith C P. 1991a. Cellular differences in Agrobacterium susceptibility and regenerative capacity restrict the development of transgenic grapevines. Journal of the American Society for Horticultural Science, 116, 356–361.
Colby S M, Juncosa A M, Stamp J A, Meredith C P. 1991b. Developmental anatomy of direct shoot organogenesis from leaf petioles of Vitis vinifera (Vitaceae). American Journal of Botany, 78, 260–269.
Comprorr M E, Gray D J. 1996. Effects of sucrose and methylglyoxal bis-(guanylhydrazone) on controlling grape somatic embryogenesis. Vitis, 35, 1–6.
Cutanda M C, Bouquet A, Chatelet P, Lopez G, Botella O, Montero F J, Torregrosa L. 2008. Somatic embryogenesis and plant regeneration of Vitis vinifera cultivars ‘Macabeo’ and ‘Tempranillo’. Vitis, 47, 159–162.
Dai L, Wang D, Xie X, Zhang C, Wang X, Xu Y, Wang Y, Zhang J. 2016. The novel gene VpPR4-1 from Vitis pseudoreticulata increases powdery mildew resistance in transgenic Vitis vinifera L. Frontiers in Plant Science, 7, 695.
Dai L, Zhou Q, Li R, Du Y, He J, Wang D, Cheng S, Zhang J, Wang Y. 2015. Establishment of a picloram-induced somatic embryogenesis system in Vitis vinifera cv. Chardonnay and genetic transformation of a stilbene synthase gene from wild-growing Vitis species. Plant Cell, Tissue and Organ Culture, 121, 397–412.
Dalla Costa L, Mandolini M, Poletti V, Martinelli L. 2010. Comparing 17-β-estradiol supply strategies for applying the XVE-Cre/loxP system in grape gene transfer (Vitis vinifera L.). Vitis, 49, 201–208.
Dalla Costa L, Piazza S, Campa M, Flachowsky H, Hanke M V, Malnoy M. 2016. Efficient heat-shock removal of the selectable marker gene in genetically modified grapevine. Plant Cell, Tissue and Organ Culture, 124, 471–481.
Das D K, Reddy M K, Upadhyaya K C, Sopory S K. 2002. An efficient leaf-disc culture method for the regeneration via somatic embryogenesis and transformation of grape (Vitis vinifera L.). Plant Cell Reports, 20, 999–1005.
Debernardi J M, Tricoli D M, Ercoli M F, Hayta S, Ronald P, Palatnik J F, Dubcovsky J. 2020. A GRF-GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nature Biotechnology, 38, 1274–1279.
Dhekney S A, Li Z T, Van Aman M, Dutt M, Tattersall J, Kelley K T, Gray D J. 2007. Genetic transformation of embryogenic cultures and recovery of transgenic plants in Vitis vinifera, Vitis rotundifolia and Vitis hybrids. Acta Horticulturae, 738, 743–748.
Dhekney S A, Li Z T, Compton M E, Gray D J. 2009a. Optimizing initiation and maintenance of Vitis embryogenic cultures. HortScience, 44, 1400–1406.
Dhekney S A, Li Z T, Dutt M, Gray D J. 2008. Agrobacterium-mediated transformation of embryogenic cultures and plant regeneration in Vitis rotundifolia Michx. (muscadine grape). Plant Cell Reports, 27, 865–872.
Dhekney S A, Li Z T, Gray D J. 2011a. Factors influencing induction and maintenance of Vitis rotundifolia Michx. embryogenic cultures. Plant Cell, Tissue and Organ Culture, 105, 175–180.
Dhekney S A, Li Z T, Gray D J. 2011b. Grapevines engineered to express cisgenic Vitis vinifera thaumatin-like protein exhibit fungal disease resistance. In Vitro Cellular & Developmental Biology - Plant, 47, 458–466.
Dhekney S A, Li Z T, Zimmerman T W, Gray D J. 2009b. Factors influencing genetic transformation and plant regeneration of Vitis. American Journal of Enology and Viticulture, 60, 285–292.
Doyle C, Higginbottom K, Swift T A, Winfield M, Bellas C, Benito-Alifonso D, Fletcher T, Carmen Galan M, Edwards K, Whitney H M. 2019. A simple method for spray-on gene editing in planta. BioRxiv, 805036.
Driver J A, Kuniyuki A H. 1984. In vitro propagation of Paradox walnut rootstock. HortScience, 19, 507–509.
Dutt M, Li Z T, Dhekney S A, Gray D J. 2007. Transgenic plants from shoot apical meristems of Vitis vinifera L. “Thompson Seedless” via Agrobacterium-mediated transformation. Plant Cell Reports, 26, 2101–2110.
Dutt M, Li Z T, Dhekney S A, Gray D J. 2008. A co-transformation system to produce transgenic grapevines free of marker genes. Plant Science, 175, 423–430.
Elidemir A Y, Uzun H I, Bayir A. 2007. Effect of different medium and sucrose concentrations on germination of somatic embryos in grape. Acta Horticulturae, 754, 117–121.
Emershad R L, Ramming D W. 1994. Somatic embryogenesis and plant development from immature zygotic embryos of seedless grapes (Vitis vinifera L.). Plant Cell Reports, 14, 6–12.
Fan C, Pu N, Wang X, Wang Y, Fang L, Xu W, Zhang J. 2008. Agrobacterium-mediated genetic transformation of grapevine (Vitis vinifera L.) with a novel stilbene synthase gene from Chinese wild Vitis pseudoreticulata. Plant Cell, Tissue and Organ Culture, 92, 197–206.
Favre J M. 1977. Premiers résultats concernant l’obtention in vitro de néoformations caulinaires chez la Vigne. Annales de l’Amélioration des Plantes, 27, 151–169.
Franks T, He D G, Thomas M. 1998. Regeneration of transgenic Vitis vinifera L. Sultana plants: Genotypic and phenotypic analysis. Molecular Breeding, 4, 321–333.
Le Gall O, Torregrosa L, Danglot Y, Candresse T, Bouquet A. 1994. Agrobacterium-mediated genetic transformation of grapevine somatic embryos and regeneration of transgenic plants expressing the coat protein of grapevine chrome mosaic nepovirus (GCMV). Plant Science, 102, 161–170.
Gambino G, Ruffa P, Vallania R, Gribaudo I. 2007. Somatic embryogenesis from whole flowers, anthers and ovaries of grapevine (Vitis spp.). Plant Cell, Tissue and Organ Culture, 90, 79–83.
Gao C, Long D, Lenk I, Nielsen K K. 2008. Comparative analysis of transgenic tall fescue (Festuca arundinacea Schreb.) plants obtained by Agrobacterium-mediated transformation and particle bombardment. Plant Cell Reports, 27, 1601–1609.
Gray D J. 1989. Effects of dehydration and exogenous growth regulators on dormancy, quiescence and germination of grape somatic embryos. In Vitro Cellular & Developmental Biology - Plant, 25, 1173–1178.
Gray D J, Benton C M. 1991. In vitro micropropagation and plant establishment of muscadine grape cultivars (Vitis rotundifolia). Plant Cell, Tissue and Organ Culture, 27, 7–14.
Gray D J, Meredith C P. 1992. Grape biotechnology. In: Hammerschlag F A, Litz R E, eds., Biotechnology of Perennial Fruit Crops. Commonwealth Agricultural Bureaux International, Wallingford. pp. 229–262.
Gribaudo I, Gambino G, Vallania R. 2004. Somatic embryogenesis from grapevine anthers: The optimal developmental stage for collecting explants. American Journal of Enology and Viticulture, 55, 427–430.
Gribaudo I, Schubert A, Camino C. 1995. Establishment of grapevine axenic root lines by inoculation with Agrobacterium rhizogenes. Advances in Horticultural Science, 9, 87–91.
Guan X, Zhao H, Xu Y, Wang Y. 2013. Studies on gene transfer of shoot apical meristems by Agrobacterium-mediated genetic transformation in a progeny of Chinese wild Vitis pseudoreticulata. Vitis, 52, 185–192.
Guellec V, David C, Branchard M, Tempé J. 1990. Agrobacterium rhizogenes mediated transformation of grapevine (Vitis vinifera L.). Plant Cell, Tissue and Organ Culture, 20, 211–215.
Gutoranov G P, Tsvetkov I J, Colova-Tsolova V M, Atanassov A I. 2001. Genetically engineered grapevines carrying GFLV coat protein and antifreeze genes. Agriculturae Conspectus Scientificus, 66, 71–76.
He R, Wu J, Zhang Y, Agüero C B, Li X, Liu S, Wang C, Andrew Walker M, Lu J. 2017. Overexpression of a thaumatin-like protein gene from Vitis amurensis improves downy mildew resistance in Vitis vinifera grapevine. Protoplasma, 254, 1579–1589.
Hébert D, Kikkert J R, Smith F D, Reisch B I. 1993. Optimization of biolistic transformation of embryogenic grape cell suspensions. Plant Cell Reports, 12, 585–589.
Hébert-Soulé D, Kikkert J R, Reisch B I. 1995. Phosphinothricin stimulates somatic embryogenesis in grape (Vitis sp. L.). Plant Cell Reports, 14, 380–384.
Hwang H H, Yu M, Lai E M. 2017. Agrobacterium-mediated plant transformation: Biology and applications. Arabidopsis Book, 15, e0186.
Iocco P, Franks T, Thomas M R. 2001. Genetic transformation of major wine grape cultivars of Vitis vinifera L. Transgenic Research, 10, 105–112.
Jardak-Jamoussi R, Bouamama B, Mliki A, Ghorbel A, Reustle G M. 2008. The use of phosphinothricin resistance as selectable marker for genetic transformation of grapevine. Vitis, 47, 35–37.
Jardak-Jamoussi R, Winterhagen P, Bouamama B, Dubois C, Mliki A, Wetzel T, Ghorbel A, Reustle G M. 2009. Development and evaluation of a GFLV inverted repeat construct for genetic transformation of grapevine. Plant Cell, Tissue and Organ Culture, 97, 187–196.
Jayasankar S, Gray D J, Litz R E. 1999. High-efficiency somatic embryogenesis and plant regeneration from suspension cultures of grapevine. Plant Cell Reports, 18, 533–537.
Jiang J, Xi H, Dai Z, Lecourieux F, Yuan L, Liu X, Patra B, Wei Y, Li S, Wang L. 2019. VvWRKY8 represses stilbene synthase genes through direct interaction with VvMYB14 to control resveratrol biosynthesis in grapevine. Journal of Experimental Botany, 70, 715–729.
Jiao L, Zhang Y, Lu J. 2017. Overexpression of a stress-responsive U-box protein gene VaPUB affects the accumulation of resistance related proteins in Vitis vinifera ‘Thompson Seedless’. Plant Physiology and Biochemistry, 112, 53–63.
Jittayasothorn Y, Yang Y, Chen S, Wang X, Zhong G Y. 2011. Influences of Agrobacterium rhizogenes strains, plant genotypes, and tissue types on the induction of transgenic hairy roots in Vitis species. Vitis, 50, 107–114.
Kandel R, Bergey D R, Dutt M, Sitther V, Li Z T, Gray D J, Dhekney S A. 2016. Evaluation of a grapevine-derived reporter gene system for precision breeding of Vitis. Plant Cell, Tissue and Organ Culture, 124, 599–609.
Kikkert J R, Ali G S, Wallace P G, Reisch B, Reustle G M. 2000. Expression of a fungal chitinase in Vitis vinifera L. ‘Merlot’ and ‘Chardonnay’ plants produced by biolistic transformation. Acta Horticulturae, 528, 297–303.
Kikkert J R, Hébert-Soulé D, Wallace P G, Striem M J, Reisch B I. 1996. Transgenic plantlets of ‘Chancellor’ grapevine (Vitis sp.) from biolistic transformation of embryogenic cell suspensions. Plant Cell Reports, 15, 311–316.
Kikkert J R, Striem M J, Vidal J R, Wallace P G, Barnard J, Reisch B I. 2005. Long-term study of somatic embryogenesis from anthers and ovaries of 12 grapevine (Vitis sp.) genotypes. In Vitro Cellular & Developmental Biology - Plant, 41, 232–239.
Kong J, Martin-Ortigosa S, Finer J, Orchard N, Gunadi A, Batts L A, Thakare D, Rush B, Schmitz O, Stuiver M, Olhoft P, Pacheco-Villalobos D. 2020. Overexpression of the transcription factor GROWTH-REGULATING FACTOR5 improves transformation of dicot and monocot species. Frontiers in Plant Science, 11, 572319.
Kurmi U S, Sharma D K, Tripathi M K, Tiwari R, Baghel B S, Tiwari S. 2011. Plant regeneration of Vitis vinifera (L) via direct and indirect organogenesis from cultured nodal segments. Journal of Agricultural Technology, 7, 721–737.
Li H, Li F, Du J, Lu H, He Z. 2008. Somatic embryogenesis and histological analysis from zygotic embryos in Vitis vinifera L. ‘Moldova’. Forestry Studies in China, 10, 253–258.
Li M Y, Jiao Y T, Wang Y T, Zhang N, Wang B B, Liu R Q, Yin X, Xu Y, Liu G T. 2020. CRISPR/Cas9-mediated VvPR4b editing decreases downy mildew resistance in grapevine (Vitis vinifera L.). Horticulture Research, 7, 149.
Li Z, Jayasankar S, Gray D J. 2001. Expression of a bifunctional green fluorescent protein (GFP) fusion marker under the control of three constitutive promoters and enhanced derivatives in transgenic grape (Vitis vinifera). Plant Science, 160, 877–887.
Li Z T, Dhekney S, Dutt M, Van Aman M, Tattersall J, Kelley K T, Gray D J. 2006. Optimizing Agrobacterium-mediated transformation of grapevine. In Vitro Cellular & Developmental Biology - Plant, 42, 220–227.
Li Z T, Dhekney S A, Dutt M, Gray D J. 2008. An improved protocol for Agrobacterium-mediated transformation of grapevine (Vitis vinifera L.). Plant Cell, Tissue and Organ Culture, 93, 311–321.
Li Z T, Dhekney S A, Gray D J. 2011. Use of the VvMybA1 gene for non-destructive quantification of promoter activity via color histogram analysis in grapevine (Vitis vinifera) and tobacco. Transgenic Research, 20, 1087–1097.
Li Z T, Hopkins D L, Gray D J. 2015. Overexpression of antimicrobial lytic peptides protects grapevine from Pierce’s disease under greenhouse but not field conditions. Transgenic Research, 24, 821–836.
Li Z T, Kim K H, Dhekney S A, Jasinski J R, Creech M R, Gray D J. 2014. An optimized procedure for plant recovery from somatic embryos significantly facilitates the genetic improvement of Vitis. Horticulture Research, 1, 14027.
Linsmaier E M, Skoog F. 1965. Organic growth factor requirements of tobacco tissue cultures. Physiologia Plantarum, 18, 100–127.
Lloyd G, McCown B. 1980. Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Combined Proceedings, International Plant Propagators’ Society, 30, 421–427.
López-Pérez A J, Carreño J, Dabauza M. 2006. Somatic embryo germination and plant regeneration of three grapevine cvs: Effect of IAA, GA3 and embryo morphology. Vitis, 45, 141–143.
López-Pérez A J, Carreño J, Martínez-Cutillas A, Dabauza M. 2005. High embryogenic ability and plant regeneration of table grapevine cultivars (Vitis vinifera L.) induced by activated charcoal. Vitis, 44, 79–85.
López-Pérez A J, Velasco L, Pazos-Navarro M, Dabauza M. 2008. Development of highly efficient genetic transformation protocols for table grape Sugraone and Crimson Seedless at low Agrobacterium density. Plant Cell, Tissue and Organ Culture, 94, 189–199.
Lowe K, La Rota M, Hoerster G, Hastings C, Wang N, Chamberlin M, Wu E, Jones T, Gordon-Kamm W. 2018. Rapid genotype “independent” Zea mays L. (maize) transformation via direct somatic embryogenesis. In Vitro Cellular & Developmental Biology - Plant, 54, 240–252.
Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho M J, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, et al. 2016. Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell, 28, 1998–2015.
Lupo R, Martell G P, Castellano M A, Boscia D, Savino V. 1994. Agrobacterium rhizogenes-transformed plant roots as a source of grapevine viruses for purification. Plant Cell, Tissue and Organ Culture, 36, 291–301.
Lv Z, Jiang R, Chen J, Chen W. 2020. Nanoparticle-mediated gene transformation strategies for plant genetic engineering. Plant Journal, 104, 880–891.
Ma H, Xiang G, Li Z, Wang Y, Dou M, Su L, Yin X, Liu R, Wang Y, Xu Y. 2018. Grapevine VpPR10.1 functions in resistance to Plasmopara viticola through triggering a cell death-like defense response by interacting with VpVDAC3. Plant Biotechnology Journal, 16, 1488–1501.
Maher M F, Nasti R A, Vollbrecht M, Starker C G, Clark M D, Voytas D F. 2020. Plant gene editing through de novo induction of meristems. Nature Biotechnology, 38, 84–89.
Maillot P, Deglène-Benbrahim L, Walter B. 2016. Efficient somatic embryogenesis from meristematic explants in grapevine (Vitis vinifera L.) cv. Chardonnay: An improved protocol. Trees, 30, 1377–1387.
Maillot P, Kieffer F, Walter B. 2006. Somatic embryogenesis from stem nodal sections of grapevine. Vitis, 45, 185–189.
Malnoy M, Viola R, Jung M H, Koo O J, Kim S, Kim J S, Velasco R, Kanchiswamy C N. 2016. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Frontiers in Plant Science, 7, 1904.
Martinelli L, Mandolino G. 1994. Genetic transformation and regeneration of transgenic plants in grapevine (Vitis rupestris S.). Theoretical and Applied Genetics, 88, 621–628.
Mezzetti B, Pandolfini T, Navacchi O, Landi L. 2002. Genetic transformation of Vitis vinifera via organogenesis. BMC Biotechnology, 2, 18.
Morgana C, Di Lorenzo R, Carimi F. 2004. Somatic embryogenesis of Vitis vinifera L. (cv. Sugraone) from stigma and style culture. Vitis, 43, 169–173.
Motoike S Y, Skirvin R M, Norton M A, Otterbacher A G. 2001. Somatic embryogenesis and long term maintenance of embryogenic lines from fox grapes. Plant Cell, Tissue and Organ Culture, 66, 121–131.
Mozsár J, Viczián O. 1996. Genotype effect on somatic embryogenesis and plant regeneration of Vitis spp. Vitis, 35, 155–157.
Mozsár J, Viczián O, Süle S. 1998. Agrobacterium-mediated genetic transformation of an interspecific grapevine. Vitis, 37, 127–130.
Mullins M G, Archie Tang F C, Facciotti D. 1990. Agrobacterium-mediated genetic transformation of grapevines: Transgenic plants of Vitis rupestris Scheele and buds of Vitis vinifera L. Nature Biotechnology, 8, 1041–1045.
Mullins M G, Srinivasan C. 1976. Somatic embryos and plantlets from an ancient clone of the grapevine (cv. Cabernet-Sauvignon) by apomixis in vitro. Journal of Experimental Botany, 27, 1022–1030.
Mulwa R M S, Norton M A, Farrand S K, Skirvin R M. 2007. Agrobacterium-mediated transformation and regeneration of transgenic ‘Chancellor’ wine grape plants expressing the tfdA gene. Vitis, 46, 110–115.
Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–497.
Nakajima I, Ban Y, Azuma A, Onoue N, Moriguchi T, Yamamoto T, Toki S, Endo M. 2017. CRISPR/Cas9-mediated targeted mutagenesis in grape. PLoS ONE, 12, e0177966.
Nakajima I, Endo M, Haji T, Moriguchi T, Yamamoto T. 2020. Embryogenic callus induction and Agrobacterium-mediated genetic transformation of ‘Shine Muscat’ grape. Plant Biotechnology, 37, 185–194.
Nakajima I, Matsuta N. 2003. Somatic embryogenesis from filaments of Vitis vinifera L. and Vitis labruscana Bailey. Vitis, 42, 53–54.
Nakano M, Hoshino Y, Mii M. 1994. Regeneration of transgenic plants of grapevine (Vitis Vinifera L.) via Agrobacterium rhizogenes-mediated transformation of embryogenic calli. Journal of Experimental Botany, 45, 649–656.
Nalwade A R, Shitole M G. 2004. Somatic embryogenesis in grape (Vitis vinifera L.) cv. Tas-A-Ganesh from leaf explants. Indian Journal of Plant Physiology, 9, 395–401.
Nicholson K L, Tarlyn N, Armour T, Swanson M E, Dhingra A. 2012. Effect of phyllotactic position and cultural treatments toward successful direct shoot organogenesis in dwarf ‘Pixie’ grapevine (Vitis vinifera L.). Plant Cell, Tissue and Organ Culture, 111, 123–129.
Nirala N K, Das D K, Srivastava P S, Sopory S K, Upadhyaya K C. 2010. Expression of a rice chitinase gene enhances antifungal potential in transgenic grapevine (Vitis vinifera L.). Vitis, 49, 181–187.
Nitsch J P, Nitsch C. 1969. Haploid plants from pollen grains. Science, 163, 85–87.
Nookaraju A, Agrawal D C. 2012. Enhanced tolerance of transgenic grapevines expressing chitinase and β-1,3-glucanase genes to downy mildew. Plant Cell, Tissue and Organ Culture, 111, 15–28.
Nookaraju A, Agrawal D C. 2013. Use of amino acids for a highly efficient somatic embryogenesis in grapevine ‘Crimson Seedless’. Vitis, 52, 137–140.
Osakabe Y, Liang Z, Ren C, Nishitani C, Osakabe K, Wada M, Komori S, Malnoy M, Velasco R, Poli M, Jung M H, Koo O J, Viola R, Kanchiswamy C N. 2018. CRISPR-Cas9-mediated genome editing in apple and grapevine. Nature Protocols, 13, 2844–2863.
Park H J, Lee H R, Pyee J, Cha H C. 2001. Regeneration of grape (Vitis labruscana cv. Kyoho) by shoot-tip culture. Journal of Plant Biology, 44, 185–192.
Passos I R S, Appezzato-da-Glória B, Vieira M L C. 1999. Embryogenic responses of Vitis spp.: Effects of genotype and polyvinylpyrrolidone. Vitis, 38, 47–50.
Peiró R, Gammoudi N, Yuste A, Olmos A, Gisbert C. 2015. Mature seeds for in vitro sanitation of the Grapevine leafroll associated virus (GLRaV-1 and GLRaV-3) from grape (Vitis vinifera L.). Spanish Journal of Agricultural Research, 13, e1005.
Perl A, Lotan O, Abu-Abied M, Holland D. 1996. Establishment of an Agrobacterium-mediated transformation system for grape (Vitis vinifera L.): The role of antioxidants during grape-Agrobacterium interactions. Nature Biotechnology, 14, 624–628.
Perl A, Saad S, Sahar N, Holland D. 1995. Establishment of long term embryogenic cultures of seedless Vitis vinifera cultivars - A synergistic effect of auxins and the role of abscisic acid. Plant Science, 104, 193–200.
Péros J P, Torregrosa L, Berger G. 1998. Variability among Vitis vinifera cultivars in micropropagation, organogenesis and antibiotic sensitivity. Journal of Experimental Botany, 49, 171–179.
Perrin M, Martin D, Joly D, Demangeat G, This P, Masson J E. 2001. Medium-dependent response of grapevine somatic embryogenic cells. Plant Science, 161, 107–116.
Pessina S, Lenzi L, Perazzolli M, Campa M, Dalla Costa L, Urso S, Valè G, Salamini F, Velasco R, Malnoy M. 2016. Knockdown of MLO genes reduces susceptibility to powdery mildew in grapevine. Horticulture Research, 3, 16016.
Pinto-Sintra A L. 2007. Establishment of embryogenic cultures and plant regeneration in the Portuguese cultivar ‘Touriga Nacional’ of Vitis vinifera L. Plant Cell, Tissue and Organ Culture, 88, 253–265.
Prado M J, Grueiro M P, González M V, Testillano P S, Domínguez C, López M, Rey M. 2010. Efficient plant regeneration through somatic embryogenesis from anthers and ovaries of six autochthonous grapevine cultivars from Galicia (Spain). Scientia Horticulturae, 125, 342–352.
Ren C, Liu X, Zhang Z, Wang Y, Duan W, Li S, Liang Z. 2016. CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Scientific Reports, 6, 32289.
Sabbadini S, Capriotti L, Limera C, Navacchi O, Tempesta G, Mezzetti B. 2019a. A plant regeneration platform to apply new breeding techniques for improving disease resistance in grapevine rootstocks and cultivars. BIO Web of Conferences, 12, 01019.
Sabbadini S, Capriotti L, Molesini B, Pandolfini T, Navacchi O, Limera C, Ricci A, Mezzetti B. 2019b. Comparison of regeneration capacity and Agrobacterium-mediated cell transformation efficiency of different cultivars and rootstocks of Vitis spp. via organogenesis. Scientific Reports, 9, 582.
Salunkhe C K, Rao P S, Mhatre M. 1997. Induction of somatic embryogenesis and plantlets in tendrils of Vitis vinifera L. Plant Cell Reports, 17, 65–67.
Sanjurjo L, Vidal J R, Segura A, de la Torre F. 2013. Genetic transformation of grapevine cells using the minimal cassette technology: The need of 3´-end protection. Journal of Biotechnology, 163, 386–390.
Santos-Rosa M, Poutaraud A, Merdinoglu D, Mestre P. 2008. Development of a transient expression system in grapevine via agro-infiltration. Plant Cell Reports, 27, 1053–1063.
Saporta R, de la Torre F, Segura A, Vidal J R. 2014. Toxic effect of antibiotics in grapevine (Vitis vinifera ‘Albariño’) for embryo emergence and transgenic plant regeneration from embryogenic cell suspension. Vitis, 53, 89–94.
Saporta R, San Pedro T, Gisbert C. 2016. Attempts at grapevine (Vitis vinifera L.) breeding through genetic transformation: The main limiting factors. Vitis, 55, 173–186.
Scorza R, Cordts J M, Gray D J, Gonsalves D, Emershad R L, Ramming D W. 1996. Producing transgenic ‘Thompson Seedless’ grape (Vitis vinifera L.) plants. Journal of the American Society for Horticultural Science, 121, 616–619.
Scorza R, Cordts J M, Ramming D W, Emershad R L. 1995. Transformation of grape (Vitis vinifera L.) zygotic-derived somatic embryos and regeneration of transgenic plants. Plant Cell Reports, 14, 589–592.
Soliman H I A. 2018. Production of genetically modified grape (Vitis vinifera L.) plants. International journal of Horticulture, Agriculture and Food science, 2, 111–120.
Stamp J A, Colby S M, Meredith C P. 1990a. Direct shoot organogenesis and plant regeneration from leaves of grape (Vitis spp.). Plant Cell, Tissue and Organ Culture, 22, 127–133.
Stamp J A, Colby S M, Meredith C P. 1990b. Improved shoot organogenesis from leaves of grape. Journal of the American Society for Horticultural Science, 115, 1038–1042.
Su H, Jiao Y T, Wang F F, Liu Y E, Niu W L, Liu G T, Xu Y. 2018. Overexpression of VpPR10.1 by an efficient transformation method enhances downy mildew resistance in V. vinifera. Plant Cell Reports, 37, 819–832.
Tang F A, Mullins M G. 1990. Adventitious bud formation in leaf explants of some grapevine rootstock and scion cultivars. Vitis, 29, 151–158.
Torregrosa L, Bouquet A. 1996. Adventitious bud formation and shoot development from in vitro leaves of Vitis×Muscadinia hybrids. Plant Cell, Tissue and Organ Culture, 45, 245–252.
Torregrosa L, Bouquet A. 1997. Agrobacterium rhizogenes and A. tumefaciens co-transformation to obtain grapevine hairy roots producing the coat protein of grapevine chrome mosaic nepovirus. Plant Cell, Tissue and Organ Culture, 49, 53–62.
Torregrosa L, Iocco P, Thomas M R. 2002. Influence of Agrobacterium strain, culture medium, and cultivar on the transformation efficiency of Vitis vinifera L. American Journal of Enology and Viticulture, 53, 183–190.
Tu M, Wang X, Yin W, Wang Y, Li Y, Zhang G, Li Z, Song J, Wang X. 2020. Grapevine VlbZIP30 improves drought resistance by directly activating VvNAC17 and promoting lignin biosynthesis through the regulation of three peroxidase genes. Horticulture Research, 7, 150.
Tvorogova V E, Fedorova Y A, Potsenkovskaya E A, Kudriashov A A, Efremova E P, Kvitkovskaya V A, Wolabu T W, Zhang F, Tadege M, Lutova L A. 2019. The WUSCHEL-related homeobox transcription factor MtWOX9-1 stimulates somatic embryogenesis in Medicago truncatula. Plant Cell, Tissue and Organ Culture, 138, 517–527.
Vidal J R, Kikkert J R, Donzelli B D, Wallace P G, Reisch B I. 2006a. Biolistic transformation of grapevine using minimal gene cassette technology. Plant Cell Reports, 25, 807–814.
Vidal J R, Kikkert J R, Malnoy M A, Wallace P G, Barnard J, Reisch B I. 2006b. Evaluation of transgenic ‘Chardonnay’ (Vitis vinifera) containing magainin genes for resistance to crown gall and powdery mildew. Transgenic Research, 15, 69–82.
Vidal J R, Kikkert J R, Wallace P G, Reisch B I. 2003. High-efficiency biolistic co-transformation and regeneration of ‘Chardonnay’ (Vitis vinifera L.) containing npt-II and antimicrobial peptide genes. Plant Cell Reports, 22, 252–260.
Vidal J R, Rama J, Taboada L, Martin C, Ibañez M, Segura A, González-Benito M E. 2009. Improved somatic embryogenesis of grapevine (Vitis vinifera) with focus on induction parameters and efficient plant regeneration. Plant Cell, Tissue and Organ Culture, 96, 85–94.
Wan D Y, Guo Y, Cheng Y, Hu Y, Xiao S Y, Wang Y J, Wen Y Q. 2020. CRISPR/Cas9-mediated mutagenesis of VvMLO3 results in enhanced resistance to powdery mildew in grapevine (Vitis vinifera). Horticulture Research, 7, 116.
Wang H, Wang W, Zhan J, Huang W, Xu H. 2015. An efficient PEG-mediated transient gene expression system in grape protoplasts and its application in subcellular localization studies of flavonoids biosynthesis enzymes. Scientia Horticulturae, 191, 82–89.
Wang Q, Li P, Hanania U, Sahar N, Mawassi M, Gafny R, Sela I, Tanne E, Perl A. 2005. Improvement of Agrobacterium-mediated transformation efficiency and transgenic plant regeneration of Vitis vinifera L. by optimizing selection regimes and utilizing cryopreserved cell suspensions. Plant Science, 168, 565–571.
Wang X, Tu M, Li Z, Wang Y, Wang X. 2018a. Current progress and future prospects for the clustered regularly interspaced short palindromic repeats (CRISPR) genome editing technology in fruit tree breeding. Critical Reviews in Plant Sciences, 37, 233–258.
Wang X, Tu M, Wang D, Liu J, Li Y, Li Z, Wang Y, Wang X. 2018b. CRISPR/Cas9-mediated efficient targeted mutagenesis in grape in the first generation. Plant Biotechnology Journal, 16, 844–855.
Wu J, Zhang Y, He R, Zhu L, Wang C, Xu X, Lu J. 2012. Optimization of transformation efficiency of suspension cultured Vitis vinifera cv. Chardonnay embryogenic cells. Journal of Integrative Agriculture, 11, 387–396.
Xie X, Agüero C B, Wang Y, Andrew Walker M. 2016. Genetic transformation of grape varieties and rootstocks via organogenesis. Plant Cell, Tissue and Organ Culture, 126, 541–552.
Xu W, Ma F, Li R, Zhou Q, Yao W, Jiao Y, Zhang C, Zhang J, Wang X, Xu Y, Wang Y. 2019. VpSTS29/STS2 enhances fungal tolerance in grapevine through a positive feedback loop. Plant, Cell & Environment, 42, 2979–2998.
Xu Z S, Yu Z Y, Zhang M, Zhang Z, Tao J M. 2014. Plant regeneration via somatic embryogenesis from solid and suspension cultures of Vitis vinifera L. cv. ‘Manicure Finger’. In Vitro Cellular & Developmental Biology - Plant, 50, 249–256.
Zhang P, Yu Z Y, Cheng Z M, Zhang Z, Tao J M. 2011. In vitro explants regeneration of the grape ‘Wink’ (Vitis vinifera L. ‘Wink’). Journal of Plant Breeding and Crop Science, 3, 276–282.
Zhao F L, Li Y J, Hu Y, Gao Y R, Zang X W, Ding Q, Wang Y J, Wen Y Q. 2016. A highly efficient grapevine mesophyll protoplast system for transient gene expression and the study of disease resistance proteins. Plant Cell, Tissue and Organ Culture, 125, 43–57.
Zhou Q, Dai L, Cheng S, He J, Wang D, Zhang J, Wang Y. 2014. A circulatory system useful both for long-term somatic embryogenesis and genetic transformation in Vitis vinifera L. cv. Thompson Seedless. Plant Cell, Tissue and Organ Culture, 118, 157–168.
Zottini M, Barizza E, Costa A, Formentin E, Ruberti C, Carimi F, Lo Schiavo F. 2008. Agroinfiltration of grapevine leaves for fast transient assays of gene expression and for long-term production of stable transformed cells. Plant Cell Reports, 27, 845–853.