Advertisement

Grape Biotechnology: Past, Present, and Future

  • Humberto PrietoEmail author
  • María Miccono
  • Carlos Aguirre
  • Evelyn Sánchez
  • Álvaro Castro
Chapter
  • 185 Downloads
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Genetic improvement of grapevine relies on conventional breeding and genetic engineering, but the latter often seems far from having a significant impact. A small but important difference with previous breeding efforts is that, today, genome studies and technology advances in grapevine genetic engineering have become available in such a way that new varieties can be developed that are compatible with market challenges. Since the completion of the first reference grapevine genome sequence, relevant information has been gathered that allows for the identification of novel genes, analysis of structural gene variants, and discovery of SNPs. Also, regulatory regions for coding sequences, analyses of small RNA populations, and modulation processes coupled to DNA modification (i.e., methylations) have started to be elucidated, thereby enabling the New Breeding Techniques (NBTs), also referred to as precision breeding. RNA interference (RNAi) and RNA-guided editing of genomes are among the most promising new techniques for RNA-based systems that affect gene expression. Also, both RNAi and RNA-guided editing of DNA are expanding technical platforms by which DNA methylation can also be proposed, thus adding possibilities for epigenetic regulation. Here, we will present and discuss advances in gene transfer procedures from a NBTs’ perspective. We will use a chronological arrangement of gene transfer experimentation carried out over the last 10 years as a complementary view to recent excellent works already available. Also, our experience in the use of the editing systems will be introduced.

Keywords

RNA interference Genome editing CRISPR-Cas Grape in vitro culture New Breeding Techniques 

References

  1. Álvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous efficient and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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 47:251–252Google Scholar
  3. An C, Orbović V, Mou Z (2013) An efficient intragenic vector for generating intragenic and cisgenic plants in Citrus. Am J Plant Sci 4:2131–2137CrossRefGoogle Scholar
  4. Aparicio-Prat E, Arnan C, Sala I, Bosch N, Guigo R, Johnson R (2015) DECKO: single-oligo, dual-CRISPR deletion of genomic elements including long non-coding RNAs. BMC Genom 16:846CrossRefGoogle Scholar
  5. Baltes NJ, Gil-Humanes J, Čermák T, Atkins PA, Voytas DF (2014) DNA replicons for plant genome engineering. Plant Cell 26:151–163.  https://doi.org/10.1105/tpc.113.119792CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297CrossRefGoogle Scholar
  7. Baumann K (2017) Genome editing: CRISPR–Cas becoming more human. Nat Rev Mol Cell Biol 18:591PubMedCrossRefGoogle Scholar
  8. Belli-Kullan J, Lopes Paim Pinto D, Bertolini E, Fasoli M, Battista Tornielli G, Pezzotti M, Meyers BC, Farina L, Zenoni S, Pè ME, Mica E (2015) miRVine: a microRNA expression atlas of grapevine based on small RNA sequencing. BMC Genom 16:393.  https://doi.org/10.1186/s12864-015-1610-5CrossRefGoogle Scholar
  9. Bertazzon N, Castiglioni C, Angelini E, Raiola A, Gardiman M, Borgo M, Ferrari S (2012) Transient silencing of the grapevine gene VvPGIP1 by agroinfiltration with a construct for RNA interference. Plant Cell Rep 31:133–143.  https://doi.org/10.1007/s00299-011-1147-2CrossRefPubMedGoogle Scholar
  10. Brazelton VA, Zarecor S, Wright DA, Wang Y, Liu J, Chen K, Yang B, Lawrence-Dill CJ (2015) A quick guide to CRISPR sgRNA design tools. GM Crops Food 6:266–276PubMedCrossRefGoogle Scholar
  11. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280PubMedCrossRefGoogle Scholar
  12. 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. Sci Hortic 204:123–127CrossRefGoogle Scholar
  13. Castro Á, Quiroz D, Sánchez E, Miccono M, Aguirre C, Ramírez A, Montes C, Prieto H (2016) Synthesis of an artificial Vitis vinifera miRNA 319e using overlapping long primers and its application for gene silencing. J Biotechnol 233:200–210.  https://doi.org/10.1016/j.jbiotec.2016.06.028CrossRefPubMedGoogle Scholar
  14. Čermák T, Belanto JJ, Curtin SJ, Starker CG, Gil-Humanes J, Mathre JW, Cegan R, Greenstein RL, Kono TJY, Koneĉná E, Voytas DF (2017) A multipurpose toolkit to enable advanced genome engineering in plants. Plant Cell 29:1196–1217PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chialva C, Muñoz C, Miccono M, Eichler E, Calderón L, Prieto H, Lijavetzky D (2018) Differential expression patterns within the grapevine stilbene synthase gene family revealed through their regulatory regions. Plant Mol Biol Rep 36:225–238.  https://doi.org/10.1007/s11105-018-1073-3CrossRefGoogle Scholar
  16. Chong J, Piron M-C, Meyer S, Merdinoglu D, Bertsch C, Mestre P (2014) The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. J Exp Bot 65:6589–6601CrossRefGoogle Scholar
  17. Conner A, Barrell P, Baldwin S, Lokerse A, Cooper P, Erasmuson A, Nap JP, Jacobs J (2007) Intragenic vectors for gene transfer without foreign DNA. Euphytica 154:341–353CrossRefGoogle Scholar
  18. Cox DBT, Gootenberg JS, Abudayyeh OO, Franklin B, Kellner MJ, Joung J, Zhang F (2017) RNA editing with CRISPR-Cas13. Science 358:1019–1027.  https://doi.org/10.1126/science.aaq0180CrossRefPubMedPubMedCentralGoogle Scholar
  19. Culianez-Macia FA, Hepburn A (1988) Right-border sequences enable the left border of an Agrobacterium tumefaciens nopaline Ti-plasmid to produce single-stranded DNA. Plant Mol Biol 11:389–399PubMedCrossRefGoogle Scholar
  20. Czarnecka E, Key JL, Gurley WB (1989) Regulatory domains of the Gmhsp17.5-E heat shock promoter of soybean. Mol Cell Biol 9:3457–3463PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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 49:201–208Google Scholar
  22. 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 Organ Cult 124:471–481CrossRefGoogle Scholar
  23. Demirci Y, Zhang B, Unver T (2017) CRISPR/Cas9: an RNA-guided highly precise synthetic tool for plant genome editing. J Cell Physiol 233:1844–1859PubMedCrossRefPubMedCentralGoogle Scholar
  24. Dhekney SA, Li ZT, Gray DJ (2011) Grapevines engineered to express cisgenic Vitis vinifera thaumatin-like protein exhibit fungal disease resistance. Vitro Cell Dev Biol Plant 47:458–466CrossRefGoogle Scholar
  25. Devers EA, Teply J, Reinert A, Gaude N, Krajinski F (2013) An endogenous artificial microRNA system for unraveling the function of root endosymbioses related genes in Medicago truncatula. BMC Plant Biol 13:82.  https://doi.org/10.1186/1471-2229-13-82CrossRefPubMedPubMedCentralGoogle Scholar
  26. Doench JG, Hartenian E, Graham DB, Tothova Z, Hegde M, Smith I, Sullender M, Ebert BL, Xavier RJ, Root DE (2014) Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat Biotechnol 32:1262–1267PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fehér A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta 1849:385–402PubMedCrossRefGoogle Scholar
  28. Fire A, Xu S, Montgomery M, Kostas S, Driver S, Mello C (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811PubMedCrossRefGoogle Scholar
  29. Fontes N, Gerós H, Papadakis AK, Delrot S, Roubelakis-Angelakis KA (2010) Isolation and use of protoplasts from grapevine tissues. In: Delrot S, Medrano H, Or E, Bavaresco L, Grando S (eds) Methodologies and results in grapevine research. Springer, Dordrecht.  https://doi.org/10.1007/978-90-481-9283-0_18CrossRefGoogle Scholar
  30. Gaj T, Gersbach CA, Barbas CF III (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405.  https://doi.org/10.1016/j.tibtech.2013.04.004CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gelvin S (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51:223–256PubMedCrossRefGoogle Scholar
  32. Gray DJ, Dhekney SA, Li ZT, Cordts JM (2011) Genetic engineering of grapevine and progress toward commercial deployment. In: Mou B, Scorza R (eds) Transgenic horticultural crops, challenges and opportunities. CRC Press, Boca Raton, pp 317–331CrossRefGoogle Scholar
  33. Hart T, Chandrashekhar M, Aregger M, Steinhart Z, Brown KR, MacLeod G, Mis M, Zimmermann M, Fradet-Turcotte A, Sun S, Mero P, Dirks P, Sidhu S, Roth FP, Rissland OS, Durocher D, Angers S, Moffat J (2015) High-resolution CRISPR screens reveal fitness genes and genotype-specific cancer liabilities. Cell 163:1515–1526.  https://doi.org/10.1016/j.cell.2015.11.015CrossRefPubMedPubMedCentralGoogle Scholar
  34. Ho TT, Zhou N, Huang J, Koirala P, Xu M, Fung R, Wu F, Mo YY (2015) Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines. Nucleic Acids Res 43(3):e17PubMedCrossRefGoogle Scholar
  35. Holme IWT (2013) Intragenesis and cisgenesis as alternatives to transgenic crop development. Plant Biotechnol J 11:395–407PubMedCrossRefPubMedCentralGoogle Scholar
  36. Incarbone M, Dunoyer B (2013) RNA silencing and its suppression: novel insights from in plant analyses. Trends Plant Sci 18:382–392PubMedCrossRefGoogle Scholar
  37. Jelly NS, Valat L, Walter B, Maillot P (2014) Transient expression assays in grapevine: a step towards genetic improvement. Plant Biotechnol J 12:1231–1245.  https://doi.org/10.1111/pbi.12294CrossRefPubMedPubMedCentralGoogle Scholar
  38. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pè ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quétier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467.  https://doi.org/10.1038/nature06148CrossRefPubMedPubMedCentralGoogle Scholar
  39. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821.  https://doi.org/10.1126/science.1225829CrossRefPubMedPubMedCentralGoogle Scholar
  40. Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–424PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kovalenko PG, Schuman NV (1997) Biotechnological advances of electroporation of grapevine and sugar beet cells. Bioelectrochem Bioenerg 43:165–168CrossRefGoogle Scholar
  42. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kurth EG, Peremyslov VV, Prokhnevsky AI, Kasschau KD, Miller M, Dolja VV (2012) Virus-derived gene expression and RNA interference vector for grapevine. J Virol 86:6002–6009PubMedPubMedCentralCrossRefGoogle Scholar
  44. Lee LY, Gelvin SB (2008) T-DNA binary vectors and systems. Plant Physiol 146:325–332.  https://doi.org/10.1104/pp.107.113001CrossRefPubMedPubMedCentralGoogle Scholar
  45. Li ZT, Kim KH, Dhekney SA, Jasinski JR, Creech MR, Gray DJ (2014) An optimized procedure for plant recovery from somatic embryos significantly facilitates the genetic improvement of Vitis. Hortic Res 1:14027–14033.  https://doi.org/10.1038/hortres.2014.27CrossRefPubMedPubMedCentralGoogle Scholar
  46. Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from a 3’-end uridylation activity in Arabidopsis. Curr Biol 15:1501–1507PubMedPubMedCentralCrossRefGoogle Scholar
  47. Lyznik LA, Gordon-Kamm WJ, Tao Y (2003) Site-specific recombination for genetic engineering in plants. Plant Cell Rep 21:925–932.  https://doi.org/10.1007/s00299-003-0616-7CrossRefPubMedGoogle Scholar
  48. Malabarba J, Buffon V, Mariath JEA, Maraschin FS, Margis-Pinheiro M, Pasquali G, Revers LF (2018) Manipulation of VviAGL11 expression changes the seed content in grapevine (Vitis vinifera L.). Plant Sci 269:126–135PubMedCrossRefPubMedCentralGoogle Scholar
  49. Malnoy M, Viola R, Jung M-H, Koo O-J, Kim S, Kim J-S, Velasco R, Kanchiswamy CN (2016) DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front Plant Sci 7:1904.  https://doi.org/10.3389/fpls.2016.01904CrossRefPubMedPubMedCentralGoogle Scholar
  50. Martinelli L, Bragagna P, Poletti V, Scienza A (1993) Somatic embryogenesis from leaf- and petiole-derived callus of Vitis rupestris. Plant Cell Rep 12:207–210PubMedCrossRefGoogle Scholar
  51. Martinelli L, Gribaudo I (2001) Somatic embryogenesis in grapevine. In: Roubelakis-Angelakis KA (ed) Molecular biology and biotechnology of the grapevine. Kluwer Academic Publishers, Dordrecht, pp 393–410Google Scholar
  52. Martinelli L, Dalla Costa L, Vaccari I, Poletti V, Gribaudo I, Gambino I, Guzzo F, Saldarelli P, Minafra A, Turturo C (2009) Application of a site-specific DNA excision strategy for marker gene removal during gene transfer in Vitis spp. Acta Hortic 827:399–403CrossRefGoogle Scholar
  53. Merz PR, Moser T, Höll J, Kortekamp A, Buchholz G, Zyprian E, Bogs J (2015) The transcription factor VvWRKY33 is involved in the regulation of grapevine (Vitis vinifera) defense against the oomycete pathogen Plasmopara viticola. Physiol Plant 153:365–380PubMedCrossRefGoogle Scholar
  54. Miccono MA, Madrid G, Aguirre C, Olivares F, Olmedo B, Mora R, Sánchez E, Quiroz D, Prieto H (2018) DNA replicon-mediated genome editing in grapevine using CRISPR/Cas9 and a paired gRNA strategy. In: Plant biology conference, Montreal, Québec, Canada, July 14–18Google Scholar
  55. Mojica FJ, Díez-Villaseñor C, Soria E, Juez G (2000) Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol 36:244–246PubMedCrossRefGoogle Scholar
  56. Molnar A, Bassett A, Thuenemann E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J 58:165–174.  https://doi.org/10.1111/j.1365-313X.2008.03767.xCrossRefPubMedGoogle Scholar
  57. Montes C, Castro Á, Barba P, Rubio J, Sánchez E, Carvajal D, Aguirre C, Tapia E, Dell Orto P, Decroocq V, Prieto H (2014) Differential RNAi responses of Nicotiana benthamiana individuals transformed with a hairpin-inducing construct during Plum pox virus challenge. Virus Genes 49:325–338.  https://doi.org/10.1007/s11262-014-1093-5CrossRefPubMedGoogle Scholar
  58. Mullins M, Srinivasan C (1976) Somatic embryos and plantlets from an ancient clone of grapevine (cv. Cabernet-Sauvignon) by apomixes in vitro. J Exp Bot 27:1022–1030CrossRefGoogle Scholar
  59. 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(5):e0177966.  https://doi.org/10.1371/journal.pone.0177966CrossRefPubMedPubMedCentralGoogle Scholar
  60. Nielsen K (2003) Transgenic organisms: time for conceptual diversification? Nat Biotechnol 21:227–228PubMedCrossRefGoogle Scholar
  61. Nødvig CS, Nielsen JB, Kogle ME, Mortensen UH (2015) A CRISPR-Cas9 system for genetic engineering of filamentous fungi. PLoS ONE 10(7):e0133085PubMedPubMedCentralCrossRefGoogle Scholar
  62. Nunan KJ, Sims IM, Bacic A, Robinson SP, Fincher GB (1997) Isolation and characterization of cell walls from the mesocarp of mature grape berries (Vitis vinifera). Planta 203(1):93–100.  https://doi.org/10.1007/s004250050169CrossRefGoogle Scholar
  63. Oláh R, Zok A, Pedryc A, Howard S, Kovács LA (2009) Somatic embryogenesis in a broad spectrum of grape genotypes. Sci Hortic 120:134–137CrossRefGoogle Scholar
  64. Ow DW (2007) GM maize from site-specific recombination technology, what next? Curr Opin Biotechnol 18:115–120PubMedCrossRefGoogle Scholar
  65. Papadakis AK, Siminis CI, Roubelakis-Angelakis KA (2001) Reduced activity of antioxidant machinery is correlated with suppression of totipotency in plant protoplasts. Plant Physiol 126:434–444PubMedPubMedCentralCrossRefGoogle Scholar
  66. Papadakis A, Fontes N, Gerós H, Roubelakis-Angelakis K (2009) Progress in grapevine protoplast technology. In: Roubelakis-Angelakis KA (ed) Grapevine molecular physiology & biotechnology. Springer, DordrechtGoogle Scholar
  67. 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. Hortic Res 3:16016–16024.  https://doi.org/10.1038/hortres.2016.16CrossRefPubMedPubMedCentralGoogle Scholar
  68. Priyam A, Woodcroft BJ, Rai V, Munagala A, Moghul I, Ter F, Gibbins MA, Moon H, Leonard G, Rumpf W, Wurm Y (2015). Sequenceserver: a modern graphical user interface for custom BLAST databases. bioRxiv 033142.  https://doi.org/10.1101/033142
  69. Pulido-Quetglas C, Aparicio-Prat E, Arnan C, Polidori T, Hermoso T, Palumbo E, Ponomarenko E, Guigo R, Johnson R (2017) Scalable design of paired CRISPR guide RNAs for genomic deletion. PLoS Comput Biol 13(3):e1005341.  https://doi.org/10.1371/journal.pcbi.1005341CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rajasekaran K, Mullins M (1983) Influence of genotype and sex-expression on formation of plantlets by cultured anthers of grapevines. Agronomie 3:233–238CrossRefGoogle Scholar
  71. Ren C, Liu X, Zhang Z, Wang Y, Duan W, Liang Z (2016) CRISPR/Cas9-mediated efficient targeted mutagenesis in Chardonnay (Vitis vinifera L.). Sci Rep 6:32289.  https://doi.org/10.1038/srep32289CrossRefPubMedPubMedCentralGoogle Scholar
  72. Reustle G, Harst M, Alleweldt G (1995) Plant regeneration of grapevine (Vitis sp.) protoplasts isolated from embryogenic tissue. Plant Cell Rep 15:238–241PubMedCrossRefGoogle Scholar
  73. Rommens CM, Humara JM, Ye J, Yan H, Richael C, Zhang L, Perry R, Swords K (2004) Crop improvement through modification of the plant’s own genome. Plant Physiol 135:421–431PubMedPubMedCentralCrossRefGoogle Scholar
  74. Rommens CM, Bougri O, Yan H, Humara JM, Owen J, Swords K, Ye J (2005) Plant-derived transfer DNAs. Plant Physiol 139:1338–1349PubMedPubMedCentralCrossRefGoogle Scholar
  75. Romon M, Soustre-Gacougnolle I, Schmitt C, Perrin M, Chevalier E, Mutterer J, Himber C, Zervudacki J, Burdloff Y, Montavon T, Zimmermann A, Elmayan T, Vaucheret H, Dunoyer P, Masson JE (2013) RNA silencing is resistant to low-temperature in grapevine. PLoS ONE 8(12):e82652.  https://doi.org/10.1371/journal.pone.0082652CrossRefPubMedPubMedCentralGoogle Scholar
  76. Rubio J, Montes C, Castro Á, Álvarez C, Olmedo B, Munoz M, Tapia E, Reyes F, Ortega M, Sánchez E, Miccono M, Dalla Costa L, Martinelli L, Malnoy M, Prieto H (2015) Genetically engineered thompson seedless grapevine plants designed for fungal tolerance: selection and characterization of the best performing individuals in a field trial. Transgenic Res 24:43–60PubMedCrossRefGoogle Scholar
  77. Salunkhe C, Rao P, Mhatre M (1997) Induction of somatic embryogenesis and plantlets in tendrils of Vitis vinifera L. Plant Cell Rep 17:65–67PubMedCrossRefGoogle Scholar
  78. Santos-Rosa M, Poutaraud A, Merdinoglu D, Mestre P (2008) Development of a transient expression system in grapevine via agro-infiltration. Plant Cell Rep 27:1053–1063PubMedCrossRefGoogle Scholar
  79. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343:84–87.  https://doi.org/10.1126/science.1247005CrossRefPubMedGoogle Scholar
  80. Shen B, Zhang W, Zhang J, Zhou J, Wang J, Chen L, Wang L, Hodgkins A, Iyer V, Huang X, Skarnes WC (2014) Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat Methods 11:399–402.  https://doi.org/10.1038/nmeth.2857CrossRefPubMedGoogle Scholar
  81. San Pedro T, Gammoudi N, Peiró R, Olmos A, Gisbert C (2017) Somatic embryogenesis from seeds in a broad range of Vitis vinifera L. varieties: rescue of true-to-type virus-free plants. Plant Biol 17:226.  https://doi.org/10.1186/s12870-017-1159-3CrossRefGoogle Scholar
  82. 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.  https://doi.org/10.5073/vitis.2016.55.173-186CrossRefGoogle Scholar
  83. Schouten HS, Krens FA, Jacobsen E (2006) Cisgenic plants are similar to traditionally bred plants: international regulations for genetically modified organisms should be altered to exempt cisgenesis. EMBO Rep 7:750–753PubMedPubMedCentralCrossRefGoogle Scholar
  84. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133PubMedPubMedCentralCrossRefGoogle Scholar
  85. Skinner ME, Uzilov AV, Stein LD, Mungall CJ, Holmes IH (2009) JBrowse: a next-generation genome browser. Genome Res 19:1630–1638.  https://doi.org/10.1101/gr.094607.109CrossRefPubMedPubMedCentralGoogle Scholar
  86. Taning CNT, Van Eynde B, Ma NYS, Smagghe G (2017) CRISPR/Cas9 in insects: applications, best practices and biosafety concerns. J Insect Physiol 18:245–257CrossRefGoogle Scholar
  87. Tapia E, Sequeida A, Castro Á, Montes C, Zamora P, López R, Acevedo F, Prieto H (2009) Development of grapevine somatic embryogenesis using an air-lift bioreactor as an efficient tool in the generation of transgenic plants. J Biotechnol 139:95–101.  https://doi.org/10.1016/j.jbiotec.2008.09.009CrossRefPubMedGoogle Scholar
  88. Terrier N, Torregrosa L, Ageorges A, Vialet S, Verrie C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 149:1028–1041PubMedPubMedCentralCrossRefGoogle Scholar
  89. Toro N, Datta A, Yanofsky M, Nester E (1988) Role of the overdrive sequence in T-DNA border cleavage in Agrobacterium. Proc Natl Acad Sci USA 85:8558–8562PubMedCrossRefGoogle Scholar
  90. Torregrosa L, Iocco P, Thomas MR (2002) Influence of Agrobacterium strain, culture medium, and cultivar on the transformation efficiency of Vitis vinifera L. Am J Enol Vitic 53:183–190Google Scholar
  91. Tzfira T, Citovsky V (2008) Agrobacterium: from biology to biotechnology, Springer edn. Springer, New YorkCrossRefGoogle Scholar
  92. Tzfira T, Li J, Lacroix B, Citovsky V (2004) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20:375–383PubMedCrossRefGoogle Scholar
  93. Valat L, Toutain S, Courtois N, Gaire F, Decout E, Pinck L, Mauro M, Burrus M (2000) GFLV replication in electroporated grapevine protoplasts. Plant Sci 155:203–212PubMedCrossRefGoogle Scholar
  94. Valat L, Fuchs M, Burrus M (2006) Transgenic grapevine rootstock clones expressing the coat protein or movement protein genes of grapevine fanleaf virus: characterization and reaction to virus infection upon protoplast electroporation. Plant Sci 170:739–747.  https://doi.org/10.1016/j.plantsci.2005.11.005CrossRefGoogle Scholar
  95. van Haaren MJ, Sedee NJ, Schilperoort RA, Hooykaas PJ (1987) Overdrive is a T-region transfer enhancer which stimulates T-strand production in Agrobacterium tumefaciens. Nucl Acids Res 15:8983–8997PubMedCrossRefGoogle Scholar
  96. Vazquez F, Legrand S, Windels D (2006) The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci 15:337–345CrossRefGoogle Scholar
  97. Vidal JR, Rama J, Taboada L, Martín C, Ibáñez M, Segura A, González-Benito ME (2009) Improved somatic embryogenesis of grapevine (Vitis vinifera) with focus on induction parameters and efficient plant regeneration. Plant Cell Tissue Organ Cult 96:85–94CrossRefGoogle Scholar
  98. Wang MB, Abbott DC, Waterhouse PM (2000) A single copy of a virus-derived transgene encoding hairpin RNA gives immunity to barley yellow dwarf virus. Mol Plant Pathol 1:347–356PubMedCrossRefGoogle Scholar
  99. Wang Q, Li P, Hanania U, Sahar N, Mawassi M, Gafny R, Selac I, Tannea E, Perlb 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 Sci 168:565–571CrossRefGoogle Scholar
  100. Wang HL, Wang W, Zhan JC, Huang WD, Xu HY (2015) An efficient PEG-mediated transient gene expression system in grape protoplasts and its application in subcellular localization studies of flavonoids biosynthesis enzymes. Sci Hortic 191:82–89.  https://doi.org/10.1016/j.scienta.2015.04.039CrossRefGoogle Scholar
  101. Wang X, Tu M, Wang D, Liu J, Li Y, Li Z, Wang X (2017) CRISPR/Cas9-mediated efficient targeted mutagenesis in grape in the first generation. Plant Biotechnol J 16:844–855.  https://doi.org/10.1111/pbi.12832CrossRefPubMedPubMedCentralGoogle Scholar
  102. Wang Y, Liu X, Ren C, Zhong G-Y, Yang L, Li S, Liang Z (2016) Identification of genomic sites for CRISPR/Cas9-based genome editing in the Vitis vinifera genome. BMC Plant Biol 16:96.  https://doi.org/10.1186/s12870-016-0787-3CrossRefPubMedPubMedCentralGoogle Scholar
  103. Warthmann N, Chen H, Ossowski S, Weigel D, Herve P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS ONE 3:e1829PubMedPubMedCentralCrossRefGoogle Scholar
  104. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA (2001) Construct design for efficient, effective and highthroughput gene silencing in plants. Plant J 27:581–590PubMedCrossRefGoogle Scholar
  105. Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771.  https://doi.org/10.1016/j.cell.2015.09.038CrossRefPubMedPubMedCentralGoogle Scholar
  106. 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 Organ Cult 125:43.  https://doi.org/10.1007/s11240-015-0928-7CrossRefGoogle Scholar
  107. 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 Organ Cult 118:157.  https://doi.org/10.1007/s11240-014-0471-yCrossRefGoogle Scholar
  108. Zhu Y-M, Hoshino Y, Nakano M, Takahashi E, Miia M (1997) Highly efficient system of plant regeneration from protoplasts of grapevine (Vitis vinifera L.) through somatic embryogenesis by using embryogenic callus culture and activated charcoal. Plant Sci 123:151–157.  https://doi.org/10.1016/S0168-9452(96)04557-8CrossRefGoogle Scholar
  109. 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 Rep 27:845–853.  https://doi.org/10.1007/s00299-008-0510-4CrossRefPubMedGoogle Scholar
  110. Zuo J, Niu QW, Geir Møller S, Chua NH (2001) Chemical-regulated, site-specific DNA excision in transgenic plants. Nat Biotechnol 19:157–161PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Humberto Prieto
    • 1
    Email author
  • María Miccono
    • 1
  • Carlos Aguirre
    • 1
  • Evelyn Sánchez
    • 2
  • Álvaro Castro
    • 3
  1. 1.Biotechnology Laboratory, La Platina StationInstituto de Investigaciones AgropecuariasLa PintanaChile
  2. 2.Doctoral Program in Integrative Genomics, Campus HuechurabaUniversidad MayorHuechurabaChile
  3. 3.Life Sciences Innovation CenterUniversity of California-Davis ChileProvidenciaChile

Personalised recommendations