A reliable protocol for the stable transformation of non-embryogenic cells cultures of grapevine (Vitis vinifera L.) and Taxus x media
Main Article Content
Keywords
Agrobacterium system, GFP, grapevine cell culture, resveratrol, stable transformation, Taxus cell cultures
Abstract
One of the major intent of metabolic engineering in cell culture systems is to increase yields of secondary metabolites. Efficient transformation methods are a priority to successfully apply metabolic engineering to cell cultures of plants that produce bioactive or therapeutic compounds, such as Vitis vinifera and Taxus x media. The aim of this study was to establish a reliable method to transform non-embryogenic cell cultures of these species. The V. vinifera cv. Gamay/cv. Monastrell cell lines and Taxus x media were used for Agrobacterium-mediated transformation using the Gateway-compatible Agrobacterium sp. binary vector system for fast reliable DNA cloning. The Taxus x media and Vitis cell lines were maintained in culture for more than 4 and 15 months, respectively, with no loss of reporter gene expression or antibiotic resistance. The introduced genes had no discernible effect on cell growth, or led to extracellular accumulation of phytoalexin trans-Resveratrol (t-R) in response to elicitation with methylated cyclodextrins (MBCD) and methyl jasmonate (MeJA) in the grapevine transgenic cell lines compared to the parental control. The method described herein provides an excellent tool to exploit exponentially growing genomic resources to enhance, optimize or diversify the production of bioactive compounds generated by grapevine and yew cell cultures, and offers a better understanding of many grapevine and yew biology areas.
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References
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2. Langcake P, Pryce RJ (1977) Production of resveratrol and viniferins by grapevines in response to UV irradiation. Phytochemistry 16:1193–6.
3. Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agr Food Chem 50:2731–41.
4. Pezet R, Cuenat P (1996) Resveratrol in wine: extraction from skin during fermentation and post-fermentation standing of must from Gamay grapes. Am J Enol Vitic 47:287–90.
5. Hall D, De Luca V (2007) Mesocarp localization of a bi-functional resveratrol/ hydroxycinnamic acid glucosyltransferase of Concord grape (Vitis lambrusca). Plant J 49:579–591.
6. Pezet R, Gindro K, Viret O, Richter H (2004) Effects of resveratrol, viniferins and pterostilbene on plasmopara viticola zoospore mobility and disease development. Vitis 43:145–8.
7. Bradamante S, Barenghi L, Villa A (2004) Cardiovascular protective effects of resveratrol. Cardiovasc Drug Rev. 22:169–88.
8. Le Corre L, Chalabi N, Delort L, Bignon YJ, Bernard-Gallon DJ (2005) Resveratrol and breast cancer chemoprevention: molecular mechanisms. Mol Nutr Food Res 49:462–471.
9. Wolter F, Ulrich S, Stein J (2004) Molecular mechanisms of the chemopreventive effects of resveratrol and its analogs in colorectal cancer: key role of polyamines. J Nutr 134:3219–22.
10. Ratan HL, Steward WP, Gescher AJ, Mellon JK (2002) Resveratrol a prostatecancer chemopreventive agent. Urol Oncol 7:223–7.
11. de la Lastra CA, Villegas I (2005) Resveratrol as an anti-inflammatory and anti-aging agent:mechanisms and clinical implications. Mol Nutr Food Res 49:405–30.
12. de la Lastra CA, Villegas I.(2007) Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem Soc T 35:1156–60.
13. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A et al. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337–42.
14. Kaeberlein M, Rabinovitch PS (2006) Medicine grapes versus gluttony. Nature 444:280–1.
15. Nakagawa K, Fukui H, Tabata M (1986) Hormonal regulation of berberine production in cell suspension cultures of thalictrum minus. Plant Cell Rep 5:69–71.
16. Christen AA, Gibson DM, Bland. J. Production of taxol or taxol-like compounds in cell culture. In: United States Patent 5019504; 1991.
17. Shimomura K, Sudo H, Saga H, Kamada H (1991) Shikonin production and secretion by hairy root cultures of lithospermum erythrorhizon. Plant Cell Rep 10:282–5.
18. Vanisree M, ChenYue L, ShuFung L, Nalawade SM, ChienYih L, HsinSheng T (2004) Studies on the production of some important secondary metabolites from medicinal plants by plant tissue cultures. Bot Bull Acad Sin 45:1–22.
19. Fernández-Pérez F, Almagro L, Pedreño MA, Gómez Ros LV (2013) Synergistic and cytotoxic action of indole alkaloids produced from elicited cell cultures of Catharanthus roseus. Pharm Biol 51:304-310.
20. Malik S, Cusidó RM, Mirjalili MH, Moyano E, Palazón J, Bonfill M (2011) Production of the anticancer drug taxol in Taxus baccata suspension cultures:A review. Process Biochemistry 46:23–34.
21. Bru R, Selles S, Casado-Vela,J, Belchi-Navarro S, Pedreño MA (2006) Modified cyclodextrins are chemically defined glucan inducers of defense responses in grapevine cell cultures. J Agric Food Chem 54:65–71.
22. Lijavetzky D, Almagro L, Belchi-Navarro S, Martínez-Zapater JM, Bru-Martinez R, Pedreño MA (2008) Synergistic effect of methyljasmonate and cyclodextrin on stilbene biosynthesis pathway gene expression and resveratrol production in Monastrell grapevine cell cultures. BMC Res Notes 1:132.
23. Martinez-Esteso MJ, Sellés-Marchart S, Vera-Urbina JC, Pedreño MA, Bru-Martinez R (2009) Changes of defense proteins in the extracellular proteome of grapevine (Vitis vinifera cv. Gamay) cell cultures in response to elicitors. J Proteomics 73:331–41.
24. Almagro L, Belchí-Navarro S, Sabater-Jara AB, Vera-Urbina JC, Selles-Marchart S, et al. (2013) Bioproduction of trans-resveratrol from grapevine cell cultures. In: Ramawat KG and Merillon JM, editors. Handbook of Natural Products. Heidelberg, Springer. 1683–1713.
25. Lim CG, Fowler ZL, Hueller T, Schaffer S, Koffas MAG (2011) High-Yield Resveratrol Production in Engineered Escherichia coli Appl. Environ. Microbiol. 77: 3451-3460.
26. Jeong YJ, An CH, Woo SG, Jeong HJ, Kim YM, Park SJ, Yoon BD, Kim CY (2014) Production of pinostilbene compounds by the expression of resveratrol O-methyltransferase genes in Escherichia coli. Enzyme Microb Technol. 54:8-14.
27. Wang Y, Bhuiya MW, Zhou R, Yu O (2014) Pterostilbene production by microorganisms expressing resveratrol O-methyltransferase. Annals of Microbiology
28. Mei YZ, Liu RX, Wang DP, Wang X, Dai CC (2015) Biocatalysis and biotransformation of resveratrol in microorganisms. Biotechnol Lett. 37(1):9-18.
29. Cusidó RM, Onrubia M, Sabater-Jara AB, Moyano E, Bonfill M, Goossens A, Pedreño MA, Palazon J (2014) A rational approach to improving the biotechnological production of taxanes in plant cell cultures of Taxus spp. Biotechnol Adv 32:1157–1167.
30. Chakrabarty R, Banerjee R, Chung SM, Farman M, Citovsky V, Hogenhout SA, Tzfira T, Goodin M (2007) PSITE vectors for stable integration or transient expression of autofluorescent protein fusions in plants: probing Nicotiana benthamiana-virus interactions. Mol Plant Microbe Interact 20:740-50.
31. Curtis MD, Grossniklaus U (2003) A Gateway TM cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiology 133:462-469.
32. Dubin MJ, Bowler C, Benvenuto G (2008) A modified Gateway cloning strategy for overexpressing tagged proteins in plants. Plant Methods 22:4-3.
33. Perl A, Lotan O, Abu-Abied M, Holland D (1996) Establishment of an Agrobacterium-mediated transformation system for grape (Vitis vilifera L.): The role of antioxidants during grape-Agrobacterium interations. Nature Biotecnology 14:596-624.
34. Vidal JR, Gomez C, Cutanda MC, Shrestha BR, Bouquet A, Thomas MR and Torregrosa L (2010) Use of gene transfer technology for functional studies in grapevine. Aust. J. Grape Wine Res. 16, 138–151.
35. Jelly NS, Valat L, Walter B, Maillot P (2014) Transient expression assays in grapevine: a step towards genetic improvement. Plant Biotechnol J. 12(9):1231-1245.
36. Das DK, Reddy MK, Upadhyaya KC, Sopory SK (2002) An efficient leaf-disc culture method for the regeneration via somatic embryogenesis and transformation of grape (Vitis vinifera L.). Plant Cell Rep 20:999–1005.
37. Iocco P, Franks T, Thomas MR (2000) Genetic transformation of major wine grape cultivars of Vitis vinifera L. Transgenic Research 10:105–112.
38. Dutt M, Li ZT, Dhekney SA, Gray DJ (2008) A co-transformation system to produce transgenic grapevines free of marker genes. Plant Sci 175:423–430.
39. Vandelle E, Poinssot B, Wendehenne D, Bentejac M, Alain P (2006) Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Mol Plant Microbe Interact 19:429–440.
40. Gago J, Grima-Pettenati J, Gallego PP (2011) Vascular-specific expression of GUS and GFP reporter genes in transgenic grapevine (Vitis vinifera L. cv. Albariño) conferred by the EgCCR promoter of Eucalyptus gunnii. Plant Physiol Biochem 49:413-419.
41. Gollop R, Even S, Colova-Tsolova V, Perl A (2002) Expression of the grape dihydroflavonol reductase gene and analysis of its promoter region. J Exp Bot 53 (373):1397-409.
42. Zapata JM, Calderon AA, Ros Barcelo A (1995) Peroxidase isoenzyme patterns in cell cultura derived from cotyledon, stem, leaf and fruit from grapevine (Vitis vinifera cv.Monastrell). Annals of Botany 75:443-448.
43. Cusidó RM, Palazón J, Navia-Osorio A, Mallol A, Bonfill M, Morales C, Piñol MT (1999) Production of taxol® and baccatine III by a selected Taxus baccata callus line and its derived cell suspension culture. Plant Sci 146:101–107.
44. Cusidó RM, Palazón J, Bonfill M, Navia-Osorio A, Morales C, Piñol MT (2002) Improved paclitaxel and baccatin III production in suspension cultures of Taxus x media. Biotechnol Prog 18:418–423.
45. Widholm JM (1972) The use fluorescein diacetate and phenosafranine for determining viability of cultured plant cells. Stain Technology 47(4):89-94.
46. Koncz C. and Schell J (1986) The promoter of T,-DNA gene Scontrols the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383-396.
47. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor, New York.
48. Maniatis T, Fritch EF, Sambrook J (1982) Molecular cloning: A laboratory manual. Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Batoko H, Zheng HQ, Hawes C, Moore I (2000) A Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201–2217.
50. Martínez-Esteso MJ, Sellés-Marchart S, Lijavetzky D, Pedreño M.A, Bru-Martínez R (2011) A DIGE-based quantitative proteomic analysis of grape berry flesh development and ripening reveals key events in sugar and organic acid metabolism. J Exp Bot 62:2521-2569.
51. Raghupathi RN, Diwan AM (1994) A protocol for protein estimation that gives a nearly constant color yield with simple proteins and nullifies the effects of four known interfering agents: microestimation of peptide groups. Anal Biochem 219:356−359.
52. Yenofsky RL, Fine M, Pellow JW (1990) A mutant neomycin phosphotransferase II gene reduces the resistance of transformants to antibiotic selection pressure. Proc Natl Acad Sci USA 87:3435-3439.
53. Colby SM, Meredith CP (1990) Kanamycin sensitivity of cultured tissues of Vitis. Plant Cell Rep 9: 237-240.
54. Torregrosa L, Lopez G, Bouquet A (2000) Antibiotic sensitivity of grapevine: a comparison between the effect of hygromycin and kanamycin on shoot development of transgenic 110 Richter rootstock (Vitis Berlandieri x Vitis rupestris) S. Afr. J. Enol. Vitic 21:32-39.
55. Saporta R, De La Torre F, Segura A, Vidal JR (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.
56. Ketchum REB, Wherland L, Croteau RB (2007) Stable transformation and long-term maintenance of transgenic Taxus cell suspension cultures. Plant Cell Rep 26:1025–1033.
57. Trick HN, Finer JJ (1997) SAAT: sonication-assisted Agrobacterium mediated transformation. Transgenic Res 6:329-336.
58. Martinez-Esteso MJ, Sellés-Marchart S, Vera-Urbina JC,Pedreño MA, Bru-Martinez R (2011) DIGE analysis of proteome changes accompanying large resveratrol production by grapevine (Vitis vinifera cv. Gamay) cell cultures in response to methyl-β-cyclodextrin and methyl jasmonate elicitors. J Proteomics. 74(8):1421-36.
59. Chandler SF and Sanchez C (2012) Genetic modification; the development of transgenic ornamental plant varieties. Plant Biotechnol J 10:891-903.
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Jun 24, 2015
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Martínez-Márquez A, Morante-Carriel J, Ramírez-Estrada K, Cusido R, Sellés-Marchart S, Palazon J, Pedreño MA, Bru-Martínez R. A reliable protocol for the stable transformation of non-embryogenic cells cultures of grapevine (Vitis vinifera L.) and Taxus x media. J Biol Methods [Internet]. 2015 Jun. 24 [cited 2024 Apr. 18];2(2):e21. Available from: https://jbmethods.org/index.php/jbm/article/view/51
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Author Biography
Roque Bru-Martínez, University of Alicante
Agroquimica y bioquimica
