Transgenic flax/linseed (Linum usitatissimum L.) – expectations and reality

https://doi.org/10.17221/104/2015-CJGPBCitation:Ludvíková M., Griga M. (2015): Transgenic flax/linseed (Linum usitatissimum L.) – expectations and reality. Czech J. Genet. Plant Breed., 51: 123-141.
download PDF
This review summarizes the history, important milestones, current status and perspectives of biotech flax/linseed (Linum usitatissimum L.), supplemented with some of our original research, breeding and data on environmentalsafety. We show how recent biotechnology methods and genetic engineering contributed to the flax/linseed breeding in order to speed up the breeding process (doubled haploids technology; in vitro selection with the use of pathogenic toxins or heavy metals; genetic transformation) and for the creation of new flax/linseed cultivars. The focus is laid on genetic engineering which represents an excellent technology to enrich the flax/linseed genepool with genes of interest, which are not naturally present in the flax/linseed genome. Different methods of flax transformation are mentioned, as well as various genes of interest that have been used for flax transformation to date aimed at improving transgenic flax properties, affecting both qualitative and quantitative traits. The fatty acid content and composition, the lignan (especially secoisolariciresinol diglucoside – SDG) content, flax fibre quality, tolerance to herbicides and resistance to diseases belong, among others, to flax traits that have already been modified by genetic engineering. Selection genes, reporter genes and also promoters that have been used for the vector construction are also summarized. This paper describes different fields of utilization of genetically modified (GM) flax with different improved properties. The history of the only so far officially registered transgenic linseed cultivar Triffid is described in detail. Finally, potential risks and benefits of flax modification are evaluated and also the prime expectations of GM flax and real current state of this technology compared. Unfortunately, the products created by this technology are under strict (albeit not scientifically-based) legislative/political control in the European Union (EU), which prevents the access of products, created by breeders using this top technology, to the EU market.
References:
Abbadi A. (2004): Biosynthesis of Very-Long-Chain Polyunsaturated Fatty Acids in Transgenic Oilseeds: Constraints on Their Accumulation. THE PLANT CELL ONLINE, 16, 2734-2748  https://doi.org/10.1105/tpc.104.026070
 
Adolphe Jennifer L., Whiting Susan J., Juurlink Bernhard H. J., Thorpe Lilian U., Alcorn Jane (2010): Health effects with consumption of the flax lignan secoisolariciresinol diglucoside. British Journal of Nutrition, 103, 929-  https://doi.org/10.1017/S0007114509992753
 
Angelova V., Ivanova R., Delibaltova V., Ivanov K. (2004): Bio-accumulation and distribution of heavy metals in fibre crops (flax, cotton and hemp). Industrial Crops and Products, 19, 197-205  https://doi.org/10.1016/j.indcrop.2003.10.001
 
Badere R.S. (2014): Linseed improvement: a glance at the major developments in recent years. In: Makde K.H., Pawar S.E. (eds): Prof. A.D. Choudhary Commemoration – A Glimpse of Current Vistas in Plant Science Research. 1st Ed. Nagpur, Hislop College Publication Cell: 75–92.
 
Barakat M. N., Cocking E. C. (1983): Plant regeneration from protoplast-derived tissues of Linum usitatissimum L. (Flax). Plant Cell Reports, 2, 314-317  https://doi.org/10.1007/BF00270190
 
Barakat M. N., Cocking E. C. (1985): An assessment of the cultural capabilities of protoplasts of some wild species of linum. Plant Cell Reports, 4, 164-167  https://doi.org/10.1007/BF00571308
 
Basiran Nazir, Armitage Philip, Scott Roderick John, Draper John (1987): Genetic transformation of flax (Linum usitatissimum) by Agrobacterium tumefaciens: regeneration of transformed shoots via a callus phase. Plant Cell Reports, 6, 396-399  https://doi.org/10.1007/BF00269571
 
Bastaki Nasmah K., Cullis Christopher A. (2014): Floral-Dip Transformation of Flax (<em>Linum usitatissimum</em>) to Generate Transgenic Progenies with a High Transformation Rate. Journal of Visualized Experiments, , -  https://doi.org/10.3791/52189
 
Bäumlein H., Boerjan W., Nagy I., Bassüner R., Van Montagu M., Inzé D., Wobus U. (1991): A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Molecular & General Genetics, 225: 459–67.
 
Beckie Hugh J., Warwick Suzanne I., Nair Harikumar, Séguin-Swartz Ginette (2003): GENE FLOW IN COMMERCIAL FIELDS OF HERBICIDE-RESISTANT CANOLA (BRASSICA NAPUS). Ecological Applications, 13, 1276-1294  https://doi.org/10.1890/02-5231
 
Belhaj Khaoula, Chaparro-Garcia Angela, Kamoun Sophien, Nekrasov Vladimir (2013): Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods, 9, 39-  https://doi.org/10.1186/1746-4811-9-39
 
Bjelková Marie, Genčurová Václava, Griga Miroslav (2011): Accumulation of cadmium by flax and linseed cultivars in field-simulated conditions: A potential for phytoremediation of Cd-contaminated soils. Industrial Crops and Products, 33, 761-774  https://doi.org/10.1016/j.indcrop.2011.01.020
 
Bleho Juraj, Obert Bohuš, Takáč Tomáš, Petrovská Beáta, Heym Claudia, Menzel Diedrik, Šamaj Jozef (2012): ER disruption and GFP degradation during non-regenerable transformation of flax with Agrobacterium tumefaciens. Protoplasma, 249, 53-63  https://doi.org/10.1007/s00709-010-0261-2
 
Boba A., Kulma A., Kostyn K., Starzycki M., Starzycka E., Szopa J. (2011): The influence of carotenoid biosynthesis modification on the Fusarium culmorum and Fusarium oxysporum resistance in flax. Physiological and Molecular Plant Pathology, 76, 39-47  https://doi.org/10.1016/j.pmpp.2011.06.002
 
Booker H.M., Mischkolz J.M., St. Louis M., Lamb E.G. (2014): Analysis of the prevalence of CDC Triffid transgenic flax in Canadian grain stocks. AgBioForum, 17: 75–83.
 
Bretagne-Sagnard Bérénice, Chupeau Yves (1996): Selection of transgenic flax plants is facilitated by spectinomycin. Transgenic Research, 5, 131-137  https://doi.org/10.1007/BF01969431
 
Broadley Martin R., Willey Neil J., Wilkins Janine C., Baker Alan J. M., Mead Andrew, White Philip J. (2001): Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytologist, 152, 9-27  https://doi.org/10.1046/j.0028-646x.2001.00238.x
 
Caillot Sébastien, Rosiau Emeline, Laplace Catherine, Thomasset Brigitte (2009): Influence of light intensity and selection scheme on regeneration time of transgenic flax plants. Plant Cell Reports, 28, 359-371  https://doi.org/10.1007/s00299-008-0638-2
 
Chen Kunling, Gao Caixia (2013): TALENs: Customizable Molecular DNA Scissors for Genome Engineering of Plants. Journal of Genetics and Genomics, 40, 271-279  https://doi.org/10.1016/j.jgg.2013.03.009
 
Chen Wei, Song Kai, Cai Yirong, Li Wangfeng, Liu Bao, Liu Lixia (2011): Genetic Modification of Soybean with a Novel Grafting Technique: Downregulating the FAD2-1 Gene Increases Oleic Acid Content. Plant Molecular Biology Reporter, 29, 866-874  https://doi.org/10.1007/s11105-011-0286-5
 
Chen Yurong, Singh Surinder, Rashid Khalid, Dribnenki Paul, Green Allan (2008): Pyramiding of alleles with different rust resistance specificities in Linum usitatissimum L.. Molecular Breeding, 21, 419-430  https://doi.org/10.1007/s11032-007-9142-6
 
Chen Yurong, Zhou Xue-Rong, Zhang Zhi-Jun, Dribnenki Paul, Singh Surinder, Green Allan (2015): Development of high oleic oil crop platform in flax through RNAi-mediated multiple FAD2 gene silencing. Plant Cell Reports, 34, 643-653  https://doi.org/10.1007/s00299-015-1737-5
 
Christian M., Qi Y., Zhang Y., Voytas D. F. (): Targeted Mutagenesis of Arabidopsis thaliana Using Engineered TAL Effector Nucleases. G3&amp;#58; Genes|Genomes|Genetics, 3, 1697-1705  https://doi.org/10.1534/g3.113.007104
 
Gomes da Cunha Ana Cristina, Fernandes Ferreira Manuel (1996): Somatic embryogenesis, organogenesis and callus growth kinetics of flax. Plant Cell, Tissue and Organ Culture, 47, 1-8  https://doi.org/10.1007/BF02318959
 
Cunha Ana, Fernandes Ferreira Manuel (1997): Differences in free sterols content and composition associated with somatic embryogenesis, shoot organogenesis and calli growth of flax. Plant Science, 124, 97-105  https://doi.org/10.1016/S0168-9452(97)04587-1
 
Cunha A., Fernandes-Ferreira M. (1999): Influence of Medium Parameters on Somatic Embryogenesis from Hypocotyl Explants of Flax (Linum usitatissimum L.). Journal of Plant Physiology, 155, 591-597  https://doi.org/10.1016/S0176-1617(99)80059-5
 
Cvečková M., Vrbová M., Pavelková M., Větrovcová M., Smýkalová I., Griga M. (2014): Transgenic linseed (Linum usitatissimum L.) with alphaHMT1a: the effect on the accumulation of several metal elements. In: 11th Int. Phytotechnologies Conference, Sept 30–Oct 3, 2014, Heraklion: 155.
 
Czemplik Magdalena, Kulma Anna, Bazela Karolina, Szopa Jan (2012): The biomedical potential of genetically modified flax seeds overexpressing the glucosyltransferase gene. BMC Complementary and Alternative Medicine, 12, 251-  https://doi.org/10.1186/1472-6882-12-251
 
Czuj Tadeusz, Żuk Magdalena, Starzycki Michał, Amir Rachel, Szopa Jan (2009): Engineering increases in sulfur amino acid contents in flax by overexpressing the yeast Met25 gene. Plant Science, 177, 584-592  https://doi.org/10.1016/j.plantsci.2009.08.008
 
Dexter Jody E., Jhala Amit J., Hills Melissa J., Yang Rong-Cai, Topinka Keith C., Weselake Randall J., Hall Linda M. (2010): Quantification and Mitigation of Adventitious Presence of Volunteer Flax (Linum usitatissimum) in Wheat. Weed Science, 58, 80-88  https://doi.org/10.1614/WS-09-104.1
 
Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EEC – Commission Declaration.
 
Directive (EU) 2015/412 of the European Parliament and of the Council (2015): Official Journal of the European Union, L68/1–8.
 
(1995): A Vindication of Plant Transgenics. Bio/Technology, 13, 308-308  https://doi.org/10.1038/nbt0495-308
 
Dong Jin-Zhuo, McHughen Alan (1993): An improved procedure for production of transgenic flax plants using Agrobacterium tumefaciens. Plant Science, 88, 61-71  https://doi.org/10.1016/0168-9452(93)90110-L
 
Drexler H.S., Scheffler J.A., Heinz E. (2003): Evaluation of putative seed-specific promoters for Linum usitatissimum. Molecular Breeding, 11: 149–158. https://doi.org/10.1023/A:1022434700122
 
Dymińska Lucyna, Szatkowski Michał, Wróbel-Kwiatkowska Magdalena, Żuk Magdalena, Kurzawa Adam, Syska Wojciech, Gągor Anna, Zawadzki Mirosław, Ptak Maciej, Mączka Mirosław, Hanuza Jerzy, Szopa Jan (2013): Improved properties of micronized genetically modified flax fibers. Journal of Biotechnology, 164, 292-299  https://doi.org/10.1016/j.jbiotec.2013.01.002
 
Ellstrand Norman C., Prentice Honor C., Hancock James F. (1999): Gene Flow and Introgression from Domesticated Plants into Their Wild Relatives. Annual Review of Ecology and Systematics, 30, 539-563  https://doi.org/10.1146/annurev.ecolsys.30.1.539
 
Finnegan E. Jean, Lawrence Gregory J., Dennis Elizabeth S., Ellis Jeffrey G. (1993): Behaviour of modified Ac elements in flax callus and regenerated plants. Plant Molecular Biology, 22, 625-633  https://doi.org/10.1007/BF00047403
 
Fujisawa Masaki, Watanabe Mio, Choi Song-Kang, Teramoto Maki, Ohyama Kanji, Misawa Norihiko (2008): Enrichment of carotenoids in flaxseed (Linum usitatissimum) by metabolic engineering with introduction of bacterial phytoene synthase gene crtB. Journal of Bioscience and Bioengineering, 105, 636-641  https://doi.org/10.1263/jbb.105.636
 
Gantz V. M., Bier E. (): The mutagenic chain reaction: A method for converting heterozygous to homozygous mutations. Science, 348, 442-444  https://doi.org/10.1126/science.aaa5945
 
Glover Dominic (2010): Exploring the Resilience of Bt Cotton's ‘Pro-Poor Success Story’. Development and Change, 41, 955-981  https://doi.org/10.1111/j.1467-7660.2010.01667.x
 
GREEN A. G. (1986): A MUTANT GENOTYPE OF FLAX ( Linum usitatissimum L.) CONTAINING VERY LOW LEVELS OF LINOLENIC ACID IN ITS SEED OIL. Canadian Journal of Plant Science, 66, 499-503  https://doi.org/10.4141/cjps86-068
 
Green A. G., Marshall D. R. (1984): Isolation of induced mutants in linseed (Linum usitatissimum) having reduced linolenic acid content. Euphytica, 33, 321-328  https://doi.org/10.1007/BF00021128
 
Griga M., Tejklová E., Seidenglanz M. (2008): Assessment of possible risks associated with release of genetically modified flax and linseed (Linum usitatissimum L.) into environment of the Czech Republic. In: 10th Int. Symp. Biosafety of Genetically Modified Organisms, Symposium Handbook: Biosafety Research of GMOs: Past Achievements and Future Challenges, Nov 16–21, 2008, Wellington: 105.
 
Griga M., Vrbova M., Horacek J., Smykal P., Tejklova E. (2009): Agrobacterium-mediated transformation of flax (Linum usitatissimum L.) with heavy metal binding proteins genes. In: Joint Annual Meeting Amer Soc Plant Biol and Phycol Soc Amer, Honolulu: 242–243.
 
Hall L.M., Good A.G., Beckie H.J, Warwick S.I. (2003): Gene flow in herbicide resistant canola (Brassica napus): The Canadian experience. In: Lelley T., Balázs E., Tepfer M. (eds): Ecological Impact of GMO Dissemination in Agroecosystems. Vienna, Facultas Verlagsund Buchhandels AG: 57–66.
 
Hano C., Martin I., Fliniaux O., Legrand B., Gutierrez L., Arroo R. R. J., Mesnard F., Lamblin F., Lainé E. (2006): Pinoresinol–lariciresinol reductase gene expression and secoisolariciresinol diglucoside accumulation in developing flax (Linum usitatissimum) seeds. Planta, 224, 1291-1301  https://doi.org/10.1007/s00425-006-0308-y
 
Haughn George W., Smith Julie, Mazur Barbara, Somerville Chris (1988): Transformation with a mutant Arabidopsis acetolactate synthase gene renders tobacco resistant to sulfonylurea herbicides. MGG Molecular & General Genetics, 211, 266-271  https://doi.org/10.1007/BF00330603
 
Haun William, Coffman Andrew, Clasen Benjamin M., Demorest Zachary L., Lowy Anita, Ray Erin, Retterath Adam, Stoddard Thomas, Juillerat Alexandre, Cedrone Frederic, Mathis Luc, Voytas Daniel F., Zhang Feng (2014): Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnology Journal, 12, 934-940  https://doi.org/10.1111/pbi.12201
 
Hepburn A.G., Clarke L.E., Blundy K.S., White J. (1983): Nopaline Ti-plasmid, pTiT37, T-DNA insertions into a flax genome. Journal of Molecular and Applied Genetics, 2: 211–24.
 
Hradilová Jana, Řehulka Pavel, Řehulková Helena, Vrbová Miroslava, Griga Miroslav, Brzobohatý Břetislav (2010): Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. ELECTROPHORESIS, 31, 421-431  https://doi.org/10.1002/elps.200900477
 
Hraška Marek, Rakouský Slavomír, Čurn Vladislav (2006): Green fluorescent protein as a vital marker for non-destructive detection of transformation events in transgenic plants. Plant Cell, Tissue and Organ Culture, 86, 303-318  https://doi.org/10.1007/s11240-006-9131-1
 
Huang S., Ziboh A. (eds) (2001): Gamma-linolenic Acid: Recent Advances in Biotechnology and Clinical Applications. Champaign, AOCS Publishing.
 
Isaac Grant E., Kerr William A. (2003): Genetically Modified Organisms and Trade Rules: Identifying Important Challenges for the WTO. The World Economy, 26, 29-42  https://doi.org/10.1111/1467-9701.00508
 
Jain Ravinder K., Thompson R.Gail, Taylor David C., MacKenzie Samuel L., McHughen Alan, Rowland Gordon G., Tenaschuk Don, Coffey Maxine (1999): Isolation and Characterization of Two Promoters from Linseed for Genetic Engineering. Crop Science, 39, 1696-  https://doi.org/10.2135/cropsci1999.3961696x
 
Jhala A.J., Hall L.M., Hall J.C. (2008): Potential hybridization of flax with weedy and wild relatives: an avenue for movement of engineered genes? Crop Science, 48: 825–840.
 
Jhala Amit J., Weselake Randall J., Hall Linda M. (2009): Genetically Engineered Flax: Potential Benefits, Risks, Regulations, and Mitigation of Transgene Movement. Crop Science, 49, 1943-  https://doi.org/10.2135/cropsci2009.05.0251
 
Jhala A.J., Bhatt H., Topinka K., Hall L.M. (2011): Pollen-mediated gene flow in flax (Linum usitatissimum L.): can genetically engineered and organic flax coexist? Heredity, 106: 557–566.
 
Jordan Mark C., McHughen Alan (1987): Selection for Chlorsulfuron Resistance in Flax (Linum usitatissimum) Cell Cultures. Journal of Plant Physiology, 131, 333-338  https://doi.org/10.1016/S0176-1617(87)80172-4
 
Jordan Mark C., McHughen Alan (1988): Glyphosate tolerant flax plants from Agrobacterium mediated gene transfer. Plant Cell Reports, 7, 281-284  https://doi.org/10.1007/BF00272543
 
Joung J. Keith, Sander Jeffry D. (): TALENs: a widely applicable technology for targeted genome editing. Nature Reviews Molecular Cell Biology, 14, 49-55  https://doi.org/10.1038/nrm3486
 
Jung Jin Hee, Kim Hyojin, Go Young Sam, Lee Saet Buyl, Hur Cheol-Goo, Kim Hyun Uk, Suh Mi Chung (2011): Identification of functional BrFAD2-1 gene encoding microsomal delta-12 fatty acid desaturase from Brassica rapa and development of Brassica napus containing high oleic acid contents. Plant Cell Reports, 30, 1881-1892  https://doi.org/10.1007/s00299-011-1095-x
 
Koronfel M. (1998): Effects of the antibiotics kanamycin, cefotaxime and carbenicillin on the differentiation of flax hypocotyls. Arabian Journal of Biotechnology, 1: 93–98.
 
Kos B., Grčman H., Leštan D. (2003): Phytoextraction of lead, zinc and cadmium from soil by selected plants. Plant, Soil and Environment, 49: 548–553.
 
Kymäläinen Hanna-Riitta, Sjöberg Anna-Maija (2008): Flax and hemp fibres as raw materials for thermal insulations. Building and Environment, 43, 1261-1269  https://doi.org/10.1016/j.buildenv.2007.03.006
 
Lamblin Frédéric, Aimé Aurélie, Hano Christophe, Roussy Isabelle, Domon Jean-Marc, Van Droogenbroeck Bart, Lainé Eric (2007): The use of the phosphomannose isomerase gene as alternative selectable marker for Agrobacterium-mediated transformation of flax (Linum usitatissimum). Plant Cell Reports, 26, 765-772  https://doi.org/10.1007/s00299-006-0280-9
 
Ling Hong-Qing, Binding Horst (1997): Transformation in protoplast cultures of Linum usitatissimum and L. suffruticosum mediated with PEG and with Agrobacterium tumefaciens. Journal of Plant Physiology, 151, 479-488  https://doi.org/10.1016/S0176-1617(97)80015-6
 
Liu Qing, Singh Surinder, Green Allan (2002): High-Oleic and High-Stearic Cottonseed Oils: Nutritionally Improved Cooking Oils Developed Using Gene Silencing. Journal of the American College of Nutrition, 21, 205S-211S  https://doi.org/10.1080/07315724.2002.10719267
 
Lorenc-Kukuła Katarzyna, Amarowicz Ryszard, Oszmiański Jan, Doermann Peter, Starzycki Michał, Skała Jacek, Żuk Magdalena, Kulma Anna, Szopa Jan (2005): Pleiotropic Effect of Phenolic Compounds Content Increases in Transgenic Flax Plant. Journal of Agricultural and Food Chemistry, 53, 3685-3692  https://doi.org/10.1021/jf047987z
 
Lorenc-Kukuła Katarzyna, Wróbel-Kwiatkowska Magdalena, Starzycki Michał, Szopa Jan (2007): Engineering flax with increased flavonoid content and thus Fusarium resistance. Physiological and Molecular Plant Pathology, 70, 38-48  https://doi.org/10.1016/j.pmpp.2007.05.005
 
Lorenc-Kukuła Katarzyna, Zuk Magdalena, Kulma Anna, Czemplik Magdalena, Kostyn Kamil, Skala Jacek, Starzycki Michał, Szopa Jan (2009): Engineering Flax with the GT Family 1 Solanum sogarandinum Glycosyltransferase SsGT1 Confers Increased Resistance to Fusarium Infection. Journal of Agricultural and Food Chemistry, 57, 6698-6705  https://doi.org/10.1021/jf900833k
 
Ludvíková M., Hanáček P., Griga M. (2014): Modification of linseed oil composition using construct to induce gene silencing. In: 6. Metodické dny, sborník abstrakt, bulletin České společnosti experimentální biologie rostlin a Fyziologické sekce Slovenské botanické společnosti. 1st Ed. Praha, Česká společnost experimentální biologie rostlin.
 
Lunshof Jeantine (2015): Regulate gene editing in wild animals. Nature, 521, 127-127  https://doi.org/10.1038/521127a
 
Malik S., Bíba O., Grúz J., Arroo R. R. J., Strnad M. (2014): Biotechnological approaches for producing aryltetralin lignans from Linum species. Phytochemistry Reviews, 13, 893-913  https://doi.org/10.1007/s11101-014-9345-5
 
Marx Vivien (2012): Genome-editing tools storm ahead. Nature Methods, 9, 1055-1059  https://doi.org/10.1038/nmeth.2220
 
McHughen Alan (1989): Agrobacterium mediated transfer of chlorsulfuron resistance to commercial flax cultivars. Plant Cell Reports, 8, 445-449  https://doi.org/10.1007/BF00269045
 
McHughen A. (2000): Transgenic linseed flax (Linum usitatissimum). In: Bajaj Y.P.S (ed.): Transgenic Crops I. Biotechnology in Agriculture and Forestry, 46: 338–351.
 
McHughen Alan, Holm Frederick (1991): Herbicide resistant transgenic flax field test: Agronomic performance in normal and sulfonylurea-containing soils. Euphytica, 55, 49-56  https://doi.org/10.1007/BF00022559
 
McHughen Alan, Holm F. A. (1995): Development and preliminary field testing of a glufosinate-ammonium tolerant transgenic flax. Canadian Journal of Plant Science, 75, 117-120  https://doi.org/10.4141/cjps95-019
 
McHughen A., Rowland G. G., Holm F. A., Bhatty R. S., Kenaschuk E. O. (1997): CDC Triffid transgenic flax. Canadian Journal of Plant Science, 77, 641-643  https://doi.org/10.4141/P96-188
 
McSheffrey S.A., McHughen A., Devine M.D. (1992): Characterization of transgenic sulfonylurea-resistant flax (Linum usitatissimum). Theoretical and Applied Genetics, 84-84, -  https://doi.org/10.1007/BF00229510
 
Millam Steve, Obert Bohuš, Pret’ová Anna (2005): Plant cell and biotechnology studies in Linum usitatissimum – a review. Plant Cell, Tissue and Organ Culture, 82, 93-103  https://doi.org/10.1007/s11240-004-6961-6
 
Miśta D., Króliczewska B., Zawadzki W., Pecka E., Steininger M., Hull S., Żuk M., Szopa J. (2011): The effect of Linola and W92/72 transgenic flax seeds on the rabbit caecal fermentation - in vitro study. Polish Journal of Veterinary Sciences, 14, -  https://doi.org/10.2478/v10181-011-0083-y
 
Mlynárová Ľudmila, Bauer Miroslav, Nap Jan-Peter, Preťová Anna (1994): High efficiency Agrobacterium-mediated gene transfer to flax. Plant Cell Reports, 13, 282-285  https://doi.org/10.1007/BF00233320
 
Musialak Magdalena, Wróbel-Kwiatkowska Magdalena, Kulma Anna, Starzycka Eligia, Szopa Jan (2008): Improving retting of fibre through genetic modification of flax to express pectinases. Transgenic Research, 17, 133-147  https://doi.org/10.1007/s11248-007-9080-4
 
Najmanova Jitka, Neumannova Eliska, Leonhardt Tereza, Zitka Ondrej, Kizek Rene, Macek Tomas, Mackova Martina, Kotrba Pavel (2012): Cadmium-induced production of phytochelatins and speciation of intracellular cadmium in organs of Linum usitatissimum seedlings. Industrial Crops and Products, 36, 536-542  https://doi.org/10.1016/j.indcrop.2011.11.008
 
Nakamura Kosuke, Akiyama Hiroshi, Yamada Chihiro, Satoh Rie, Makiyama Daiki, Sakata Kozue, Kawakami Hiroshi, Mano Junichi, Kitta Kazumi, Teshima Reiko (2010): Novel Method to Detect a Construct-Specific Sequence of the Acetolactate Synthase Gene in Genetically-Modified Flax CDC Triffid (FP967). Biological & Pharmaceutical Bulletin, 33, 532-534  https://doi.org/10.1248/bpb.33.532
 
Nichterlein Karin, Marquard R., Friedt W. (1988): Breeding for Modified Fatty Acid Composition by Induced Mutations in Linseed (Linum usitatissimum L.). Plant Breeding, 101, 190-199  https://doi.org/10.1111/j.1439-0523.1988.tb00287.x
 
Ntiamoah Charles, Rowland Gordon G. (1997): Inheritance and characterization of two low linolenic acid EMS-induced McGregor mutant flax ( Linumusitatissimum ). Canadian Journal of Plant Science, 77, 353-358  https://doi.org/10.4141/P96-137
 
Obert Bohuš, Dedičová Beata, Hricová Andrea, šamaj Jozef, Pret'ová Anna (2004): Flax anther culture: effect of genotype, cold treatment and media. Plant Cell, Tissue and Organ Culture, 79, 233-238  https://doi.org/10.1007/s11240-004-0664-x
 
O'Connor B.J., Robertson A.J., Gusta L.V. (1991): Differential Stress Tolerance and Cross Adaptation in a Somaclonal Variant of Flax. Journal of Plant Physiology, 139, 32-36  https://doi.org/10.1016/S0176-1617(11)80160-4
 
Patel D., Vaghasiya J., Pancholi S.S., Paul A. (2012): Therapeutic potential of secoisolariciresinol diglucoside: a plant lignan. International Journal of Pharmaceutical Sciences and Drug Research, 4: 15–18.
 
Pavelek M., Tejklová E., Ondřej M., Vrbová M. (2012): Developments in fibrous flax breeding and cultivation. In: Kozlowski R. (ed.): Handbook of Natural Fibres, Vol. 1: Properties and Factors Affecting Breeding and Cultivation. Oxford, Woodhead Publishing Ltd.: 393–468.
 
Pennisi E. (): The Tale of the TALEs. Science, 338, 1408-1411  https://doi.org/10.1126/science.338.6113.1408
 
Polyakov A.V., Chikrizova O.F., Kalyaeva M.A., Zakhar-chenko N.S., Balokhina N.V., Buryanov Y.I. (1998): The transformation of fiber flax plants. Russian Journal of Plant Physiology, 45: 764–769.
 
Preťová A., Obert B. (2003): Flax (Linum usitatisimum L.) – a plant system for study of embryogenesis. Acta Biologica Cracoviensia, 45:15–18.
 
Preťová A., Obert B., Bartošová Z. (2007): Flax. In: Pua E.Ch., Davey M.R. (eds): Transgenic Crops VI. Series: Biotechnology in Agriculture and Forestry. Heidelberg, Springer: 129–148.
 
Qi Baoxiu, Beaudoin Frédéric, Fraser Tom, Stobart A.Keith, Napier Johnathan A, Lazarus Colin M (2002): Identification of a cDNA encoding a novel C18-Δ9 polyunsaturated fatty acid-specific elongating activity from the docosahexaenoic acid (DHA)-producing microalga, Isochrysis galbana11The nucleotide sequence reported in this paper has been submitted to the GenBank™/EBI Data Bank with accession number AF390174.. FEBS Letters, 510, 159-165  https://doi.org/10.1016/S0014-5793(01)03247-1
 
Qi Baoxiu, Fraser Tom, Mugford Sam, Dobson Gary, Sayanova Olga, Butler Justine, Napier Johnathan A, Stobart A Keith, Lazarus Colin M (): Production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in plants. Nature Biotechnology, 22, 739-745  https://doi.org/10.1038/nbt972
 
Qiu Xiao, Hong Haiping, Datla Nagamani, MacKenzie Samuel L, Taylor David C, Thomas Terry L (2002): Expression of borage Δ6 desaturase in Saccharomyces cerevisiae and oilseed crops. Canadian Journal of Botany, 80, 42-49  https://doi.org/10.1139/b01-130
 
Rakouský S., Tejklová E. (1999): Methods and prospects of flax transgenesis. Czech Journal of Genetics and Plant Breeding, 35: 125–129.
 
Rakouský S., Tejklová E., Wiesner I., Wiesnerová T., Kocábek T., Ondřej M. (1999): Hygromycin B – An alternative in flax transformant selection. Biologia Plantarum, 42: 361–369. https://doi.org/10.1023/A:1002457000944
 
Rakouský S., Tejklová E., Wiesner I. (2001): Recent advances in flax biotechnology in the Czech Republic. In: Kozlowski R., Atanasov A. (eds): Natural Fibres: Bast Plants in the New Millennium, June 3–6, 2001, Borovets: 151–155.
 
Rakouský S., Ondřej M., Sehnal F., Habuštová O. Hussein H.M., Ovesná J., Kučera L., Kocourek F., Říha K., Dostálová R., Seidenglanz M., Tejklová E., Griga M. (2004): Transgenic plant products and their introduction into the environment and crop protection systems, a risk assessment. In: Nap J.-P., Atanassov A., Stiekema W.J. (eds): Genomics for Biosafety in Plant Biotechnology. Amsterdam, IOS Press: 173–184.
 
Renouard Sullivan, Corbin Cyrielle, Lopez Tatiana, Montguillon Josiane, Gutierrez Laurent, Lamblin Frédéric, Lainé Eric, Hano Christophe (2012): Abscisic acid regulates pinoresinol–lariciresinol reductase gene expression and secoisolariciresinol accumulation in developing flax (Linum usitatissimum L.) seeds. Planta, 235, 85-98  https://doi.org/10.1007/s00425-011-1492-y
 
Renouard Sullivan, Tribalatc Marie-Aude, Lamblin Frederic, Mongelard Gaëlle, Fliniaux Ophélie, Corbin Cyrielle, Marosevic Djurdjica, Pilard Serge, Demailly Hervé, Gutierrez Laurent, Hano Christophe, Mesnard François, Lainé Eric (2014): RNAi-mediated pinoresinol lariciresinol reductase gene silencing in flax (Linum usitatissimum L.) seed coat: Consequences on lignans and neolignans accumulation. Journal of Plant Physiology, 171, 1372-1377  https://doi.org/10.1016/j.jplph.2014.06.005
 
Rissler J., Mellon M. (1996): The Ecological Risks of Engineered Crops. Cambridge, MIT Press.
 
Rowland G. G. (1991): An EMS-induced low-linolenic-acid mutant in McGregor flax ( Linum usitatissimum L.). Canadian Journal of Plant Science, 71, 393-396  https://doi.org/10.4141/cjps91-054
 
Rowland G. G., Bhatty R. S. (1990): Ethyl methanesulphonate induced fatty acid mutations in flax. Journal of the American Oil Chemists’ Society, 67, 213-214  https://doi.org/10.1007/BF02540645
 
Rowland G. G., McHughen A., Gusta L. V., Bhatty R. S., MacKenzie S. L., Taylor D. C. (1995): The application of chemical mutagenesis and biotechnology to the modification of linseed (Linum usitatissimum L.). Euphytica, 85, 317-321  https://doi.org/10.1007/BF00023961
 
Ruiz-López Noemí, Haslam Richard P., Venegas-Calerón Mónica, Larson Tony R., Graham Ian A., Napier Johnathan A., Sayanova Olga (2009): The synthesis and accumulation of stearidonic acid in transgenic plants: a novel source of ‘heart-healthy’ omega-3 fatty acids. Plant Biotechnology Journal, 7, 704-716  https://doi.org/10.1111/j.1467-7652.2009.00436.x
 
Rutkowska-Krause I., Mankowska G., Lukaszewicz M., Szopa J. (2003): Regeneration of flax ( Linum usitatissimum L.) plants from anther culture and somatic tissue with increased resistance to Fusarium oxysporum. Plant Cell Reports, 22, 110-116  https://doi.org/10.1007/s00299-003-0662-1
 
Ryan C., Smyth S. (2012): Economic implications of low level presence in a zero tolerance European import market: The case of Canadian Triffid flax. AgBioForum, 15: 21–30.
 
Schouten Henk J., Jacobsen Evert (2008): Cisgenesis and intragenesis, sisters in innovative plant breeding. Trends in Plant Science, 13, 260-261  https://doi.org/10.1016/j.tplants.2008.04.005
 
Schouten Henk J, Krens Frans A, Jacobsen Evert (2006): Cisgenic plants are similar to traditionally bred plants: International regulations for genetically modified organisms should be altered to exempt cisgenesis. EMBO reports, 7, 750-753  https://doi.org/10.1038/sj.embor.7400769
 
Shi Gangrong, Cai Qingsheng (2009): Cadmium tolerance and accumulation in eight potential energy crops. Biotechnology Advances, 27, 555-561  https://doi.org/10.1016/j.biotechadv.2009.04.006
 
Shysha E. N., Korhovyu V. I., Bayer G. Ya., Guzenko E. V., Lemesh V. A., Kartel’ N. A., Yemets A. I., Blume Ya. B. (2013): Genetic transformation of flax (Linum usaitatissimum L.) with the chimeric GFP-TUA6 gene for the visualization of microtubules. Cytology and Genetics, 47, 63-69  https://doi.org/10.3103/S0095452713020096
 
Siegień Irena, Adamczuk Aneta, Wróblewska Katarzyna (2013): Light affects in vitro organogenesis of Linum usitatissimum L. and its cyanogenic potential. Acta Physiologiae Plantarum, 35, 781-789  https://doi.org/10.1007/s11738-012-1118-4
 
Simopoulos A.P (2002): The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomedicine & Pharmacotherapy, 56, 365-379  https://doi.org/10.1016/S0753-3322(02)00253-6
 
Skórkowska-Telichowska Katarzyna, Żuk Magdalena, Kulma Anna, Bugajska-Prusak Ada, Ratajczak Katarzyna, Gąsiorowski Kazimierz, Kostyn Kamil, Szopa Jan (2010): New dressing materials derived from transgenic flax products to treat long-standing venous ulcers-a pilot study. Wound Repair and Regeneration, 18, 168-179  https://doi.org/10.1111/j.1524-475X.2010.00578.x
 
Smykalova Iva, Vrbova Miroslava, Tejklova Eva, Vetrovcova Martina, Griga Miroslav (2010): Large scale screening of heavy metal tolerance in flax/linseed (Linum usitatissimum L.) tested in vitro. Industrial Crops and Products, 32, 527-533  https://doi.org/10.1016/j.indcrop.2010.06.027
 
Snow Allison A. (1997): Commercialization of Transgenic Plants: Potential Ecological Risks. BioScience, 47, 86-96  https://doi.org/10.2307/1313019
 
Soudek Petr, Katrušáková Adéla, Sedláček Lukáš, Petrová Šárka, Kočí Vladimír, Maršík Petr, Griga Miroslav, Vaněk Tomáš (2010): Effect of Heavy Metals on Inhibition of Root Elongation in 23 Cultivars of Flax (Linum usitatissimum L.). Archives of Environmental Contamination and Toxicology, 59, 194-203  https://doi.org/10.1007/s00244-010-9480-y
 
Stoutjesdijk P. A. (): hpRNA-Mediated Targeting of the Arabidopsis FAD2 Gene Gives Highly Efficient and Stable Silencing. PLANT PHYSIOLOGY, 129, 1723-1731  https://doi.org/10.1104/pp.006353
 
Tejklová E. (1996): Some factors affecting anther culture in Linum usitatissimum L. Rostlinná výroba, 42: 249–260. (in Czech)
 
Tejklová E., Bjelková M. (2011): New Varieties: Low-linolenic linseed (Linum usitatissimum L.) Allan. Czech Journal of Genetics and Plant Breeding, 47: 41–42.
 
Tejklová E., Seidenglanz M., Griga M. (2009): Evaluation of risk assessment associated with release of genetically modified flax (Linum usitatissimum L.) into the environment in the Czech Republic. In: Sehnal F., Drobník J. (eds.): White Book of Genetically Modified Crops. EU Regulations and Research Experience from the Czech Republic. České Budějovice, Biology Centre AS CR: 74.
 
Tejklová E., Bjelková M., Pavelek M. (2011): New Varieties: medium-linolenic linseed (Linum usitatissimum L.) Raciol. Czech Journal of Genetics and Plant Breeding, 47: 128–130.
 
Thompson L. U. (2005): Dietary Flaxseed Alters Tumor Biological Markers in Postmenopausal Breast Cancer. Clinical Cancer Research, 11, 3828-3835  https://doi.org/10.1158/1078-0432.CCR-04-2326
 
Tian B.M., Sun D.D., Lian Y.L., Shu H.Y., Ling H., Zang X., Wang B.N., Pei Z.Q. (2011): Analysis of the RNAi targeting FAD2 gene on oleic acid composition in transgenic plants of Brassica napus. African Journal of Microbiology Research, 5: 817–822.
 
Truksa Martin, MacKenzie Samuel L., Qiu Xiao (2003): Molecular analysis of flax 2S storage protein conlinin and seed specific activity of its promoter. Plant Physiology and Biochemistry, 41, 141-147  https://doi.org/10.1016/S0981-9428(02)00022-0
 
Vanella Rosario, Weston Anna, Brodmann Peter, Kübler Eric (2014): Development of an event-specific assay for the qualitative and quantitative detection of the genetically modified flax CDC Triffid (FP967). Food Control, 41, 128-133  https://doi.org/10.1016/j.foodcont.2014.01.014
 
Viju Crina, Yeung May T., Kerr William A. (2014): Zero Tolerance for GM Flax and the Rules of Trade. The World Economy, 37, 137-150  https://doi.org/10.1111/twec.12077
 
Vrbová M. (2013): Molecular contingency of flax resistance to heavy metals and possibility of its influencing via transgenesis. [Ph.D. Thesis.] Brno, Mendel University.
 
Vrbová M., Horáček J., Smýkal P., Griga M. (2009): Flax (Linum usitatissimum L.) transformation with heavy metal binding protein genes. In: Sehnal F., Drobník J. (eds): White Book of Genetically Modified Crops. EU Regulations and Research Experience from the Czech Republic. České Budějovice, Biology Centre AS CR: 57.
 
Vrbová Miroslava, Kotrba Pavel, Horáček Jiří, Smýkal Petr, Švábová Lenka, Větrovcová Martina, Smýkalová Iva, Griga Miroslav (2013): Enhanced accumulation of cadmium in Linum usitatissimum L. plants due to overproduction of metallothionein α-domain as a fusion to β-glucuronidase protein. Plant Cell, Tissue and Organ Culture (PCTOC), 112, 321-330  https://doi.org/10.1007/s11240-012-0239-1
 
Vrinten Patricia, Wu Guohai, Truksa Martin, Qiu Xiao (2007): Production of Polyunsaturated Fatty Acids in Transgenic Plants. Biotechnology and Genetic Engineering Reviews, 24, 263-280  https://doi.org/10.1080/02648725.2007.10648103
 
Wagner Nicholas, Mroczka Andrew, Roberts Peter D., Schreckengost William, Voelker Toni (2011): RNAi trigger fragment truncation attenuates soybean FAD2-1 transcript suppression and yields intermediate oil phenotypes. Plant Biotechnology Journal, 9, 723-728  https://doi.org/10.1111/j.1467-7652.2010.00573.x
 
Warwick S.I., Stewart C.N. Jr. (2005): Crops come from wild plants – How domestication, transgenes, and linkage together shape ferality. In: Gressel J.B. (ed.): Crop Ferality and Volunteerism. Boca Raton, Taylor & Francis Group: 9–30.
 
Wijayanto Teguh, McHughen Alan (1999): Genetic transformation of Linum by particle bombardment. In Vitro Cellular & Developmental Biology - Plant, 35, 456-465  https://doi.org/10.1007/s11627-999-0068-z
 
Wojtasik Wioleta, Kulma Anna, Dymińska Lucyna, Hanuza Jerzy, Żebrowski Jacek, Szopa Jan (2013): Fibres from flax overproducing β-1,3-glucanase show increased accumulation of pectin and phenolics and thus higher antioxidant capacity. BMC Biotechnology, 13, 10-  https://doi.org/10.1186/1472-6750-13-10
 
Wróbel Magdalena, Zebrowski Jacek, Szopa Jan (2004): Polyhydroxybutyrate synthesis in transgenic flax. Journal of Biotechnology, 107, 41-54  https://doi.org/10.1016/j.jbiotec.2003.10.005
 
Wróbel-Kwiatkowska M., Zebrowski J., Starzycki M., Oszmianski J., Szopa J. (2007a): Engineering of PHB synthesis causes improved elastic properties of flax fibers. Biotechnology Progress, 23: 269–277.
 
Wróbel-Kwiatkowska M., Starzycki M., Zebrowski J., Oszmiański J., Szopa J. (2007b): Lignin deficiency in transgenic flax resulted in plants with improved mechanical properties. Journal of Biotechnology, 128: 919–934.
 
Wróbel-Kwiatkowska Magdalena, Skórkowska-Telichowska Katarzyna, Dymińska Lucyna, Mączka Mirosław, Hanuza Jerzy, Szopa Jan (2009): Biochemical, mechanical, and spectroscopic analyses of genetically engineered flax fibers producing bioplastic (poly-β-hydroxybutyrate). Biotechnology Progress, 25, 1489-1498  https://doi.org/10.1002/btpr.194
 
Wróbel-Kwiatkowska M., Czemplik M., Kulma A., Żuk M., Kaczmar J., Dyminska L., Hanuza J., Ptak M., Szopa J. (2012a): New biocomposites based on bioplastic flax fibers and biodegradable polymers. Biotechnology Progress, 28: 1336–1346.
 
Wróbel-Kwiatkowska M., Turnau K., Góralska K., Anielska T., Szopa J. (2012b): Effects of genetic modifications to flax (Linum usitatissimum) on arbuscular mycorrhiza and plant performance. Mycorrhiza, 22: 493–499.
 
Wugar D., Cottier T. (2008): Genetic Engineering and the World Trade System. Cambridge, Cambridge University Press.
 
Wyndham J. (1951): The Day of the Triffids. New York, Doubleday & Company.
 
Xu Rongfang, Li Hao, Qin Ruiying, Wang Lu, Li Li, Wei Pengcheng, Yang Jianbo (2014): Gene targeting using the Agrobacterium tumefaciens-mediated CRISPR-Cas system in rice. Rice, 7, -  https://doi.org/10.1186/s12284-014-0005-6
 
Yang Mingfeng, Zheng Guiling, Zhang Fayun, Xu Yinong (2006): FAD2-silencing has pleiotropic effect on polar lipids of leaves and varied effect in different organs of transgenic tobacco. Plant Science, 170, 170-177  https://doi.org/10.1016/j.plantsci.2005.08.022
 
Zanwar Anand, Hegde Mahabaleshwar, Bodhankar Subhash (2011): Cardioprotective activity of flax lignan concentrate extracted from seeds of Linum usitatissimum in isoprenalin induced myocardial necrosis in rats. Interdisciplinary Toxicology, 4, -  https://doi.org/10.2478/v10102-011-0016-8
 
Zaplin Ella Simone, Liu Qing, Li Zhongyi, Butardo Vito M., Blanchard Christopher L., Rahman Sadequr (2013): Production of high oleic rice grains by suppressing the expression of the OsFAD2-1 gene. Functional Plant Biology, 40, 996-  https://doi.org/10.1071/FP12301
 
Zhan Xiang-can, Jones David A., Kerr Allen (1988): Regeneration of flax plants transformed by Agrobacterium rhizogenes. Plant Molecular Biology, 11, 551-559  https://doi.org/10.1007/BF00017455
 
Zuk M., Kulma A., Dyminska L., Szołtysek K., Prescha A., Hanuza J., Szopa J. (2011a): Flavonoid engineering of flax potentiate its biotechnological application. BMC Biotechnology, 11: 10.
 
Zuk M., Dymińska L., Kulma A., Boba A., Prescha A., Szopa J., Mączka M., Zając A., Szołtysek K., Hanuza J. (2011b): IR and Raman studies of oil and seedcake extracts from natural and genetically modified flax seeds. Spectrochimica Acta. Part A, Molecular and Biomolecular Spectroscopy, 78: 1080–1089.
 
Zuk Magdalena, Prescha Anna, Stryczewska Monika, Szopa Jan (2012): Engineering Flax Plants To Increase Their Antioxidant Capacity and Improve Oil Composition and Stability. Journal of Agricultural and Food Chemistry, 60, 5003-5012  https://doi.org/10.1021/jf300421m
 
Zuk Magdalena, Dorotkiewicz-Jach Agata, Drulis-Kawa Zuzanna, Arendt Malgorzata, Kulma Anna, Szopa Jan (2014): Bactericidal activities of GM flax seedcake extract on pathogenic bacteria clinical strains. BMC Biotechnology, 14, 70-  https://doi.org/10.1186/1472-6750-14-70
 
download PDF

© 2019 Czech Academy of Agricultural Sciences