Malays. Appl. Biol. (2014) 43(1): 1–12
TRANSPOSABLE ELEMENTS AND THE DETECTION OF SOMACLONAL VARIATION IN PLANT TISSUE CULTURE:
A REVIEW
AZMAN, A.S.1, MHIRI, C.2, GRANDBASTIEN, M.A.2 and TAM, S.M.3*
1Jeffrey Cheah School of Medicine and Health Sciences,
Monash University Malaysia, Jalan Lagoon Selatan, 46150, Bandar Sunway, Selangor, Malaysia
2Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParis Tech,
Batiment 2, INRA Versailles, Route de St Cyr, 78026 Versailles cedex, France
3School of Biosciences, Taylor’s University, Jalan Taylor’s,
47500, Subang Jaya, Selangor, Malaysia
*E-mail:
This e-mail address is being protected from spambots. You need JavaScript enabled to view it
ABSTRACT
Plant tissue culture uses the genetic potential, or totipotency, of plants to regenerate and give rise to a whole plant. Tissue culture-derived plants are expected to have identical genetic material to the parent, and thus can serve as an effective tool for controlled, mass clonal propagation. However, somaclonal variation has been observed in plant tissue culture due to either point mutations, transposition activity of mobile genetic elements, chromosomal rearrangements, or ploidy level changes, causing genetic instability. Tissue culture-induced mutations associated with transposable element activities have been reported from many plant studies, related to stress conditions during tissue culture such as wounding, exposure to hormones and/or specific compounds in the growth media, and genomic shocks from cytological changes. Transposable elements are repetitive DNA fragments with the ability to transpose from one region to another within a genome. Mutations that may occur during plant tissue culture suggest that the plantlets have to be regularly monitored. Methyl-sensitive transposon display (MSTD) is an advanced, efficient DNA fingerprinting technique that can simultaneously detect genetic variation, changes in transposable element insertion sites and the status of cytosine methylation of DNA in plant genomes. The main principles and notes for application of MSTD such as design of element-specific primers, identification of transposable element sequences in plant genomes, selection of the isochizomer enzymes used, and different classes of banding pattern shown are briefly discussed based on our preliminary work with Nicotiana benthamiana (Tnt1 retroelement) and Musa acuminata (Copia-33 Mad-I retroelement) examples.
Key words: Methyl-sensitive transposon display (MSTD), somaclonal variation, transposable elements
REFERENCES
Akimoto, K., Katakami, H., Kim, H.J., Ogawa, E., Sano, C.M., Wada, Y. and Sano, H. 2007. Epigenetic inheritance in rice plants. Annals of Botany 100: 205-217.
Angeles, J.G.C., Laurena, A.C. and Tecson-Mendoza, E.M. 2005. Extraction of genomic DNA from lipid-, polysaccharide-, and polyphenol-rich coconut (Cocos nucifera L.). Plant Molecular Biology Reporter 23: 297a-297i.
Arkhipova, I.R. and Meselson, M. 2005. Diverse DNA transposons in rotifiers of the class Bdelloidea. Proceeding of National Academy of Science of United States of America 102(33): 11781-11786.
Azman, A.S. 2011. Detection of genomic instability during somatic embryogenesis of oil palm. Honours thesis, Monash University Sunway Campus.
Bailey, J.A., Liu, G. and Eichler, E.E. 2003. An Alu transposition model for the origin and expansion of human segmental duplication. The American Journal of Human Genetics 73: 823-834.
Brettell, R.I.S. and Dennis E.S. 1991. Reactivation of a silent Ac following tissue culture is associated with heritable alterations in its methylation pattern. Molecular Genomics and Genetics 229: 365–372.
Bui, Q.T. and Grandbastien, M.-A. 2012. LTR Retrotransposons as controlling elements of genome response to stress? In: M.-A. Grandbastien and J.M. Casacuberta (eds.). Plant Transposable Elements. Topics in Current Genetics 24, Springer-Verlag, Berlin Heidelberg. pp. 273-296.
Burg, K., Helmersson, A., Bozhkov, P. and von Arnold, S. 2007. Development and genetic variation in nuclear microsatellite stability during somatic embryogenesis in pine. Journal of Experimental Botany 58(3): 687-698.
Casa, A.M., Brouwer, C., Nagel, A., Wang, L., Zhang, Q., Kresovich, S. and Wessler, S.R. 2000. The MITE family heartbreaker (Hbr): molecular marker in maize. Proceeding of the National Academy of Science of the United State of America 97: 10083-10089.
Chandler, M. and Mahillon, J. 2002. Insertion sequences revisited. In: Craig, N.L., Craigie, R., Gellert, M. and Lambowitz, A.M. (eds) Mobile DNA II. American Society for Microbiology Press. Washington. pp. 305-366.
Chandrika, M. and Rai, V.R. 2009. Genetic fidelity in micropropagated plantlets of Ochreinauclea missionis an endemic, threatened and medicinal tree using ISSR markers. African Journal of Biotechnology 8(13): 2933-2938.
Chen, J.M., Stenson, P.D., Cooper, D.N. and Ferec, C. 2005. A systematic analysis of LINE-I endonuclease-dependent retrotranspositional events causing human genetic disease. Human Genetics 117: 411-427.
Chuang, S.J., Chen, C.L., Chen, J.J., Chou, W.Y. and Sung, J.M. 2009. Detection of somaclonal variation in micro-propagated Echinacae purpurea using AFLP marker. Scientia Horticulturae 120(1): 121-126.
Collier, L.S. and Largaespada, D.A. .2007. Transposable elements and the dynamic somatic genome. Genome Biology 8(Suppl 1):S5 (DOI:10.1186/gb-2007-8-S1-S5): 1-5.
Dam, A., Paul, S. and Bandyopadhyay, T.K. 2010. Direct somatic embryogenesis and plant regeneration from leaf explants of Limonium sinensis (Girard) Kuntze. Scientia Horticulturae 126: 253-260.
Debnath, M., Malik, C.P. and Bisen, P.S. 2006. Micropropagation: a tool for the production of high quality plant-based medicines. Current Pharmaceutical Biotechnology 7: 33-49.
d’Erfurth, I., Cosson, V., Eschstruth, A., Lucas, H., Kondorosi, A. and Ratet, P. 2003. Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. The Plant Journal 34: 95-106.
De Setta, N., Costa, A.P.P., Lopes, F.R., Sluys, M.V. and Carareto, C.M.A. 2007. Transposon display supports transpositional activity of P elements in species of the saltans group of Drosophila. Indian Academy of Science 86(1): 37-43.
Devos, K.M., Brown, J.K.M. and Bennetzen, J.L. 2002. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Research 12: 1075-1079.
Dobránzski, J. and Texeira de Silva, J.A. 2010. Micropropagation of apple- A review. Biotechnology Advance 28: 462-488.
Dooner, H.K. and Weil, C.F. 2007. Give-and-take: interaction between DNA transposon and their host plant genomes. Current Opinion in Genetics and Development 17(6): 486-492.
Du, X.Y., Zhang, Q.L. and Luo, Z.R. 2009. Comparison of four molecular markers for genetics analysis in Diospyros L. (Ebenaceae). Plant Systematics and Evolution 281: 171-181.
Eka, C.R., Akomeah, P. and Asemota, O. 2005. Somatic embryogenesis in date palm (Phoenix dactylifera L.) from apical meristem tissues from ‘zebia’ and ‘loko’ landraces. African Journal of Biotechnology 4(3): 244-246.
Elmeer, K.M.S., Gallagher, T.F. and Hennerty, M.J. 2009. RAPD-based detection of genomic instability in cucumber plants derived from somatic embryogenesis. African Journal of Biotechnology 8(14): 3219-3222.
Eshraghi, P., Zarghami, R. and Ofoghi, H. 2005. Genetic stability of micropropagated plantlets in date palm. Journal of Sciences, Islamic Republic of Iran 16(4): 311-315.
Evans, D.A. 1989. Somaclonal variation- Genetic basis and breeding applications. Trends in Genetics 5(2): 46-50.
Fay, M.F. 1992. Practical considerations in the development of a botanic garden micropropagation laboratory. Botanic gardens in changing worlds. The Proceedings of the Third International Botanic Gardens Conservation Congress. Rio de Janeiro.
Feschotte, C., Jiang, N. and Wessler, S.R. 2002. Plant transposable elements: Where genetics meets genomics. Nature Review Genetics 3: 329-341.
Fras, A. and Maluszynska, J. 2004. The correlation between the chromosome variation in callus and genotype of explants of Arabidopsis thaliana. Genetica 121: 145–154.
Fulneek, J. and Kovaík, A. 2014. How to interpret Methylation Sensitive Amplified Polymorphism (MSAP) profiles? BMC Genetics 15:2.
Gatica-Arias, A.M., Arrieta-Espinoza, G. and Esquivel, A.M.E. 2008. Plant regenerantion via indirect somatic embryogenesis and optimization of genetic transformation in Coffea arabica L. cvs. Caturra and Catuaí. Electronic Journal of Biotechnology 11(1): 1-12.
Gaut, B.S. and Ross-Ibarra, J. 2008. Selection on major components of Angiosperm genomes. Science 320: 484-486.
Grandbastien, M.A. 1998. Avtivation of plant retrotransposons under stress conditions. Trends in Plant Science 3(5): 181-187.
Hirochika, H. 1993. Activation of tobacco retrotransposons during tissue culture. The EMBO Journal 12: 2521-2528.
Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H. and Kanda, M. 1996. Retrotransposon of rice involved in mutations induced by tissue culture. Proceeding of National Academy of Science USA 93: 7783-7788.
Huang, X., Lu, G., Zhao, Q., Liu, X. and Han, B. 2008. Genome-wide analysis of transposon insertion polymorphism reveals intraspecific variation in cultivated rice. Genome Analysis 148: 25-40.
Huang, J., Zhang, K., Shen, Y., Huang, Z., Li, M., Tang, D., Gu, M. and Cheng, Z. 2009. Identification of a high frequency transposon induced by tissue culture, nDaiZ, a member of the hAT family in rice. Genomics 93: 274-281.
Ikeda R., Kokubu C., Yusa K., Keng V. W., Horie K., and Takeda J. 2007. Sleeping Beauty transposase has an affinity for heterochromatin conformation. Molecular Cell Biology 27:1665–1676.
Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I., and Paszkowski, J. 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472: 115–119.
Ito, H. 2012. Small RNAs and transposon silencing in plants. Development Growth and Differentiation 54: 100–107.
Ito, H. 2013. Small RNAs and regulation of transposons in plants. Genes and Genetic Systems 88: 3–7.
Jaligot, E., Rival, A., Beule, T., Dussert, S., and Verdeil, J. L. 2000. Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Reporter 19: 684–690.
Jaligot, E., Beulé, T., Baurens, F.C., Billotte, N. and Rival, A. 2004. Search for methylation-sensitive amplification polymorphisms associated with the “mantled” variant phenotype in oil palm (Elaeis guineensis Jacq.). Genome 47: 224-228.
Jursch, T., Miskey, C., Izsvák1, Z. and Ivics, Z. 2013. Regulation of DNA transposition by CpG methylation and chromatin structure in human cells. Mobile DNA 4:15.
Kapitonov, V.V. and Jurka, J. 2008. A universal classification of eukaryotic transposable elements implemented in Repbase. Nature Review Genetics 9: 411-412.
Karajol, K. and Naik, G.R. 2011. Defective viral coat protein and retrotransposons might play role in NaCl stress tolerance in Pigeon pea (Cajanus cajan) cultivar. World Journal of Science and Technology 1(2): 17-25.
Kazazian, H.H. Jr. 2004. Mobile elements: drivers of genome evolution. Science 303: 1626-1632.
Kaeppler, S.M., Kaeppler, H.F. and Rhee, Y. 2000. Epigenetic aspects of somaclonal variation in plants. Plant Molecular Biology 43: 179–188.
Kikuchi, K., Terauchi, K., Wada, M. and Hirano, H. 2003. The plant MITE mPing is mobilized in anther culture. Nature 421: 167–170.
Kohany, O., Gentles, A.I., Hankus, L. and Jurka, J. 2006. Annotation, submission & sequencing of repetitive elements in Repbase: Repbase Submitter and Censor. BMC Bioinformatics 7:474.
Kolomietz, E., Meyn, M.S., Pandita, A. and Squire, J.A. 2002. The role of Alu repeat clusters as mediators of recurrent chromosomal aberrations in tumors. Gene Chromosomes Cancer 35: 97-112.
Krauss, V., Eisenhardt, C. and Unger, T. 2009. The genome of the stick insect Medauroidea extradentata is strongly methylated within genes and repetitive DNA. PLoS ONE 4(9): e7223. doi:10.1371/journal.pone.0007223.
Krikorian, A.D. and Berquam, D.L. 1969. Plant cell and tissue cultures: the role of Haberlandt. Botanical Review 35: 59-87.
Kour, G., Kour, B., Kalu, S. and Dhar, M.K. 2009. Genetic and epigenetic instability of amplification-prone sequences of a novel B chromosome induced by tissue culture in Plantago lagopus L. Plant Cell Report 28: 1857-1867.
Kuan, L.I., Chuang, W., Shan, Y. and Hui-Xia, S. 2010. Comparing genetics characteristic of retrotransposon TOS17 during different tissue culture processes in the rice cultivars Nipponbare and Shishoubaimao. Agricultural Science in China 9(2): 157-162.
Kubis, S.E., Castilho, A.M.M.F., Vershinin, A.V. and Heslop-Harrison, J.S. 2003. Retroelement, transposon and methylation status in the genome of oil palm (Elaeis guineensis) and the relationship to somaclonal variation. Plant Molecular Biology 52: 69-79.
Le, Q.H. and Bureau, T. 2004. Prediction and quality assessment of transposon insertion display data. BioTechniques 36:222-228.
Lenoir, A., Lavie, L. Prieto, J.L., Goubely, C., Coˆte´, J.-C., Pe´lissier, T. and Deragon, J.M. 2001. The Evolutionary Origin and Genomic Organization of SINEs in Arabidopsis thaliana. Molecular Biology and Evolution 18(12):2315–2322.
Lisch, D. 2009. Epigenetic regulation of transposable elements in plants. Annual Review of Plant Biology 60: 43-66.
Lippman, Z. and Martienssen, R. .2004. The role of RNA interference in heterochromatic silencing. Nature 431:364–370.
Lopes, T., Pinto, G., Loureiro, J., Costa, A. and Santos, C. 2006. Determination of genetic stability in long-term somatic embryogenic cultures and derived plantlets of cork oak using microsatellite markers. Tree Physiology 26: 1145-1152.
Lu, Y., Rong, T. and Cao, M. 2008. Analysis of DNA methylation in different maizes tissues. Journal of Genetics and Genomics 35: 41-48.
Macas, J., Neumann, P. and Navrátilová, A. 2007. Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8: 427.
Mandal, P.K., Rawal, K., Ramaswamy, R., Bhattacharya, A. and Battacharya, S. 2006. Identification of insertion hot spots for non-LTR retrotransposons: computational and biochemical application to Entamoeba histlytica. Nucleic Acid Research 34(20): 5752-5763.
Martienssen, R.A. and Colot, V. 2001. DNA methylation and epigenetic inheritance in plant and filamentous fungi. Science 293 (5532): 1070-1074.
Marum, L., Rocheta, M., Maroco, J., Oliveira, M. M. and Miguel, C. 2009. Analysis of genetic stability at SSR loci during somatic embryogenesis in maritime pine (Pinus pinaster). Plant Cell Reports 28: 673-682.
Matzke, M. and Birchler, J.A. 2005. RNAi-mediated pathways in the nucleus. Nature Reviews Genetics 6: 24-35.
Melayah, D., Bonnivard, E., Chalhoub, B., Audeon, C., and Grandbastien, M.A. 2001. The mobility of the tobacco retrotransposon correlates with its transcriptional activation by fungal factors. The Plant Journal 28: 159-168.
Meyers, B.C., Tingey, S.V. and Morgante, M. 2001. Abundance, distribution and transcriptional activity of repetitive elements in the maize genome. Genome Research 11: 1660-1676.
Michiba, K., Okamoto, T. and Mii, M. 2001. Increasing ploidy level in cell suspension culture of Doritaenopsis by exogenous application of 2,4-dichlorophenoxyacetic acid. Plant Physiology 112: 142-148.
Mirouze, M., Reinders, J., Bucher, E., Nishimura, T., Schneeberger, K., Ossowski, S., Cao, J., Weigel, D., Paszkowski, J., and Mathieu, O. 2009. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461: 427–430.
Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K. and Hirochika, H. 2003. Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retroransposon-rich regions of the genome. Plant Cell 15: 1771-1780.
Miyao A., Nakagome M., Ohnuma T., Yamagata H., Kanamori H., Katayose Y., Takahashi A., Matsumoto T., and Hirochika H. 2012. Molecular spectrum of somaclonal variation in regenerated rice revealed by whole-genome sequencing. Plant Cell Physiology 53: 256–264.
Momose, M., Abe, Y. and Ozeki, Y. 2010. Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics 186: 59-66.
Morgante, M., Hanafey, M. and Powell, W. 2002. Microsatellites are preferentially associated with non-repetitive DNA in plant genomes. Nature Genetics 30: 194-200.
Nontaswatsri, C. and Fukai, S. 2005. Regenerative callus of Dianthus ‘Telstar Scarlet’ showing mixoploidy produce diploid plants. Plant Cell, Tissue and Organ Culture 83: 351–355.
Ostertag, E.M. and Kazazian, H.H.Jr. 2001. Biology of mammalian retrotransposons. Annual Review of Genetics 35: 501-538.
Ostertag, E.M., Goodier, J.L., Zhang, Y. and Kazazian, H.H.Jr. 2003. SVA elements are non-autonomous retrotransposon that cause disease in human. The American Journal of Human Genetics 73: 1444-1451.
Ouyang S. and Buell C.R. 2004. The TIGR Plant Repeat Databases: a collective resource for the identification of repetitive sequences in plants. Nucleic Acids Res. 32(Database issue): D360-3.
Paek, K.Y., Hanh, E.J. and Park, S.Y. 2011. Micropropagation of Phalaenopsis orchids via protocorms and protocorm-like body. Methods in Molecular Biology 710(4): 293-306.
Parisod, C., Salmon, A., Zerjal, T., Tenaillon, M., Grandbastien, M.A. and Ainouche, M. 2009. Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytologist 184: 1003-1015.
Parisod C., Salmon, A. Ainouche, M. and Grandbastien, M.-A. 2014. Detecting epigenetic effects of transposable elements in plants. In: Charles Spillane and Peter C. McKeown (eds.). Plant Epigenetics and Epigenomics: Methods and Protocols, Methods in Molecular Biology, vol. 1112. Springer Science&Business Media, New York. pp. 211-217.
Peraza-Echeverria, S., Herrera-Valencia, V.A. and James-Kay, A. 2001. Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Science 71: 359-367.
Picault N., Chaparro C., Piegu B., Stenger W., Formey D., Llauro C., Descombin J., Sabot F., Lasserre E., Meynard D., Guiderdoni E., and Panaud, O. 2009. Identification of an active LTR retrotransposon in rice. Plant Journal 58: 754–765.
Piegu, B., Guvot, R., Picault, N., Roulin, A., Sanival, A., Kim, H., Cllura, K., Brar, D.S., Jackson, S., Wing, R.A. and Panaud O. 2006. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Research 16(10): 1262-1269.
Pontaroli, A.C. and Camadro, E.L. 2005. Somaclonal variation in Asparagus officinalis plants regenerated by organogenesis from long-term callus cultures. Genetic and Molecular Biology 28(3): 423-430.
Puente, R., González, A.I., Ruiz, M.L. and Polanco, C. 2008. Somaclonal variation in rye (Secale cereals L.) analyzed using polymorphic and sequenced AFLP markers. In Vitro Cell & Development Biology-Plant 44: 419-426.
Qin, Y., Li, H.L., Guo, Y.D. 2007. High frequency embryogenesis, regeneration of broccoli (Brassica oleracea var. italica) and analysis of genetic stability by RAPD. Scientia Horticulturae 111: 203-208.
Rasheed, S., Fatima, T., Husnain, T., Bashir, K. and Riazuddin, S. 2005. RAPD characterization of somaclonal variation in indica basmati rice. Pakistan Journal of Botany 37(2): 249-262.
Reyna-Lopez GE, Simpson J, Ruiz-Herrera J. 1997. Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Molecular Genomics and Genetics 253(6):703-710.
Rout, G.R., Mohapatra, A. and Mohan Jain, S. 2006. Tissue culture of ornamental pot plant: A critical review on present scenario and future prospect. Biotechnology Advance 24: 531-560.
Rozen, S. and Skaletsky, H.J. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz, S. and Misener, S. (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press. New Jersey. pp. 365-386.
Sabot, F., Picault, N., El-Baidouri, M., Llauro, C., Chaparro, C., Piegu, B., Roulin, A., Guiderdoni, E., Delabastide, M., McCombie, R., and Panaud, O. 2011. Transpositional landscape of the rice genome revealed by paired-end mapping of high-throughput re-sequencing data. Plant Journal 66: 241–246.
Sen, S.K., Han, K., Wang, J., Lee, J., Wang, H., Callinan, P.A., Dyer, M., Cordaux, R., Liang, P. and Batzer, M.A. 2006. Human genomic deletions mediated by recombinant between Alu elements. The American Journal of Human Genetics 79: 41-53.
Shirasu K., Schulman, A.H., Lahaye, T., Schulze-Lefert, P. 2000. A contiguous 66 kb barley DNA sequence provides evidence for reversible genome expansion. Genome Research 10: 908-915.
Sianipar, F.S., Wattimena, G.A., Soehartono, M.T., Aswidinnoor, H., Toruan_Mathius, N. and Ginting, G. 2008. DNA methylation detection of oil palm (Elaeis guineensis Jacq.) somatic embryo by randomly amplified DNA fingerprinting with methylation-sensitive (RAF-SM) and RP-HPLC. Journal of Biotechnology Research in Tropical Region 1: 1-6.
Singh, M.P. and Kumar, S. 2009. Principal and methodology in plant tissue culture. APH Publishing, India. pp. 9-56.
Slotkin, R.K. and Martienssen, R. 2007. Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics 8: 272-285.
Soniya, E.V., Banerjee, N.S. and Das, M.R. 2001. Genetic analysis of somaclonal variation among callus-derived plants of tomato. Current Science 80(9): 1213-1215.
Syed, N.H. and Flavell, A.J. 2007. Sequence-specific amplification polymorphisms (SSAPs): a multi-locus approach for analyzing transposon insertions. Nature Protocol 6(1): 2746-2752.
Tahara, M., Aoki, T., Suzuka, S., Yamashita, H., Tanaka, M., Matsunaga, S., and Kokumai, S. 2004. Isolation of an active element from a high-copy-number family of retrotransposons in the sweetpotato genome. Molecular Genetics and Genomics 272:116–127.
Takata, M., Kiyohara, A., Takasu, A., Kishima, Y., Ohtsubo, H. and Sano, Y. 2007. Rice transposable elements are characterized by various methylation environments in the genome. BMC Genomics 8: 469.
Takebe, I., Labib, G. and Melchers, G. 1971. Regeneration of whole plants from isolated mesiphyll protoplasts of tobacco. Naturwissenschaften 58: 318-320.
Tanurdzic, M., Vaughn, M.W., Jiang, H., Lee, T.J., Slotkin, R.K., Sosinski, B., Thompson, W.F., Doerge, R.W., and Martienssen, R.A. 2008. Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6:2880–2895.
Temel, A., Kartal, G. and Gozukirmizi, N. 2008. Genetic and epigenetic variations in barley calli culture. Biotechnology and Biotechnological Equipment 22(4): 911-914.
Thorpe, T.A. 2007. History of plant tissue culture. Molecular Biotechnology 37: 169-180.
Todorovska, E. 2007. Retrotransposons and their role in plant-genome evolution. Biotechnology and Biotechnological Equipment 21(3): 294-305.
Tsaftaris, A.S., Polidoros, A.N., Koumproglou, R., Tani, E., Kovacevic, N. and Abatzidou, E. 2005. ‘Epigenetic mechanism in plants and their implications in plant breeding’. In Tuberosa, R., Phillips, R.L. and Gale, M. (eds). Proceedings of the International Congress “In the Wake of the Double Helix: From the Green Revolution to the Gene Revolution”. Avenue Media. Italy. pp. 157-171.
Vasil, V. and Hildebrand, A.C. 1965. Differentiation of tobacco plants from single, isolated cells in micro-cultures. Science 150: 889-892.
Vázquez, A.M. and Linacero, R. 2010. Stress and somaclonal variation. In: Pua E.-C.; Davey M. (eds). Plant Developmental Biology – Biotechnological Perspectives, vol. 2. Springer, New York. pp 45–64.
Venkatachalam, L. and Sreedhar, R.V. 2007. Micropropagation in banana using high levels of cytokinins does not involve any genetic changes as revealed by RAPD and ISSR markers. Plant Growth Regulation 51: 193-205.
Venturi, S., Dondini, L., Donini, P. and Sansavini, S. 2006. Retrotransposon characterization and fingerprinting of apple clones by S-SAP markers. Theoretical and Applied Genetics 112(3): 440-444.
Vergara-Galicia, J., Aguirre-Crespo, F., Castillo-España, P., Arroyo-Mora, A., López-Escamilla, A.L., Villalobos-Molina, R. and Estrada-Soto, S. 2010. Micropropagation and vasorelaxant activity of Laelia autumnalis (Orchidaceae). Natural Product Research 24(2): 106-114.
Vizel, M., Loya, Y., Downs, C.A. and Kramarsky-Winter, E. 2010. A novel method for coral explants culture and micropropagation. Marine Biotechnology (DOI 10.1007/s10126-010-9313-z): 1-10.
Wegscheider, E., Benjak, A. and Forneck, A. 2009. Clonal variation in Pinot noir revealed by S-SAP involving universal retrotransposon-based sequences. American Journal of Enology and Viticulture 60(1): 104-109.
Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., Flavell, A., Leroy, P., Morgante, M., Panaud, O., Paux, E., SanMiguel, P. and Schulman, A.H. .2007. A unified classification system for eukaryotic transposable elements. Natural Review Genetics 8: 973-982.
Xiong, L.Z., Xu, C.G., Saghai, M.M.A. and Zhang, Q. 1999. Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Molecular and General Genetics 261: 439-446.
Yusa K., Takeda J., and Horie, K. 2004. Enhancement of Sleeping Beauty transposition by CpG methylation: possible role of heterochromatin formation. Molecular Cell Biology 24:4004–4018.
Zedek, F., Šmerda, J., Šmarda, P. and Bureš, P. 2010. Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biology 10: 265.
Zerjal, T., Joets, J., Alix, K., Grandbastien, M.A. and Tenaillon, M.I. 2009. Contrasting evolutionary patterns and target specificities among three Tourist-like MITE families in the maize genome. Plant Molecular Biology 71: 99-114.







