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Physiological and biochemical analysis of growth abnormalities associated with plant tissue culture

  • Review Report
  • Tissue Culture/Biotechnology
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Abstract

Micropropagation is an important tool in the multiplication of genetically uniform plants that possess desirable traits for horticultural industry. Like many other technologies, it has gone through different stages of evolution that focused mainly on the production efficiency in terms of quantity. However, several problems affecting the quality of the multiplied plants such as shoot tip necrosis, abnormal and inefficient root development, hyperhydration, fasciation and habituation, have not been adequately investigated using additives or modification of growth conditions. Molecular markers can be used to observe genome modifications of the cloned plants but genetic uniformity is not directly related to phenotypic uniformity, therefore molecular markers may not be useful to understand the bases of these undesirable phenomena. In general, although the tissue culture procedure produces quality propagules, the process induces a stress reaction in the developing plantlets. Plants may show a multitude of responses, including epigenetic variations. Epigenetic regulation is not only important for generating differentiated cell types during plant development, but also in maintaining the stability and integrity of their respective gene expression profiles. In plant tissue culture, changes in DNA methylation and in histone modifications have also been reported in many cases during the de-differentiation pathway, ranging from axillary shoot proliferation to protoplast formation. Information on molecular techniques is increasing rapidly together with the decreasing costs of the molecular detection. It is, therefore, important to employ epigenetic markers to understand all desirable or undesirable physiological responses that occur during tissue culture in the production of quality propagules.

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Literature Cited

  • Aina, R., S. Sgorbati, A. Santagostino, M. Labra, A. Ghiani, and S. Citterio. 2004. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol. Plant. 121:472–480.

    Article  CAS  Google Scholar 

  • Akin-Idowu, P.E., D.O. Ibitoye, and O.T. Ademoyegun. 2009. Tissue culture as a plant production technique for horticultural crops. Afr. J. Biotech. 8:3782–3788.

    Google Scholar 

  • Alwee, S.S., C.G. Van Der Linden, J. Van Der Schoot, S. De Folter, G.C. Angenent, S.C. Cheah, and M.J.M. Smulders. 2006. Characterization of oil palm MADS box genes in relation to the mantled flower abnormality. Plant Cell Tissue Organ. Cult. 85:331–344.

    Article  Google Scholar 

  • Appelgren, M. and O.M. Heide. 1972. Regeneration in Streptocarpus leaf discs and its regulation by temperature and growth substances. Physiol. Plant. 27:417–423.

    Article  CAS  Google Scholar 

  • Aufsatz, W., M.F. Mette, J. Van Der Winden, M. Matzke, and A.J. Matzke. 2002. HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J. 21:6832–6841.

    Article  PubMed  CAS  Google Scholar 

  • Bairu, M.W. and M.E. Kane. 2011a. Physiological and developmental problems encountered by in vitro cultured plants. Plant Growth Regul. 63:101–103.

    Article  CAS  Google Scholar 

  • Bairu, M.W., A.O. Aremu, and J. Van Staden. 2011b. Somaclonal variation in plants: Causes and detection methods. Plant Growth Regul. 63:147–173.

    Article  CAS  Google Scholar 

  • Bairu, M.W., O. Novák, K. Doležal, and J. Van Staden. 2011c. Changes in endogenous cytokinin profiles in micropropagated Harpagophytum procumbens in relation to shoot-tip necrosis and cytokinin treatments. Plant Growth Regul. 63:105–114.

    Article  CAS  Google Scholar 

  • Bairu, M.W., W.A. Stirk, and J. Van Staden. 2009. Factors contributing to in vitro shoot-tip necrosis and their physiological interactions. Plant Cell Tissue Organ. Cult. 98:239–248.

    Article  Google Scholar 

  • Baránek, M., B. Křižan, E. Ondrušíková, and M. Pidra. 2010. DNA methylation changes in grapevine somaclones following in vitro culture and thermotherapy. Plant Cell Tissue Organ. Cult. 101:11–22.

    Article  CAS  Google Scholar 

  • Benson, E.E. 2000. In vitro plant recalcitrance: An introduction. In vitro Cell. Dev. Biol. Plant. 36:141–148.

    Article  Google Scholar 

  • Brand, M.H. 2011. Tissue proliferation condition in micropropagated ericaceous plants. Plant Growth Regul 63:131–136.

    Article  CAS  Google Scholar 

  • Brand, M.H. and Y. Ruan. 2000. Response of rhododendron ‘Montego’ with “tissue proliferation” to cytokinin and auxin in vitro. Hortscience 35:136–140.

    CAS  Google Scholar 

  • Brzeski, J. and A. Jerzmanowski. 2002. Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatine remodeling factors. J. Biol. Chem. 278:823–828.

    Article  PubMed  Google Scholar 

  • Camporeale, G., A.M. Oommen, J.B. Griffin, G. Sarath, and J. Zempleni. 2007. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J. Nutr. Biochem. 18:760–768.

    Article  PubMed  CAS  Google Scholar 

  • Cassells, A.C. and R.F. Curry. 2001. Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: Implications for micropropagators and genetic engineers. Plant Cell Tissue Organ. Cult. 64:145–157.

    Article  CAS  Google Scholar 

  • Chen, L.T. and K. Wu. 2010. Role of histone deacetylases HDA6 and HDA19 in ABA and abiotic stress response. Plant Signal. Behav. 5:1318–20.

    Article  PubMed  CAS  Google Scholar 

  • Choi, S.W. and S. Friso. 2010. Epigenetics: A new bridge between nutrition and health. Adv. Nutr. 1:8–16.

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y., M. Gehring, L. Johnson, M. Hannon, J.J. Harada, R.B. Goldberg, S.E. Jacobsen, and R.L. Fischer. 2002. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110:33–42.

    Article  PubMed  CAS  Google Scholar 

  • Clark, S.E., M.P. Running, and E.M. Meyerowitz. 1993. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119:397–418.

    PubMed  CAS  Google Scholar 

  • D’Arth, S.M., S.I. Simpson, J.F. Seelye, and P.E. Jameson. 2002. Bushiness and cytokinin sensivity in micropropagated Zantedeschia. Plant Cell Tissue Organ. Cult. 70:113–118.

    Article  Google Scholar 

  • De Klerk, G.J. 1990. How to measure somaclonal variation. Acta Bot. Neerl. 39:129–144.

    Google Scholar 

  • De Klerk, G.J. 2007. Stress in plants cultured in vitro. Propag. Ornam. Plants 7:129–137.

    Google Scholar 

  • De Klerk, G.J., J. Ter Brugge, and S. Marinova. 1997. Effectiveness of indolacetic acid, indolebutyric acid and naphtelenacetic acid during adventitious root formation in vitro in Malus “Jork 9”. Plant Cell Tissue Organ. Cult. 49:39–44.

    Article  Google Scholar 

  • Debergh, P., J. Aitken-Christie, D. Cohen, B. Grout, S. Von Arnold, R. Zimmerman, and M. Ziv. 1992. Reconsideration of the term ‘vitrification’ as used in micropropagation. Plant Cell Tissue Organ. Cult. 30:135–140.

    Article  Google Scholar 

  • Desjardins, Y., J.F. Dubuc, and A. Badr. 2009. In vitro culture of plants: A stressful activity! Acta Hort. 812:29–50.

    CAS  Google Scholar 

  • Earley, K., R.J. Lawrence, O. Pontes, R. Reuther, A.J. Enciso, M. Silva, N. Neves, M. Gross, W. Viegas, and C.S. Pikaard. 2006. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 20:1283–1293.

    Article  PubMed  CAS  Google Scholar 

  • Economou, A.S. and P.E. Read. 1987. Light treatments to improve efficiency of in vitro propagation systems. HortScience 22:751–754.

    Google Scholar 

  • Fang, W. and R.C. Jao. 2000. A review on artificial lighting of tissue cultures and transplants, p. 108–113. In: C. Kubota and C. Chun. (eds.). Transplant production in the 21st century. Kluwer Academic Publishers, Netherlands.

    Google Scholar 

  • Feher, A., T.P. Pasternak, and D. Dudits. 2003. Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ. Cult. 74:201–228.

    Article  CAS  Google Scholar 

  • Fonnesbech, M. 1974. Temperature effects on shoot and root development from Begonia × cheimantha petiole segments grown in vitro. Physiol. Plant. 32:282–286.

    Article  Google Scholar 

  • Fraga, M.F., R. Rodríguez, and M.J. Cañal. 2002. Genomic DNA methylation-demethylation during aging and reinvigoration of Pinus radiata. Tree Physiol. 22:813–816.

    Article  PubMed  CAS  Google Scholar 

  • Friml, J. 2003. Auxin transport-shaping the plant. Curr. Opin. Plant. Biol. 6:7–12.

    Article  PubMed  CAS  Google Scholar 

  • Frommer, M., L.E. McDonald, D.S. Millar, C.M. Collis, F. Watt, G.W. Grigg, P.L. Molloy, and C.L. Paul. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. USA 89:1827–1831.

    Article  PubMed  CAS  Google Scholar 

  • Fukui, K. 1983. Sequential occurrence of mutations in a growing rice callus Theo. Appl. Genet. 65:225–230.

    Article  Google Scholar 

  • Gauthert, R.J. 1942. Hétéro-auxines et cultures de tissus végétaux. Bull. Soc. Chim. Biol. 24:13–41.

    Google Scholar 

  • George, E.F. 1993. Plant propagation by tissue culture. Part 1. The technology. Exegetics Ltd., Basingstoke, UK.

    Google Scholar 

  • George, E.F. 1996. Plant propagation by tissue culture. Part 2. In practice. Exegetics Ltd., Basingstoke, UK.

    Google Scholar 

  • Goldberg, A.D., C.D. Allis, and E. Bernstein. 2007. Epigenetics: A landscape takes shape. Cell 128:635–638.

    Article  PubMed  CAS  Google Scholar 

  • Gonzalgo, M.L. and P.A. Jones. 1997. Rapid quantitation of methylation differences at specific sites using methylation-sensitive single nucleotide primer extension (Ms-SNuPE). Nucleic Acids Res. 25:2529–2531.

    Article  PubMed  CAS  Google Scholar 

  • Grafi, G. 2004. How cells dedifferentiate: A lesson from plants. Dev. Biol. 268:1–6.

    Article  PubMed  CAS  Google Scholar 

  • Griesbach, R. and P. Semeniuk. 1987. Use of somaclonal variation in the improvement of Eustoma grandiflorum. J. Heredity 78: 114–116.

    Google Scholar 

  • Halperin, W. 1995. In vitro embryogenesis: Some historial issues and unresolved problems, p. 1–16. In: T.A. Thorpe (ed.). In vitro embryogenesis in plants. Springer, Netherlands.

    Chapter  Google Scholar 

  • Henderson, I.R. and S.E. Jacobsen. 2007. Epigenetic inheritance in plants. Nature 447:418–424.

    Article  PubMed  CAS  Google Scholar 

  • Hirochika, H., K. Sugimoto, Y. Otsuki, H. Tsugawa, and M. Kanda. 1996. Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. USA 93:7783–7788.

    Article  PubMed  CAS  Google Scholar 

  • Iliev, I. and P. Kitin. 2011. Origin, morphology, and anatomy of fasciation in plants cultured in vivo and in vitro. Plant Growth Regul. 63:115–129.

    Article  CAS  Google Scholar 

  • Irish, E.E. and D. McMurray. 2006. Rejuvenation by shoot apex culture recapitulates the developmental increase of methylation at the maize gene Pl-Blotched. Plant Mol. Biol. 60:747–758

    Article  PubMed  CAS  Google Scholar 

  • Jaligot, E., T. Beulé, and A. Rival. 2002. Methylation-sensitive RFLPs: Characterisation of two oil palm markers showing somaclonal variation-associated polymorphism. Theor. Appl. Genet. 104:1263–1269.

    Article  PubMed  CAS  Google Scholar 

  • Jones, O.P. and C.A. Webster. 1989. Improved rooting from conventional cuttings taken from micropropagated plants of Pyrus communis rootstock. J. Hort. Sci. 64:429–434.

    Google Scholar 

  • Jones, O.P., M. Welander, B.J. Waller, and M.S. Ridout. 1996. Micropropagation of adult birch trees: Production and field performance. Tree Physiol. 16:521–255.

    Article  PubMed  Google Scholar 

  • Jordan, K.A., J. Norikane, and T. Takakura. 2001. Control of LED to achieve light quality and intensity in tissue culture and micro-propagation studies. Acta Hort. 562:135–140.

    Google Scholar 

  • Kaeppler, S.M., H.F. Kaeppler, and Y. Rhee. 2000. Epigenetic aspects of somaclonal variation in plants. Plant Mol. Biol. 43:179–188.

    Article  PubMed  CAS  Google Scholar 

  • Kaldis, A., D. Tsementzi, O. Tanriverdi, and K.E. Vlachonasios. 2011. Arabidopsis thaliana transcriptional co-activators ADA2b and SGF29a are implicated in salt stress responses. Planta 233:749–762.

    Article  PubMed  CAS  Google Scholar 

  • Kataeva, N.V., I.G. Alexandrova, R.G. Butenko, and E.V. Dragavtceva. 1991. Effect of applied and internal hormones on vitrification and apical necrosis of different plants cultured in vitro. Plant Cell Tissue Organ Cult. 27:149–154.

    Article  CAS  Google Scholar 

  • Kaufmann, K., J.M. Muino, M. Osteras, L. Farinelli, P. Krajewski, and G.C. Angenent. 2010. Chromatin immunoprecipitation (ChlP) of plant transcription factors followed by sequencing (ChlP-SEQ) or hybridization to whole genome arrays (ChlP-CHIP). Nature Protocols 5:457–472.

    Article  PubMed  CAS  Google Scholar 

  • Kim, D.H., M.R. Doyle, S. Sung, and R.M. Amasino. 2009a. Vernalization: Winter and the timing of flowering in plants. Ann. Rev. Cell Dev. Biol. 25:277–299.

    Article  CAS  Google Scholar 

  • Kim, J.M., T.K. To, J. Ishida, T. Morosawa, M. Kawashima, A. Matsui, T. Toyoda, H. Kimura, K. Shinozaki, and M. Seki. 2008. Alterations of lysine modifications on histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol. 49:1580–1588.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J.M., T.K. To, T. Nishioka, and M. Seki. 2009b. Chromatin regulation functions in plant abiotic stress responses. Plant, Cell Environ. 33:604–611.

    Article  CAS  Google Scholar 

  • Kovařik, A., B. Koukalová, M. Bezděk, and Z. Opatrný. 1997. Hypermethylation of tobacco heterochromatic loci in response to osmoticstress. Theor. Appl. Genet. 95:301–306.

    Article  Google Scholar 

  • Krizova, K., M. Fojtova, A. Depicker, and A. Kovari. 2009. Cell culture-induced gradual and frequent epigenetic reprogramming of invertedly repeated tobacco transgene epialleles. Plant Physiol. 149:1493–1504.

    Article  PubMed  CAS  Google Scholar 

  • Labra, M., C. Vannini, F. Sala, and M. Bracale. 2002. Methylation changes in specific sequences in response to water deficit. Plant Biosyst. 136:269–276.

    Article  Google Scholar 

  • Larkin, P. and W. Scowcroft. 1981. Somaclonal variation A novel source of variability from cell cultures for plant improvement. Theor. Appl. Genet. 60:197–214.

    Article  Google Scholar 

  • Laux, T. 2003. The stem cell concept in plants: A matter of debate. Cell 113:281–283.

    Article  PubMed  CAS  Google Scholar 

  • Law, J.A. and S.E. Jacobsen. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:204–220.

    Article  PubMed  CAS  Google Scholar 

  • Lee, J.M. 2004. Plant cell culture and its applications, p. 931–933. In: R.M. Goodman (ed.). Encyclopaedia of plant and crop sciences. Marcel Dekker, USA.

    Google Scholar 

  • Leon, J., E. Rojo, and J.J. Sanchez-Serrano. 2001. Wound signalling in plants. J. Exp. Bot. 52:1–9.

    Article  PubMed  CAS  Google Scholar 

  • Lister, R., B.D. Gregory, and J.R. Ecker. 2009. Next is now: New technologies for sequencing of genomes, transcriptomes, and beyond. Current Opinion Plant Biol. 12:107–118.

    Article  CAS  Google Scholar 

  • Lister, R., R.C. O’Malley, J. Tonti-Filippini, B.D. Gregory, C.C. Berry, A.H. Millar, and J.R. Ecker. 2008. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Z., Y. Zhu, J. Gao, F. Yu, A. Dong, and W.H. Shen. 2009. Molecular and reverse genetic characterization of Nucleosome Assembly Protein1 (NAP1) genes unravels their function in transcription and nucleotide excision repair in Arabidopsis thaliana. Plant J. 59:27–38.

    Article  PubMed  CAS  Google Scholar 

  • Luo, M., X. Liu, P. Singh, Y. Cui, L. Zimmerli, and K. Wu. 2012a. Chromatin modifications and remodeling in plant abiotic stress responses. Biochim. Biophys. Acta 1819:129–136.

    Article  PubMed  CAS  Google Scholar 

  • Luo, M., Y.Y. Wang, X. Liu, S. Yang, and K. Wu. 2012b. HD2 proteins interact with RPD3-type histone deacetylases. Plant Signal Behav. 7:608–610.

    Article  PubMed  CAS  Google Scholar 

  • Manzano, C., E. Ramirez-Parra, I. Casimiro, S. Otero, B. Desvoyes, B. De Rybe, T. Beeckman, P. Casero, C. Gutierrez, and C. del Pozo. 2012. Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiol. 160:749–62.

    Article  PubMed  CAS  Google Scholar 

  • Matarazzo, M.R., F. Lembo, T. Angrisano, E. Ballestar, M. Ferraro, R. Pero, M.L. De Bonis, C.B. Bruni, M. Esteller, M. D’Esposito, and L. Chiariotti. 2004. In vivo analysis of DNA methylation patterns recognized by specific proteins: Coupling ChIP and bisulfite analysis. BioTechniq. 37:666–673.

    CAS  Google Scholar 

  • Matzke, M., T. Kanno, L. Daxinger, B. Huettel, and A.J.M. Matzke. 2009. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21:367–376.

    Article  PubMed  CAS  Google Scholar 

  • McClintock, B. 1984. The significance of responses of the genome to challenge. Science 226:792–801.

    Article  PubMed  CAS  Google Scholar 

  • Meins, F. 1989. Habituation: Heritable variation in the requirement of cultured plant-cells for hormones. Ann. Rev. Genet. 23:395–408.

    Article  PubMed  CAS  Google Scholar 

  • Metzke, M.L. 2010. Sequencing technologies — The next generation. Nature Rev. Genet. 11:31–46.

    Article  CAS  Google Scholar 

  • Miguel, C. and L. Marum. 2011. An epigenetic view of plant cells cultured in vitro: Somaclonal variation and beyond. J. Expt. Bot. 62:3713–3725.

    Article  CAS  Google Scholar 

  • Mineo, L. 1990. Plant tissue culture techniques, p. 151–174. In: C.A. Goldman (ed.). Tested studies for laboratory teaching. Vol. 11. Association for Biology Laboratory Education (ABLE). http://www.ableweb.org/volumes/vol-11/9-mineo.pdf

    Google Scholar 

  • Molinier, J., G. Ries, C. Zipfel, and B. Hohn. 2006. Transgeneration memory of stress in plants. Nature 442:1046–1049.

    Article  PubMed  CAS  Google Scholar 

  • Morel, G.M. 1948. Recherches sur la culture associee de parasites obligatoires et de tissues vegetaux. Ann. Epiphyties 14:123–124.

    Google Scholar 

  • Morel, G.M. 1960. Producing virus-free Cymbidium. Amer. Orchid Soc. Bull. 25:495–497.

    Google Scholar 

  • Morini, S., C. D’Onofrio, G. Bellocchi, and M. Fisichella. 2000. Effect of 2,4-D and light quality on callus production and differentiation from in vitro cultured quince leaves. Plant Cell Tissue Organ Cult. 63:47–55.

    Article  CAS  Google Scholar 

  • Moyo, M., J.F. Finnie, and J. Van Staden. 2011. Recalcitrant effects associated with the development of basal callus-like tissue on caulogenesis and rhizogenesis in Sclerocarya birrea. Plant Growth Regul. 63:187–195.

    Article  CAS  Google Scholar 

  • Nathan, D., K. Ingvarsdottir, D.E. Sterner, G.R. Bylebyl, M. Dokmanovic, J.A. Dorsey, K.A. Whelan, M. Krsmanovic, W.S. Lane, and P.B. Meluh. 2006. Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 20:966–976.

    Article  PubMed  CAS  Google Scholar 

  • Neelakandan, A. and K. Wang. 2012. Recent progress in the under standing of tissue culture-induced genome level changes in plants and potential application. Plant Cell Rep. 31:597–620.

    Article  PubMed  CAS  Google Scholar 

  • Nesi, B., D. Trinchello, S. Lazzereschi, B. Ruffoni, and A. Grassotti. 2009. Production of lily symptomless virus-free plants via shoot meristem tip culture and in vitro thermotherapy. Hortscience 44:217–219.

    Google Scholar 

  • Oh, T.J., M.A. Cullis, K. Kunert, I. Engelborghs, R. Swennen, and C.A. Cullis. 2007. Genomic changes associated with somaclonal variation in banana (Musa spp.). Physiol. Plant. 129:766–774.

    Article  CAS  Google Scholar 

  • Patterson, G.I., C.J. Thorpe, and V.L. Chandler. 1993 Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135:881–894.

    PubMed  CAS  Google Scholar 

  • Peredo, E.L., R. Arroyo-García, and B.M. Reed. 2009. Genetic stability of in vitro conserved germplasm of Humulus lupulus L. Agricultural and food science, Vol. 18. Nro 2:144–151.

    Article  Google Scholar 

  • Perruc, E., N. Kinoshita, and L. Lopez-Molina. 2007. The role of chromatin-remodeling factor PKL in balancing osmotic stress responses during Arabidopsis seed germination. Plant J. 52:927–936.

    Article  PubMed  CAS  Google Scholar 

  • Peschke, V.M. and R.L. Phillips. 1992. Genetic implications of somaclonal variations in plants. Adv. Genet. 30:41–75.

    Article  CAS  Google Scholar 

  • Pierik, R.L.M., P. van Leeuwen, and G.C.C.M. Rigter. 1979. Regeneration of leaf explants of Anthurium andreanum Lind. in vitro. Neth. J. Agric. Sci. 27:221–236.

    CAS  Google Scholar 

  • Pischke, M.S., E.L. Huttlin, A.D. Hegeman, and M.R. Sussman. 2006. A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol. 140:1255–1278.

    Article  PubMed  CAS  Google Scholar 

  • Pontes, O., C.F. Li, P.C. Nunes, J. Haag, T. Ream, A. Vitins, S.E. Jacobsen, and C.S. Pikaard. 2006. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92.

    Article  PubMed  CAS  Google Scholar 

  • Probst, A.V., M. Fagard, F. Proux, P. Mourrain, S. Boutet, K. Earley, R.J. Lawrence, C.S. Pikaard, J. Murfett, and I. Furner. 2004. Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034.

    Article  PubMed  CAS  Google Scholar 

  • Read, P.E. and A. Economou. 1982. Supplemental lighting in the propagation of deciduous azalea. Proc. Intl. Plant Propagators Soc. 32:639–645.

    Google Scholar 

  • Read, P.E. and J.E. Preece. 2009. Micropropagation of ornamentals: The wave of the future? Acta Hort. 812:51–62.

    Google Scholar 

  • Read, P.E., A.S. Economou, and C.D. Fellman. 1984. Manipulating stock plants for improved in vitro mass propagation, p. 467–473. In: F.J. Novak, L. Havel, and J. Dolezel (eds.). Proc. Intl. Symp. Plant Tissue Cell Cult. Application to crop improvement. Acad. Sci. Prague, Czech.

    Google Scholar 

  • Reyna-López, G.E., J. Simpson, and J. Ruiz-Herrera. 1997. Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol. Gen. Genet. 253:703–710.

    Article  PubMed  Google Scholar 

  • Rival, A., T. Beulé, F. Aberlenc Bertossi, J. Tregear, and E. Jaligot. 2010. Plant epigenetics: From genome to epigenomes. Notulae Botanicae Horti. Agrobotanici Cluj 38:9–15.

    CAS  Google Scholar 

  • Rodriguez, J.L., J. Pascual, M. Viejo, L. Valledor, M. Meijion, R. Hasbún, N.Y. Yrei, M.E. Santamaría, M. Pérez, M. Fernández Fraga, M. Berdasco, R. Rodríguez Fernández, and M.J. Cañal. 2012. Basic procedures for epigenetic analysis in plant cell and tissue culture. Methods Mol. Biol. 877:325–341.

    Article  PubMed  CAS  Google Scholar 

  • Roh, M.S. and M. Wocial. 1989. In vitro production of Achimenantha ‘Inferno’ as influenced by season and the source of the explants. Acta Hort. 252:129–136.

    Google Scholar 

  • Roh, T.Y., W.C. Ngau, K. Cui, D. Landsman, and K. Zhao. 2004. High-resolution genome-wide mapping of histone modifications. Nat. Biotechnol. 22:1013–1016.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, V., S. Locatelli, S., Varotto, G. Donn, R. Pirona, D.A. Henderson, H. Hartings, and M. Motto. 2007. Maize histone deacetylase hda101 is involved in plant development, gene transcription, and sequence-specific modulation of histone modification of genes and repeats. Plant Cell. 19:1145–1162.

    Article  PubMed  CAS  Google Scholar 

  • Roudier, F., F.K. Teixeira, and V. Colot. 2009. Chromatin indexing in Arabidopsis thaliana: An epigenomic tale of tails and more. Trends Genet. 25:511–517.

    Article  PubMed  CAS  Google Scholar 

  • Ruffoni, B., L. Pistelli, A. Bertoli, and L. Pistelli. 2010. Plant cell cultures: Bioreactors for industrial production. Adv. Expt. Med. Biol. 698:203–218.

    Article  CAS  Google Scholar 

  • Ruffoni, B., L. Semeria, M. Laura, M. Savona, and A. Bisio. 2005. In vitro morphogenesis and micropropagation of Anemone coronaria L. hybrids. Prop. Ornamental Plants 5(2):3–6.

    Google Scholar 

  • Sablowski, R. 2004. Plant and animal stem cells: Conceptually similar, molecularly distinct? Trends Cell Biol. 14:605–611.

    Article  PubMed  CAS  Google Scholar 

  • Saez, A., J. Rodrigues, S. Santiago, P. Rubio, and L. Rodriguez. 2008. HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis Plant Cell 20:2972–2988.

    Article  PubMed  CAS  Google Scholar 

  • Sakai, H., T. Honma, T. Aoyama, S. Sato, T. Kato, S. Tabata, and A. Oka. 2001. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519–1521.

    Article  PubMed  CAS  Google Scholar 

  • Savona, M., R. Mattioli, S. Nigro, G. Falasca, F. Della Rovere, P. Costantino, S. De Vries, B. Ruffoni, M. Trovato, and M.M. Altamura. 2012. Two SERK genes are markers of pluripotency in Cyclamen persicum Mill. J. Exp. Bot. 63:471–488.

    Article  PubMed  CAS  Google Scholar 

  • Schmitt, F., E.J. Oakeley, and J.P. Jost. 1997. Antibiotics induce genome-wide ypermethylation in cultured Nicotiana tabacum. Plants — J. Biol. Chem. 272:1534–1540.

    Article  CAS  Google Scholar 

  • Scippa, G.S., M. Di Michele, E. Onelli, G. Patrignani, D. Chiatante, and E.A. Bray. 2004. The histone-like protein H1-S and the response of tomato leaves to water deficit. J. Exp. Bot. 55:99–109.

    Article  PubMed  CAS  Google Scholar 

  • Shi, H., S.H. Wei, Y.W. Leu, F. Rahmatpanah, J.C. Liu, P.S. Yan, K.P. Nephew, and T.H.M. Huang. 2003. Triple analysis of the cancer epigenome: An integrated microarray system for assessing gene expression, DNA methylation, and histone acetylation. Cancer Res. 63:2164–2171.

    PubMed  CAS  Google Scholar 

  • Siebert, M., R.J. Wetherbee, and D.D. Job. 1975. The effects of light intensity and spectral quality on growth and shoot initiation in tobacco callus. Plant Physiol. 56:130–139.

    Article  Google Scholar 

  • Singh, M.B. and P.L. Bhalla. 2006. Plant stem cells carve their own niche. Trends Plant Sci. 11:241–246.

    Article  PubMed  CAS  Google Scholar 

  • Skoog, F. and C.O. Miller. 1957. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11:118–131.

    PubMed  CAS  Google Scholar 

  • Smulders, M.J.M. and G.J. De Klerk. 2011. Epigenetics in plant tissue culture. Plant Growth Regul. 63:137–146.

    Article  CAS  Google Scholar 

  • Smulders, M.J.M., W. Rus-Kortekaas, and B. Vosman. 1995. Tissue culture-induced DNA methylation polymorphisms in repetitive DNA of tomato calli and regenerated plants. Theor. Appl. Genet. 91:1257–1264.

    Article  CAS  Google Scholar 

  • Song, C.P., M. Agarwal, M. Ohta, Y. Guo, U. Halfter, P. Wang, and J.K. Zhu. 2005. Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses Plant Cell 17:2384–2396.

    Article  PubMed  CAS  Google Scholar 

  • Sridha. S. and K. Wu. 2006. Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J. 46:124–133.

    Article  PubMed  CAS  Google Scholar 

  • Steward, F.C., M.O. Mapes, and K. Mears. 1958. Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cells. Am. J. Bot. 45:705–708.

    Article  Google Scholar 

  • Sunkar, R., V. Chinnusamy, J. Zhu, and J.K. Zhu. 2007. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci. 12:301–309.

    Article  PubMed  CAS  Google Scholar 

  • Topoonyanont, N. and P.C. Debergh. 2001. Reducing bushiness in micropropagated gerbera. Plant Cell Tissue Organ. Cult. 67:133–144.

    Article  CAS  Google Scholar 

  • Tsuji, H., H. Saika, N. Tsutsumi, A. Hirai, and M. Nakazono. 2006. Dynamic and reversible changes in histone H3-Lys4 methylation and H3 acetylation occurring at submergence-inducible genes in rice. Plant Cell Physiol. 47:995–1003.

    Article  PubMed  CAS  Google Scholar 

  • Valledor, L, M. Meijon, R. Hasbun, M. Jesus Canal, and R. Rodriguez. 2010. Variations in DNA methylation, acetylated histone H4, and methylated histone H3 during Pinus radiata needle maturation in relation to the loss of in vitro organogenic capability. J. Plant Physiol. 167:351–357.

    Article  PubMed  CAS  Google Scholar 

  • Valledor, L., R. Hasbún, M. Meijón, J.L. Rodríguez, E. Santamará, M. Viejo, M. Berdasco, I. Feito, M.F. Fraga, M.J. Cañal, and R. Rodríguez. 2007. Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Organ. Cult. 91:75–86.

    Article  CAS  Google Scholar 

  • Van Staden, J., C.W. Fennell, and N.J. Taylor. 2006. Plant stress in vitro: The role of phytohormones. Acta Hort. 725:55–61.

    Google Scholar 

  • Vaucheret, H. 2006. Post-transcriptional small RNA pathways in plants: Mechanisms and regulations. Genes Dev. 20:759–771.

    Article  PubMed  CAS  Google Scholar 

  • Vaughn, M.W., M. Tanurdžić, Z. Lippman, H. Jiang, R. Carrasquillo, P.D. Rabinowicz, N. Dedhia, W.R. McCombie, N. Agier, A. Bulski, V. Colot, R.W. Doerge, and R.A. Martienssen. 2007. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol. 5:1617–1629.

    Article  CAS  Google Scholar 

  • Verdeil, J.L., L. Alemanno, N. Niemenak, and T.J. Tranbarger. 2007. Pluripotent versus totipotent plant stem cells: dependence versus autonomy? TRENDS in Plant Sci. 12(6):245–252.

    Article  CAS  Google Scholar 

  • Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van de Lee, M. Hornes, A. Frijters, J. Pot, J. Peleman, and M. Kuiper. 1995. AFLP: A new technique for DNA fingerprinting. Nucleic Acids Res. 21:4407–4414.

    Article  Google Scholar 

  • Waddington, C.H. 1942. The epigenotype. Endeavour 1:18–20.

    Google Scholar 

  • Wang, C., J. Xu, D. Zhang, Z. Wilson, and D. Zhang. 2010. An effective approach for identification of in vivo protein-DNA binding sites from paired-end ChlP-SEQ data. BMC Bioinformatics 11:81.

    Article  PubMed  CAS  Google Scholar 

  • Wang, P.J. and C.Y. Hu. 1982. In vitro mass tuberization and virus-free seed-potato production in Taiwan. Am. Potato J. 59:33–37.

    Article  Google Scholar 

  • Ward, H.B. and B.D. Vance. 1967. Effects of monochromatic radiation on growth of Pelargonium callus tissue. J. Exp. Bot. 19:119–124.

    Article  Google Scholar 

  • Weigel, D. and G. Jurgens. 2002. Stem cells that make stems. Nature 415:751–754.

    Article  PubMed  CAS  Google Scholar 

  • Werckmeister, P. 1971. Light induction of geotropism and the control of proliferation and growth of Cymbidium in tissue culture. Bot. Gaz. 132:346–350.

    Article  Google Scholar 

  • Werner, T., V. Motyka, V. Laucou, R. Smets, H. Van Onckelen, and T. Schmulling. 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550.

    Article  PubMed  CAS  Google Scholar 

  • Williams, L. and J.C. Fletcher. 2005. Stem cell regulation in the Arabidopsis shoot apical meristem. Curr. Opin. Plant Biol. 8:582–586.

    Article  PubMed  CAS  Google Scholar 

  • Xie, Z., L.K. Johansen, A.M. Gustafson, K.D. Kasschau, A.D. Lellis, D. Zilberman, S.E. Jacobsen, J.C. Carrington. 2004. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:e104.

    Article  PubMed  Google Scholar 

  • Xiong, Z. and P.W. Laird. 1997. COBRA: A sensitive and quantitative DNA methylation assay. Nucleic Acids Res. 25:2532–2534.

    Article  PubMed  CAS  Google Scholar 

  • Yeung, E.C. 1995. Structural and developmental patterns in somatic embryogenesis, p. 205–247. In: T.A. Thorpe (ed.). In vitro embryogenesis in plants. Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Zehr, B.E., M.E. Williams, D.R. Duncan, and J.M. Widholm. 1987. Somaclonal variation in the progeny of plants regenerated from callus cultures of seven inbred lines of maize. Can. J. Bot. 65: 491–499. DOI:10.1139/b87-061.

    Article  Google Scholar 

  • Zhang, K., V.V. Sridhar, J. Zhu, A. Kapoor, and J.K. Zhu. 2007. Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS ONE 2(11)e1210. DOI:10.1371/journal. pone.0001210.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Y., C. Rohde, S. Tieriing, T.P. Jurkowski, C. Bock, D. Santacruz, S. Ragozin, R. Reinhardt, M. Groth, J. Waiter, and A. Jeitsch. 2009. DNA methylation analysis of chromosome 21 gene promoters at single base pair and single allele resolution. PLoS Genet. 5(3):e1000438. DOI:10.1371/journal.pgen.1000438.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Z., S. Zhang, Y. Zhang, X. Wang, D. Li, Q. Li, M. Yue, Q. Li, Y.E. Zhang, Y. Xu, Y. Xue, K. Chong, and S. Bao. 2011. Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23:396–411.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, C., L. Zhang, J. Duan, B. Miki, and K. Wu. 2005. HISTONE DEACETYLASE19 is involved in jasmonic acid and ethylene signaling of pathogen response in Arabidopsis. Plant Cell 17:1196–1204.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J., J.C. Jeong, Y. Zhu, I. Sokolchik, S. Miyazaki, J.-K. Zhu, P.M. Hasegawa, H.J. Bohnert, H. Shi, D.-J. Yun, and R.A. Bressan. 2007. Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc. Natl. Acad. Sci. USA. 105:4945–4950.

    Article  Google Scholar 

  • Ziv, M. 1991. Vitrification: Morphological and physiological disorders of in vitro plants, p. 45–70. In: P.C. Debergh and R.H. Zimmerman (eds.). Micropropagation: Technology and applications. Kluwer Academic Publishers, Dordrecht.

    Chapter  Google Scholar 

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Ruffoni, B., Savona, M. Physiological and biochemical analysis of growth abnormalities associated with plant tissue culture. Hortic. Environ. Biotechnol. 54, 191–205 (2013). https://doi.org/10.1007/s13580-013-0009-y

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