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Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications

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Abstract

In vitro cell and tissue-based systems have tremendous potential in fundamental research and for commercial applications such as clonal propagation, genetic engineering and production of valuable metabolites. Since the invention of plant cell and tissue culture techniques more than half a century ago, scientists have been trying to understand the morphological, physiological, biochemical and molecular changes associated with tissue culture responses. Establishment of de novo developmental cell fate in vitro is governed by factors such as genetic make-up, stress and plant growth regulators. In vitro culture is believed to destabilize the genetic and epigenetic program of intact plant tissue and can lead to chromosomal and DNA sequence variations, methylation changes, transposon activation, and generation of somaclonal variants. In this review, we discuss the current status of understanding the genomic and epigenomic changes that take place under in vitro conditions. It is hoped that a precise and comprehensive knowledge of the molecular basis of these variations and acquisition of developmental cell fate would help to devise strategies to improve the totipotency and embryogenic capability in recalcitrant species and genotypes, and to address bottlenecks associated with clonal propagation.

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References

  • Agrawal GK, Yamazaki M, Kobayashi M, Hirochika R, Miyao A, Hirochika H (2001) Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel OsTATC gene. Plant Physiol 125:1248–1257

    Article  PubMed  CAS  Google Scholar 

  • Aichinger E, Villar CBR, Farrona S, Reyes JC, Hennig L, Köhler C (2009) CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5:e1000605

    Article  PubMed  CAS  Google Scholar 

  • Alemanno L, Devic M, Niemenak N, Sanier C, Guilleminot J, Rio M, Verdeil J-L, Montoro P (2008) Characterization of leafy cotyledon1-like during embryogenesis in Theobroma cacao L. Planta 227:853–866

    Article  PubMed  CAS  Google Scholar 

  • Almeida R, Allshire RC (2005) RNA silencing and genome regulation. Trends Cell Biol 15:251–258

    Article  PubMed  CAS  Google Scholar 

  • Alves E, Ballesteros I, Linacero R, Vázquez AM (2005) RYS1, a foldback transposon, is activated by tissue culture and shows preferential insertion points into the rye genome. Theor Appl Genet 111:431–436

    Article  PubMed  CAS  Google Scholar 

  • Andreev O, Spiridonova KV, Solovyan VT, Kunakh VA (2005) Variability of ribosomal RNA genes in Rauwolfia species: parallelism between tissue culture-induced rearrangements and interspecies polymorphism. Cell Biol Int 29:21–27

    Article  PubMed  CAS  Google Scholar 

  • Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Müllner AE, Luschnig C (2010) Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci USA 107:10308–10313

    Article  PubMed  CAS  Google Scholar 

  • Atta R, Laurens L, Boucheron-Dubuisson E, Guivarćh A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644

    Article  PubMed  CAS  Google Scholar 

  • Bairu MW, Aremu AO, Staden JV (2011) Somaclonal variation in plants: causes and detection methods. Plant Growth Regul 63:147–173

    Article  CAS  Google Scholar 

  • Banno H, Ikeda Y, Niu QW, Chua NH (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618

    Article  PubMed  CAS  Google Scholar 

  • Bao Y, Dharmawardhana P, Mockler TC, Strauss SH (2009) Genome scale transcriptome analysis of shoot organogenesis in Populus. BMC Plant Biol 9:132–146

    Article  PubMed  CAS  Google Scholar 

  • Barret P, Brinkman M, Beckert M (2006) A sequence related to rice Pong transposable element displays transcriptional activation by in vitro culture and reveals somaclonal variations in maize. Genome 49:1399–1407

    Article  PubMed  CAS  Google Scholar 

  • Bassuner BM, Lam R, Lukowitz W, Yeung EC (2007) Auxin and root initiation in somatic embryos of Arabidopsis. Plant Cell Rep 26:1–11

    Article  PubMed  CAS  Google Scholar 

  • Baudino S, Hansen S, Brettschneider R, Hecht VF, Dresselhaus T, Lörz H, Dumas C, Rogowsky PM (2001) Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta 213:1–10

    Article  PubMed  CAS  Google Scholar 

  • Bednarek PT, Orłowska R, Koebner RMD, Zimny J (2007) Quantification of the tissue-culture induced variation in barley (Hordeum vulgare L.). BMC Plant Biol 7:10–18

    Article  PubMed  CAS  Google Scholar 

  • Berdasco M, Alcázar R, García-Ortiz MV, Ballestar E, Fernández AF, Roldán-Arjona T, Tiburcio AF, Altabella T, Buisine N, Quesneville H, Baudry A, Lepiniec L, Alaminos M, Rodríguez R, Lloyd A, Colot V, Bender J, Canal MJ, Esteller M, Fraga MF (2008) Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells. PLoS One 3:e3306

    Article  PubMed  CAS  Google Scholar 

  • Bolibok H, Gruszczyńska A, Hromadajudycka A, Rakoczy-Trojanowska M (2007) The identification of QTLs associated with the in vitro response of rye (Secale cereale L.). Cell Mol Biol Lett 12:523–535

    Article  PubMed  CAS  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  PubMed  CAS  Google Scholar 

  • Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou JP, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7:e1002014

    Article  PubMed  CAS  Google Scholar 

  • Brettell RIS, Dennis ES (1991) Reactivation of a silent Ac following tissue culture is associated with heritable alterations in its methylation pattern. Mol Gen Genet 3:365–372

    Article  Google Scholar 

  • Brettell RIS, Dennis ES, Scowcroft WR, Peacock WJ (1986) Molecular analysis of a somaclonal variant of alcohol dehydrogenase. Mol Gen Genet 202:235–239

    Article  CAS  Google Scholar 

  • Cao X, Jacobsen SE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99:16491–16498

    Article  PubMed  CAS  Google Scholar 

  • Cary AJ, Che P, Howell SH (2002) Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J 32:867–877

    Article  PubMed  CAS  Google Scholar 

  • Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J (2004) Interaction of polycomb-group proteins controlling flowering in Arabidopsis. Development 131:5263–5276

    Article  PubMed  CAS  Google Scholar 

  • Che P, Love TM, Frame BR, Wang K, Carriquiry AL, Howell SH (2006a) Gene expression patterns during somatic embryo development and germination in maize Hi II callus culture. Plant Mol Biol 62:1–14

    Article  PubMed  CAS  Google Scholar 

  • Che P, Lall S, Nettleton D, Howell SH (2006b) Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol 141:620–637

    Article  PubMed  CAS  Google Scholar 

  • Che P, Lall S, Howell SH (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226:1183–1194

    Article  PubMed  CAS  Google Scholar 

  • Chen SK, Kurdyukov S, Kereszt A, Wang XD, Gresshoff PM, Rose RJ (2009a) The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula. Planta 230:827–840

    Article  PubMed  CAS  Google Scholar 

  • Chen X-Y, Kim ST, Cho WK, Rim Y, Kim S, Kim S-W, Kang KY, Park ZY, Kim J-Y (2009b) Proteomics of weakly bound cell wall proteins in rice calli. J Plant Physiol 166:675–685

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Molitor A, Liu C, Shen WH (2010) The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res 20:1332–1344

    Article  PubMed  CAS  Google Scholar 

  • Cheng C, Daigen M, Hirochika H (2006) Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics 276:378–390

    Article  PubMed  CAS  Google Scholar 

  • Chiappetta A, Fambrini M, Petrarulo M, Rapparini F, Michelotti V, Bruno L, Greco M, Baraldi R, Salvini M, Pugliesi C, Bitonti MB (2009) Ectopic expression of LEAFY COTYLEDON1-LIKE gene and localized auxin accumulation mark embryogenic competence in epiphyllous plants of Helianthus annuus × H. tuberosus. Ann Bot 103:735–747

    Article  PubMed  CAS  Google Scholar 

  • Cho WK, Chen XY, Chu H, Rim Y, Kim S, Kim ST, Kim S-W, Park Z-Y, Kim J-Y (2009) Proteomic analysis of the secretome of rice calli. Physiol Plant 135:331–341

    Article  PubMed  CAS  Google Scholar 

  • Christou P (1988) Habituation in in vitro soybean cultures. Plant Physiol 87:809–812

    Article  PubMed  CAS  Google Scholar 

  • Chuck G, Lincoln C, Hake S (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8:1277–1289

    Article  PubMed  CAS  Google Scholar 

  • Daimon Y, Takabe K, Tasaka M (2003) The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol 44:113–121

    Article  PubMed  CAS  Google Scholar 

  • Dean Rider S Jr, Henderson JT, Jerome RE, Edenberg HJ, Romero-Severson J, Ogas J (2003) Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J 35:33–43

    Article  PubMed  CAS  Google Scholar 

  • Deng W, Luo K, Li Z, Yang Y (2009) A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci 177:43–48

    Article  CAS  Google Scholar 

  • Dennis ES, Brettell RIS, Peacock WJ (1987) A tissue culture induced Adh1 null mutant of maize results from a single base change. Mol Gen Genet 210:181–183

    Article  CAS  Google Scholar 

  • Duclercq J, Sangwan-Norreel B, Catterou M, Sangwan RS (2011) De novo shoot organogenesis: from art to science. Trends Plant Sci. doi:10.1016/j.tplants.2011.08.004

  • Duncan DR, Kriz AL, Paiva R, Widholm JM (2003) Globulin-1 gene expression in regenerable Zea mays (maize) callus. Plant Cell Rep 21:684–689

    PubMed  CAS  Google Scholar 

  • Durante M, Cecchini E, Natali L, Citti L, Geri C, Parenti R, Nuti Ronchi V (1989) 5-Azacytidine-induced tumorous transformation and DNA hypomethylation in Nicotiana tissue cultures. Dev Genet 10:298–303

    Article  PubMed  CAS  Google Scholar 

  • Elhiti M, Tahir M, Gulden RH, Khamiss K, Stasolla C (2010) Modulation of embryo-forming capacity in culture through the expression of Brassica genes involved in the regulation of the shoot apical meristem. J Exp Bot 61:4069–4085

    Article  PubMed  CAS  Google Scholar 

  • Elhiti M, Ashihara H, Stasolla C (2011) Distinct fluctuations in nucleotide metabolism accompany the enhanced in vitro embryogenic capacity of Brassica cells over-expressing SHOOTMERISTEMLESS. Planta. doi:10.1007/s00425-011-1482-0

  • Evrensel C, Yilmaz S, Temel A, Gozukirmizi N (2011) Variations in BARE-1 insertion patterns in barley callus cultures. Genet Mol Res 10:980–987

    Article  PubMed  CAS  Google Scholar 

  • Fukai E, Umehara Y, Sato S, Endo M, Kouchi H, Hayashi M, Stougaard J, Hirochika H (2010) Derepression of the plant Chromovirus LORE1 induces germline transposition in regenerated plants. PLoS Genet 6:e1000868

    Article  PubMed  CAS  Google Scholar 

  • Fukuoka H, Kawata M, Tkaiwa M (1994) Molecular changes of organelle DNA sequences in rice through dedifferentiation, long-term culture or the morphogenesis process. Plant Mol Biol 26:899–907

    Article  PubMed  CAS  Google Scholar 

  • Furuta K, Kubo M, Sano K, Demura T, Fukuda H, Liu Y-G, Shibata D, Kakimoto T (2011) The CKH2/PKL chromatin remodeling factor negatively regulates cytokinin responses in Arabidopsis calli. Plant Cell Physiol 52:618–628

    Article  PubMed  CAS  Google Scholar 

  • Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988

    Article  PubMed  CAS  Google Scholar 

  • Gambino G, Minuto M, Boccacci P, Perrone I, Vallania R, Gribaudo I (2011) Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot 62:1089–1101

    Article  PubMed  CAS  Google Scholar 

  • Gernand D, Golczyk H, Rutten T, Ilnicki T, Houben A, Joachimiak AJ (2007) Tissue culture triggers chromosome alterations, amplification, and transposition of repeat sequences in Allium fistulosum. Genome 50:435–442

    Article  PubMed  CAS  Google Scholar 

  • Gong H, Jiao Y, Hu W–W, Pua E-C (2005) Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro. Plant Mol Biol 57:53–66

    Article  PubMed  CAS  Google Scholar 

  • Grafi G, Ben-Meir H, Avivi Y, Moshe M, Dahan Y, Zemach A (2007) Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation. Dev Biol 306:838–846

    Article  PubMed  CAS  Google Scholar 

  • Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3:181–187

    Article  Google Scholar 

  • Grandbastien M-A, Lucas H, Morel J-B, Mhiri C, Vernhettes S, Casacuberta JM (1997) The expression of the tobacco Tnt1 retrotransposon is linked to plant defense responses. Genetica 100:241–252

    Article  PubMed  CAS  Google Scholar 

  • Gruhler A, Schulze WX, Matthiesen R, Mann M, Jensen ON (2005) Stable isotope labeling of Arabidopsis thaliana cells and quantitative proteomics by mass spectrometry. Mol Cell Proteomics 4:1697–1709

    Article  PubMed  CAS  Google Scholar 

  • Guo WL, Wu R, Zhang YF, Liu XM, Wang HY, Gong L, Zhang ZH, Liu B (2007) Tissue culture-induced locus-specific alteration in DNA methylation and its correlation with genetic variation in Codonopsis lanceolata Benth. et Hook. Plant Cell Rep 26:1297–1307

    Article  PubMed  CAS  Google Scholar 

  • Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15. Plant Physiol 133:653–663

    Article  PubMed  CAS  Google Scholar 

  • Hecht V, Vielle-Calzada J-P, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis Somatic Embryogenesis Receptor Kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816

    Article  PubMed  CAS  Google Scholar 

  • Heidmann I, de Lange B, Lambalk J, Angenent GC, Boutilier K (2011) Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep 30:1107–1115

    Article  PubMed  CAS  Google Scholar 

  • Helleboid S, Bauw G, Belingheri L, Vasseur J, Hilbert JL (1998) Extracellular β-1,3-glucanases are induced during early somatic embryogenesis in Cichorium. Planta 205:56–63

    Article  PubMed  CAS  Google Scholar 

  • Helleboid S, Chapman A, Hendriks T, Inźe D, Vasseur J, Hilbert JL (2000) Cloning of β-1,3-glucanases expressed during Cichorium somatic embryogenesis. Plant Mol Biol 42:377–386

    Article  PubMed  CAS  Google Scholar 

  • Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826

    Article  PubMed  CAS  Google Scholar 

  • Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 12:2521–2528

    PubMed  CAS  Google Scholar 

  • Hirochika H (2001) Contribution of the Tos17 retrotransposon to rice functional genomics. Curr Opin Plant Biol 4:118–122

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta 222:107–117

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Zhang K, Shen Y, Huang Z, Li M, Tang D, Gu M, 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

    Article  PubMed  CAS  Google Scholar 

  • Ikeda Y, Banno H, Niu Q-W, Howell SH, Chua NH (2006) The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis regulates CUP-SHAPED COTYLEDON 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol 47:1443–1456

    Article  PubMed  CAS  Google Scholar 

  • Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063

    Article  PubMed  CAS  Google Scholar 

  • Iwase A, Mitsuda N, Koyama T, Hiratsu K, Kojima M, Arai T, Inoue Y, Seki M, Sakakibara H, Sugimoto K, Ohme-Takagi M (2011) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21:508–514

    Article  PubMed  CAS  Google Scholar 

  • Jain SM (2001) Tissue culture-derived variation in crop improvement. Euphytica 118:153–166

    Article  CAS  Google Scholar 

  • Jaligot E, Beulé T, Rival A (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 

  • Jaligot E, Adler S, Debladis E, Beulé T, Richaud F, Ilbert P, Finnegan EJ, Rival A (2011) Epigenetic imbalance and the floral developmental abnormality of the in vitro-regenerated oil palm Elaeis guineensis. Ann Bot. doi:10.1093/aob/mcq266

  • Jarillo JA, Piñeiro M, Cubas P, Martínez-Zapater JM (2009) Chromatin remodeling in plant development. Int J Dev Biol 53:1581–1596

    Article  PubMed  CAS  Google Scholar 

  • Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421:163–167

    Article  PubMed  CAS  Google Scholar 

  • Jiang C, Mithani A, Gan X, Belfield EJ, Klingler JP, Zhu J-K, Ragoussis J, Mott R, Harberd NP (2011) Regenerant Arabidopsis lineages display a distinct genome-wide spectrum of mutations conferring variant phenotypes. Curr Biol 21:1385–1390

    Article  PubMed  CAS  Google Scholar 

  • Jin S, Mushke R, Zhu H, Tu L, Lin Z, Zhang Y, Zhang X (2008) Detection of somaclonal variation of cotton (Gossypium hirsutum) using cytogenetics, flow cytometry and molecular markers. Plant Cell Rep 27:1303–1316

    Article  PubMed  CAS  Google Scholar 

  • Johnson SS, Phillips RL, Rines HW (1987) Possible role of heterochromatin in chromosome breakage induced by tissue culture in oats (Avena sativa L.). Genome 29:439–446

    Article  Google Scholar 

  • Johnson KL, Kibble NA, Bacic A, Schultz CJ (2011) A fasciclin-like arabinogalactan-protein (FLA) mutant of Arabidopsis thaliana, fla1, shows defects in shoot regeneration. PLoS One 6:e25154

    Article  PubMed  CAS  Google Scholar 

  • Jung Y-H, Jeong S-H, Kim SH, Singh R, Lee J, Cho Y-S, Agrawal GK, Rakwal R, Jwa N-S (2008) Systematic secretome analyses of rice leaf and seed callus suspension-cultured cells: workflow development and establishment of high-density two-dimensional gel reference maps. J Proteome Res 7:5187–5210

    Article  PubMed  CAS  Google Scholar 

  • Kaeppler SM, Phillips RL (1993a) DNA methylation and tissue culture-induced variation in plants. In Vitro Cell Dev Biol 29P:125–130

    CAS  Google Scholar 

  • Kaeppler SM, Phillips RL (1993b) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci USA 90:8773–8776

    Article  PubMed  CAS  Google Scholar 

  • Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188

    Article  PubMed  CAS  Google Scholar 

  • Kakani A, Li G, Peng Z (2009) Role of AUX1 in the control of organ identity during in vitro organogenesis and in mediating tissue specific auxin and cytokinin interaction in Arabidopsis. Planta 229:645–657

    Article  PubMed  CAS  Google Scholar 

  • Kandasamy MK, Gilliland LU, McKinney EC, Meagher RB (2001) One plant Actin isovariant, ACT7, is induced by auxin and required for normal callus formation. Plant Cell 13:1541–1554

    Article  PubMed  CAS  Google Scholar 

  • Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S (2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18:626–638

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi K, Terauchi K, Wada M, Hirano HY (2003) The plant MITE mPing is mobilized in anther culture. Nature 421:167–170

    Article  PubMed  CAS  Google Scholar 

  • Komatsu M, Shimamoto K, Kyozuka J (2003) Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon Karma. Plant Cell 15:1934–1944

    Article  PubMed  CAS  Google Scholar 

  • Koukalova B, Fojtova M, Lim KY, Fulnecek J, Leitch AR, Kovarik A (2005) Dedifferentiation of tobacco cells is associated with ribosomal RNA gene hypomethylation, increased transcription, and chromatin alterations. Plant Physiol 139:275–286

    Article  PubMed  CAS  Google Scholar 

  • Kour GL, Kour B, Kaul S, Dhar MK (2009) Genetic and epigenetic instability of amplification-prone sequences of a novel B chromosome induced by tissue culture in Plantago lagopus. Plant Cell Rep 28:1857–1867

    Article  PubMed  CAS  Google Scholar 

  • Krakowsky MD, Lee M, Garay L, Woodman-Clikeman W, Long MJ, Sharopova N, Frame B, Wang K (2006) Quantitative trait loci for callus initiation and totipotency in maize (Zea mays L.). Theor Appl Genet 113:821–830

    Article  PubMed  CAS  Google Scholar 

  • Krsnik-Rasol M (1991) Peroxidase as a developmental marker in plant tissue culture. Int J Dev Biol 35:259–263

    PubMed  CAS  Google Scholar 

  • Kubis SE, Castilho AM, Vershinin AV, Heslop-Harrison JS (2003) Retroelements, transposons and methylation status in the genome of oil palm (Elaeis guineensis) and the relationship to somaclonal variation. Plant Mol Biol 52:69–79

    Article  PubMed  CAS  Google Scholar 

  • La H, Ding B, Mishra GP, Zhou B, Yang H, Bellizzi Mdel R, Chen S, Meyers BC, Peng Z, Zhu JK, Wang GL (2011) A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proc Natl Acad Sci USA. doi:10.1073/pnas.1112704108

  • Ladyżyński M, Burza W, Malepszy S (2002) Relationship between somaclonal variation and type of culture in cucumber. Euphytica 125:349–356

    Article  Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation: a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214

    Article  Google Scholar 

  • Larkin PJ, Scowcroft WR (1983) Somaclonal variation and crop improvement. In: Kosuge T et al (eds) Genetic engineering of plants: an agricultural perspective. Plenum, New York, pp 289–314

    Google Scholar 

  • Leal F, Loureiro J, Rodriguez E, Pais MS, Santos C, Pinto-Carnide O (2006) Nuclear DNA content of Vitis vinifera cultivars and ploidy level analyses of somatic embryo-derived plants obtained from anther culture. Plant Cell Rep 25:978–985

    Article  PubMed  CAS  Google Scholar 

  • Ledwoń A, Gaj MD (2009) LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Rep 28:1677–1688

    Article  PubMed  CAS  Google Scholar 

  • Lee ML, Phillips RL (1987) Genomic rearrangements in maize induced by tissue culture. Genome 29:122–128

    Article  Google Scholar 

  • Leljak-Levanić D, Bauer N, Mihaljević S, Jelaska S (2004) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23:120–127

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Butenko Y, Grafi G (2005) Histone deacetylation is required for progression through mitosis in tobacco cells. Plant J 41:346–352

    Article  PubMed  CAS  Google Scholar 

  • Li X, Yu X, Wang N, Feng Q, Dong Z, Liu L, Shen J, Liu B (2007) Genetic and epigenetic instabilities induced by tissue culture in wild barley (Hordeum brevisubulatum (Trin.) Link). Plant Cell Tiss Organ Cult 90:153–168

    Article  Google Scholar 

  • Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243

    Article  PubMed  CAS  Google Scholar 

  • Lin X, Long L, Shan X, Zhang S, Shen S, Liu B (2006) In planta mobilization of mPing and its putative autonomous element Pong in rice by hydrostatic pressurization. J Exp Bot 57:2313–2323

    Article  PubMed  CAS  Google Scholar 

  • Linacero RE, Alves F, Vazquez AM (2000) Hot spots of DNA instability revealed through the study of somaclonal variation. Theor Appl Genet 100:506–511

    Article  CAS  Google Scholar 

  • Linkiewicz A, Filipeck M, Tomczak A, Grabowska A, Malepszy S (2004) The cloning of sequences differentially transcribed during the induction of somatic embryogenesis in cucumber (Cucumis sativus L.). Cell Mol Biol Lett 9:795–804

    PubMed  CAS  Google Scholar 

  • Liu B, Wendel JF (2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43:874–880

    Article  PubMed  CAS  Google Scholar 

  • Liu L, White MJ, MacRae TH (1999) Transcription factors and their genes in higher plants. Functional domains, evolution and regulation. Eur J Biochem 262:247–257

    Article  PubMed  CAS  Google Scholar 

  • Liu ZL, Han FP, Tan M, Shan XH, Dong YZ, Wang XZ, Fedak G, Hao S, Liu B (2004) Activation of a rice endogenous retrotransposon Tos17 in tissue culture is accompanied by cytosine demethylation and causes heritable alteration in methylation pattern of flanking genomic regions. Theor Appl Genet 109:200–209

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Yu CW, Duan J, Luo M, Wang K, Tian G, Cui Y, Wu K (2011) HDA6 directly interacts with DNA methyltransferase MET1 and maintains transposable elements silencing in Arabidopsis. Plant Physiol. doi:10.1104/pp.111.184275

  • Long L, Ou X, Liu J, Lin X, Sheng L, Liu B (2009) The spaceflight environment can induce transpositional activation of multiple endogenous transposable elements in a genotype-dependent manner in rice. J Plant Physiol 166:2035–2045

    Article  PubMed  CAS  Google Scholar 

  • López CMR, Wetten AC, Wilkinson MJ (2010) Progressive erosion of genetic and epigenetic variation in callus-derived cocoa (Theobroma cacao) plants. New Phytol 186:856–868

    Article  CAS  Google Scholar 

  • LoSchiavo F, Pitto L, Giuliano G, Torti G, Nuti-Ronchi V, Marazziti D, Vergara R, Orselli S, Terzi M (1989) DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiation, hormones and hypomethylating drugs. Theor Appl Genet 77:325–331

    Article  CAS  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong W, Yamagishi K, Fisher RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAF COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  PubMed  CAS  Google Scholar 

  • Lowe K, Hoerster G, Sun X, Scelonge C, Bao Z, Newman L, Zhang J, Shen B, Bruce W, Gordon-Kamm W (2011) Tetracycline-inducible expression of the ODP2 gene in maize produces callus from leaves. In vitro biology meeting proceedings, P-3018

  • Lu S, Peng X, Guo Z, Zhang G, Wang Z, Wang C, Pang C, Fan Z, Wang J (2007) In vitro selection of salinity tolerant variants from triploid bermudagrass (Cynodon transvaalensis × C. dactylon) and their physiological responses to salt and drought stress. Plant Cell Rep 26:1413–1420

    Article  PubMed  CAS  Google Scholar 

  • Luo Y-C, Zhou H, Li Y, Chen J-Y, Yang J-H, Chen Y-Q, Qu L-H (2006) Rice embryogenic calli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant post-embryogenic development. FEBS Lett 580:5111–5116

    Article  PubMed  CAS  Google Scholar 

  • Madlung A, Comai L (2004) The effect of stress on genome regulation and structure. Ann Bot 94:481–495

    Article  PubMed  CAS  Google Scholar 

  • Mangolin CA, Prioli AJ, Machado MF (1994) Isozyme patterns in callus cultures and in plants regenerated from calli of Cereus peruvianus (Cactaceae). Biochem Genet 32:237–247

    Article  PubMed  CAS  Google Scholar 

  • Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang X-D, VandenBosch KA, Rose RJ (2008) The transcription factor MtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiol 146:1622–1636

    Article  PubMed  CAS  Google Scholar 

  • Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22:1104–1117

    Article  PubMed  CAS  Google Scholar 

  • Marsch-Martinez N, Greco R, Becker JD, Dixit S, Bergervoet JH, Karaba A, de Folter S, Pereira A (2006) BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol Biol 62:825–843

    Article  PubMed  CAS  Google Scholar 

  • Marsoni M, Bracale M, Espen L, Prinsi B, Negri AS, Vannini C (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Rep 27:347–356

    Article  PubMed  CAS  Google Scholar 

  • Martin RC, Liu PP, Goloviznina NA, Nonogaki H (2010) MicroRNA, seeds, and Darwin? Diverse function of miRNA in seed biology and plant responses to stress. J Exp Bot 61:2229–2234

    Article  PubMed  CAS  Google Scholar 

  • Mathieu M, Lelu-Walter MA, Blervacq AS, David H, Hawkins S, Neutelings G (2006) Germin-like genes are expressed during somatic embryogenesis and early development of conifers. Plant Mol Biol 61:615–627

    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. Annu Rev Genet 23:395–408

    Article  PubMed  CAS  Google Scholar 

  • Mhiri C, Morel J-B, Vernhettes S, Casacuberta JM, Lucas H, Grandbastien M-A (1997) The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol 33:257–266

    Article  PubMed  CAS  Google Scholar 

  • Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot. doi:10.1093/jxb/err155

  • Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimadak H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214

    Article  PubMed  CAS  Google Scholar 

  • Miwa H, Kinoshita A, Fukuda H, Sawa S (2009) Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J Plant Res 122:31–39

    Article  PubMed  CAS  Google Scholar 

  • Momose M, Abe Y, Ozeki Y (2010) Miniature inverted-repeat transposable elements of Stowaway are active in potato. Genetics 186:59–66

    Article  PubMed  CAS  Google Scholar 

  • Morcillo F, Gallard A, Pillot M, Jouannic S, Aberlenc-Bertossi F, Collin M, Verdeil JL, Tregear JW (2007) EgAP2-1, an AINTEGUMENTA-like (AIL) gene expressed in meristematic and proliferating tissues of embryos in oil palm. Planta 226:1353–1362

    Article  PubMed  CAS  Google Scholar 

  • Morgens PH, Grabau EA, Gesteland RF (1984) A novel soybean mitochondrial transcript resulting from a DNA rearrangement involving the 5S rRNA gene. Nucleic Acids Res 12:5665–5684

    Article  PubMed  CAS  Google Scholar 

  • Morris DA (2000) Transmembrane auxin carrier systems—dynamic regulators of polar auxin transport. Plant Growth Regul 32:161–172

    Article  PubMed  CAS  Google Scholar 

  • Motte H, Verstraeten I, Werbrouck S, Geelen D (2011) CUC2 as an early marker for regeneration competence in Arabidopsis root explants. J Plant Physiol 168:1598–1601

    Article  PubMed  CAS  Google Scholar 

  • Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, Inoue H, Tanisaka T (2003) Mobilization of a transposon in the rice genome. Nature 421:170–172

    Article  PubMed  CAS  Google Scholar 

  • Ngezahayo F, Xu C, Wang H, Jiang L, Pang J, Liu B (2009) Tissue culture-induced transpositional activity of mPing is correlated with cytosine methylation in rice. BMC Plant Biol 9:91–105

    Article  PubMed  CAS  Google Scholar 

  • Nolan KE, Saeed NA, Rose RJ (2006) The stress kinase gene MtSK1 in Medicago truncatula with particular reference to somatic embryogenesis. Plant Cell Rep 25:711–722

    Article  PubMed  CAS  Google Scholar 

  • Ogas J, Cheng J-C, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–94

    Article  PubMed  CAS  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96:13839–13844

    Article  PubMed  CAS  Google Scholar 

  • Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased thermotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58:3373–3383

    Article  PubMed  CAS  Google Scholar 

  • Ouakfaoui SE, Schnell J, Abdeen A, Colville A, Labbé H, Han S, Baum B, Laberge S, Miki B (2010) Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 74:313–326

    Article  PubMed  CAS  Google Scholar 

  • Ozeki Y, Davies E, Takeda J (1997) Somatic variation during long term subculturing of plant cells caused by insertion of a transposable element in a phenylalanine ammonia-lyase (PAL) gene. Mol Gen Genet 254:407–416

    Article  PubMed  CAS  Google Scholar 

  • Palama TL, Menard P, Fock I, Choi YH, Bourdon E, Govinden-Soulange J, Bahut M, Payet B, Verpoorte R, Kodja H (2010) Shoot differentiation from protocorm callus cultures of Vanilla planifolia (Orchidaceae): proteomic and metabolic responses at early stage. BMC Plant Biol 10:82

    Article  PubMed  CAS  Google Scholar 

  • Palovaara J, Hakman I (2008) Conifer WOX-related homeodomain transcription factors, developmental consideration and expression dynamic of WOX2 during Picea abies somatic embryogenesis. Plant Mol Biol 66:533–549

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Murthy HN, Chakrabarthy D, Paek KY (2009) Detection of epigenetic variation in tissue culture derived plants of Doritaenopsis by methylation sensitive amplification polymorphism (MSAP) analysis. In Vitro Cell Dev Biol Plant 45:104–108

    Article  CAS  Google Scholar 

  • Park S-Y, Klimaszewska K, Park J-Y, Mansfield SD (2010) Lodgepole pine: the first evidence of seed-based somatic embryogenesis and the expression of embryogenesis marker genes in shoot bud cultures of adult trees. Tree Physiol 30:1469–1478

    Article  PubMed  CAS  Google Scholar 

  • Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van der Geest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68:225–237

    Article  PubMed  CAS  Google Scholar 

  • Peredo EL, Revilla MA, Arroyo-García R (2006) Assessment of genetic and epigenetic variation in hop plants regenerated from sequential subcultures of organogenic calli. J Plant Physiol 163:1071–1079

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Núñez MT, Souza R, Sáenz L, Chan JL, Zúñiga-Aguilar JJ, Oropeza C (2009) Detection of a SERK-like gene in coconut and analysis of its expression during the formation of embryogenic callus and somatic embryos. Plant Cell Rep 28:11–19

    Article  PubMed  CAS  Google Scholar 

  • Peschke VM, Phillips RL (1991) Activation of the maize transposable element Suppressor-mutator (Spm) in tissue culture. Theor Appl Genet 81:90–97

    Article  Google Scholar 

  • Peschke VM, Phillips RL, Gengenbach BG (1987) Discovery of transposable element activity among progeny of tissue culture-derived maize plants. Science 238:804–807

    Article  PubMed  CAS  Google Scholar 

  • Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci USA 91:5222–5226

    Article  PubMed  CAS  Google Scholar 

  • Picault N, Chaparro C, Piegu B, Stenger W, Formey D, Llauro C, Descombin J, Sabot F, Lasserre E, Meynard D, Guiderdoni E, Panaud O (2009) Identification of an active LTR retrotransposon in rice. Plant J 58:754–765

    Article  PubMed  CAS  Google Scholar 

  • Pischke MS, Huttlin EL, Hegeman AD, Sussman MR (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140:1255–1278

    Article  PubMed  CAS  Google Scholar 

  • Planckaert F, Walbot V (1989) Molecular and genetic characterization of Mu transposable elements in Zea mays: behavior in callus culture and regenerated plants. Genetics 123:567–578

    PubMed  CAS  Google Scholar 

  • Pouteau S, Huttner E, Grandbastien MA, Caboche M (1991) Specific expression of the tobacco Tnt1 retrotransposon in protoplasts. EMBO J 10:1911–1918

    PubMed  CAS  Google Scholar 

  • Pouteau S, Grandbastien M-A, Boccara M (1994) Microbial elicitors of plant defence responses activate transcription of a retrotransposon. Plant J 5:535–542

    Article  CAS  Google Scholar 

  • Pryor A, Faulker K, Rhoades MM, Peacock WJ (1980) Asynchronous replication of heterochromatin in maize. Proc Natl Acad Sci USA 77:6705–6709

    Article  PubMed  CAS  Google Scholar 

  • Rakocevic A, Mondy S, Tirichine L, Cosson V, Brocard L, Iantcheva A, Cayrel A, Devier B, Abu El-Heba GA, Ratet P (2009) MERE1, a low-copy-number copia-type retroelement in Medicago truncatula active during tissue culture. Plant Physiol 151:1250–1263

    Article  PubMed  CAS  Google Scholar 

  • Rhee Y, Lin H, Buell R, Childs K, Kaeppler S (2009) Ac2 allele of maize identified in regenerant-derived progeny from tissue culture results from insertion of a novel transposon. Maydica 54:429–437

    Google Scholar 

  • Rhee Y, Sekhon RS, Chopra S, Kaeppler S (2010) Tissue culture-induced novel epialleles of a Myb transcription factor encoded by pericarp color1 in maize. Genetics 186:843–855

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Enriquez J, Dickinson HG, Grant-Downton RT (2011) MicroRNA misregulation: an overlooked factor generating somaclonal variation? Trends Plant Sci 16:242–248

    Article  PubMed  CAS  Google Scholar 

  • Romanov GA, Lomin SN, Schmülling T (2006) Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. J Exp Bot 57:4051–4058

    Article  PubMed  CAS  Google Scholar 

  • Ruzicka DR, Kandasamy MK, McKinney EC, Burgos-Rivera B, Meagher RB (2007) The ancient subclasses of Arabidopsis ACTIN DEPOLYMERIZING FACTOR genes exhibit novel and differential expression. Plant J 52:460–472

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Sentoku N, Miura Y, Hirochika H, Kitano H, Matsuoka M (1999) Loss-of-function mutations in the rice homeobox gene OSH15 affect the architecture of internodes resulting in dwarf plants. EMBO J 18:992–1002

    Article  PubMed  CAS  Google Scholar 

  • Sato M, Kawabe T, Hosokawa M, Tatsuzawa F, Doi M (2011a) Tissue culture-induced flower-color changes in Saintpaulia caused by excision of the transposon inserted in the flavonoid 3′,5′ hydroxylase (F3′5′H) promoter. Plant Cell Rep 30:929–939

    Article  PubMed  CAS  Google Scholar 

  • Sato M, Hosokawa M, Doi M (2011b) Somaclonal variation is induced de novo via the tissue culture process: a study quantifying mutated cells in Saintpaulia. PLoS One 6:e23541

    Article  PubMed  CAS  Google Scholar 

  • Schellenbaum P, Jacques A, Maillot P, Bertsch C, Mazet F, Farine S, Walter B (2008a) Characterization of VvSERK1, VvSERK2, VvSERK3 and VvL1L genes and their expression during somatic embryogenesis of grapevine (Vitis vinifera L.). Plant Cell Rep 27:1799–1809

    Article  PubMed  CAS  Google Scholar 

  • Schellenbaum P, Mohler V, Wenzel G, Walter B (2008b) Variation in DNA methylation patterns of grapevine somaclones (Vitis vinifera L.). BMC Plant Biol 8:78

    Google Scholar 

  • Schmidt ED, Guzzo F, Toonen M, de Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062

    PubMed  CAS  Google Scholar 

  • Schmitt F, Oakeley EJ, Jost JP (1997) Antibiotics induce genome-wide hypermethylation in cultured Nicotiana tabacum plants. J Biol Chem 272:1534–1540

    Article  PubMed  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M, Kohlberg S, Sgro J, Delgado B, Mead K, Chinwalla A, Leonard S, Crouse K, Collura K, Kudrna D, Currie J, He R, Angelova A, Rajasekar S, Mueller T, Lomeli R, Scara G, Ko A, Delaney K, Wissotski M, Lopez G, Campos D, Braidotti M, Ashley E, Golser W, Kim H, Lee S, Lin J, Dujmic Z, Kim W, Talag J, Zuccolo A, Fan C, Sebastian A, Kramer M, Spiegel L, Nascimento L, Zutavern T, Miller B, Ambroise C, Muller S, Spooner W, Narechania A, Ren L, Wei S, Kumari S, Faga B, Levy MJ, McMahan L, Van Buren P, Vaughn MW, Ying K, Yeh CT, Emrich SJ, Jia Y, Kalyanaraman A, Hsia AP, Barbazuk WB, Baucom RS, Brutnell TP, Carpita NC, Chaparro C, Chia JM, Deragon JM, Estill JC, Fu Y, Jeddeloh JA, Han Y, Lee H, Li P, Lisch DR, Liu S, Liu Z, Nagel DH, McCann MC, SanMiguel P, Myers AM, Nettleton D, Nguyen J, Penning BW, Ponnala L, Schneider KL, Schwartz DC, Sharma A, Soderlund C, Springer NM, Sun Q, Wang H, Waterman M, Westerman R, Wolfgruber TK, Yang L, Yu Y, Zhang L, Zhou S, Zhu Q, Bennetzen JL, Dawe RK, Jiang J, Jiang N, Presting GG, Wessler SR, Aluru S, Martienssen RA, Clifton SW, McCombie WR, Wing RA, Wilson RK (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Google Scholar 

  • Schütz W, Hausmann N, Krug K, Hampp R, Macek B (2011) Extending SILAC to proteomics of plant cell lines. Plant Cell 23:1701–1705

    Article  PubMed  CAS  Google Scholar 

  • Shibukawa T, Yazawa K, Kikuchi A, Kamada H (2009) Possible involvement of DNA methylation on expression regulation of carrot LEC1 gene in its 5′-upstream region. Gene 437:22–31

    Article  PubMed  CAS  Google Scholar 

  • Singla B, Tyagi AK, Khurana JP, Khurana P (2007) Analysis of expression profile of selected genes expressed during auxin-induced somatic embryogenesis in leaf base system of wheat (Triticum aestivum) and their possible interactions. Plant Mol Biol 65:677–692

    Article  PubMed  CAS  Google Scholar 

  • Singla B, Khurana JP, Khurana P (2008) Characterization of three somatic embryogenesis receptor kinase genes from wheat, Triticum aestivum. Plant Cell Rep 27:833–843

    Article  PubMed  CAS  Google Scholar 

  • Sinha N, Williams R, Hake S (1993) Overexpression of the maize homeobox gene, Knotted1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–795

    Article  PubMed  CAS  Google Scholar 

  • Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 54:118–130

    Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  PubMed  CAS  Google Scholar 

  • Smulders MJM, de Klerk GJ (2011) Epigenetics in plant tissue culture. Plant Growth Regul 63:137–146

    Article  CAS  Google Scholar 

  • Smýkal P, Valledor L, Rodríguez R, Griga M (2007) Assessment of genetic and epigenetic stability in long-term in vitro shoot culture of pea (Pisum sativum L.). Plant Cell Rep 26:1985–1998

    Article  PubMed  CAS  Google Scholar 

  • Song X, Han Y, Teng W, Sun G, Li W (2010) Identification of QTL underlying somatic embryogenesis capacity of immature embryos in soybean (Glycine max (L.) Merr.). Plant Cell Rep 29:125–131

    Article  PubMed  CAS  Google Scholar 

  • Sotirova V, Shtereva L, Zagorska N, Dimitrov B, Bogatsevska N (1999) Resistance responses of plants regenerated from tomato anther and somatic tissue cultures to Clavibacter michiganense. Israel J Plant Sci 47:237–243

    Google Scholar 

  • Sreedhar RV, Venkatachalam L, Bhagyalakshmi N (2007) Genetic fidelity of long-term micropropagated shoot cultures of vanilla (Vanilla planifolia Andrews) as assessed by molecular markers. Biotechnol J 2:1007–1013

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan C, Liu Z, Heidmann I, Supena ED, Fukuoka H, Joosen R, Lambalk J, Angenent G, Scorza R, Custers JB, Boutilier K (2007) Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta 225:341–351

    Article  PubMed  CAS  Google Scholar 

  • Steward FC, Mapes MO, Kent AE, Holsten RD (1964) Growth and development of cultured plant cells. Science 143:20–27

    Article  PubMed  CAS  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    Article  PubMed  CAS  Google Scholar 

  • Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59:448–460

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Wang HHY, McCarty DR (2007) Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes. Plant Physiol 143:902–911

    Article  PubMed  CAS  Google Scholar 

  • Taguchi-Shiobara F, Yamamoto T, Yano M, Oka S (2006) Mapping QTLs that control the performance of rice tissue culture and evaluation of derived near-isogenic lines. Theor Appl Genet 112:968–976

    Article  PubMed  CAS  Google Scholar 

  • Takada S, Hibara K, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135

    PubMed  CAS  Google Scholar 

  • Takeda S, Sugimoto K, Otsuki H, Hirochika H (1999) A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J 18:383–393

    Article  PubMed  CAS  Google Scholar 

  • Tanaka M, Kikuchi A, Kamada H (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146:149–161

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Newton RJ (2005) Mevalonate kinase activity during different stages of plant regeneration from nodular callus cultures in white pine (Pinus strobus). Tree Physiol 26:195–200

    Article  CAS  Google Scholar 

  • Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6:2880–2895

    Article  PubMed  CAS  Google Scholar 

  • Tenedini E, Roncaglia E, Ferrari F, Orlandi C, Bianchi E, Bicciato S, Tagliafico E, Ferrari S (2010) Integrated analysis of microRNA and mRNA expression profiles in physiological myelopoiesis: role of hsa-mir-299–5p in CD34+ progenitor cells commitment. Cell Death Dis 1:e28

    Article  PubMed  CAS  Google Scholar 

  • Thakare D, Tang W, Hill K, Perry SE (2008) The MADS-domain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol 146:1663–1672

    Article  PubMed  CAS  Google Scholar 

  • Thomas C, Meyer D, Himber C, Steinmetz A (2004) Spatial expression of a sunflower SERK gene during induction of somatic embryogenesis and shoot organogenesis. Plant Physiol Biochem 42:35–42

    Article  PubMed  CAS  Google Scholar 

  • Tsuwamoto R, Yokoi S, Takahata Y (2010) Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 73:481–492

    Article  PubMed  CAS  Google Scholar 

  • Uddenberg D, Valladares S, Abrahamsson M, Sundström JF, Sundås-Larsson A, von Arnold S (2011) Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta. doi:10.1007/s00425-011-1418-8

  • van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, de Vries SC (2001) N-Acetylglucosamine and glucosaminecontaining arabinogalactan proteins control somatic embryogenesis. Plant Physiol 125:1880–1890

    Article  PubMed  Google Scholar 

  • Verdeil J-L, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252

    Article  PubMed  CAS  Google Scholar 

  • Vicient CM (2010) Transcriptional activity of transposable elements in maize. BMC Genomics 11:601–610

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16:1206–1219

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Elhiti M, Hebelstrup KH, Hill RD, Stasolla C (2011) Manipulation of hemoglobin expression affects Arabidopsis shoot organogenesis. Plant Physiol Biochem. doi:10.1016/j.plaphy.2011.06.005

  • Weber J, Georgiev V, Pavlov A, Bley T (2008) Flow cytometric investigations of diploid and tetraploid plants and in vitro cultures of Datura stramonium and Hyoscyamus niger. Cytometry A 73:931–939

    PubMed  Google Scholar 

  • Willmann MR, Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10:503–511

    Article  PubMed  CAS  Google Scholar 

  • Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155:1871–1884

    Article  PubMed  CAS  Google Scholar 

  • Wrather JA, Freytag AH (1991) Selection of atrazine tolerant soybean calli and expression of that tolerance in regenerated plants. Plant Cell Rep 10:44–47

    Article  CAS  Google Scholar 

  • Wu X-M, Liu M-Y, Ge X–X, Xu Q, Guo W–W (2011) Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 233:495–505

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi M, Kato H, Yoshida S, Yamamura S, Uchimiya H, Umeda M (2003) Control of in vitro organogenesis by cyclin dependent kinase activities in plants. Proc Natl Acad Sci USA 100:8019–8023

    Article  PubMed  CAS  Google Scholar 

  • Yamashita H, Tahara M (2006) A LINE-type retrotransposon active in meristem stem cells causes heritable transpositions in the sweet potato genome. Plant Mol Biol 61:79–94

    Article  PubMed  CAS  Google Scholar 

  • Yin L, Tao Y, Zhao K, Shao J, Li X, Liu G, Liu S, Zhu L (2007) Proteomic and transcriptomic analysis of rice mature seed-derived callus differentiation. Proteomics 7:755–768

    Article  PubMed  CAS  Google Scholar 

  • Yin L, Lan Y, Zhu L (2008) Analysis of the protein expression profiling during rice callus differentiation under different plant hormone conditions. Plant Mol Biol 68:597–617

    Article  PubMed  CAS  Google Scholar 

  • Yoshii M, Shimizu T, Yamazaki M, Higashi T, Miyao A, Hirochika H, Omura T (2009) Disruption of a novel gene for a NAC-domain protein in rice confers resistance to rice dwarf virus. Plant J 57:615–625

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Feng Z, Wang G, Li F, Du X, Zhu J (2010) Initiation of dedifferentiation and structural changes in in vitro cultured petiole of Arabidopsis thaliana. Protoplasma 241:75–81

    Article  PubMed  Google Scholar 

  • Yu X, Li X, Zhao X, Jiang L, Miao G, Pang J, Qi X, Liu B (2011) Tissue culture-induced genomic alteration in maize (Zea mays) inbred lines and F1 hybrids. Ann Appl Biol 158:237–247

    Article  CAS  Google Scholar 

  • Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y (2006) Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Mol Biol 60:167–183

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Wong L, Meng L, Lemaux PG (2002) Similarity of expression patterns of knotted1 and ZmLEC1 during somatic and zygotic embryogenesis in maize (Zea mays L.). Planta 215:191–194

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Xu C, Yan H, Zhao N, Wettstein DV, Liu B (2009) Limited tissue culture-induced mutations and linked epigenetic modifications in F1 hybrids of sorghum pure lines are accompanied by increased transcription of DNA methyltransferases and 5-methylcytosine glycosylases. Plant J 57:666–679

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Wang H, Dong Z, Qi B, Xu K, Liu B (2010a) Tissue culture-induced variation at simple sequence repeats in sorghum (Sorghum bicolor L.) is genotype-dependent and associated with down-regulated expression of a mismatch repair gene, MLH3. Plant Cell Rep 29:51–59

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Qi L (2010b) Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem Biophys Res Commun 398:355–360

    Article  PubMed  CAS  Google Scholar 

  • Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009) Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21:2563–2577

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman L (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5:1411–1423

    Article  PubMed  Google Scholar 

  • Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Special thanks to Bronwyn Frame, Diane Luth, Marcy Main and Susana Martin-Ortigosa for critical reading of the manuscript and constructive comments. We wish to apologize if we have overlooked or omitted some contributions due to space limitations. This work is partially supported by National Science Foundation DBI-0923827 and Plant Sciences Institute of Iowa State University.

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Authors and Affiliations

  1. Department of Agronomy, Iowa State University, G405 Agronomy Hall, Ames, IA, 50011-1010, USA

    Anjanasree K. Neelakandan & Kan Wang

  2. Center for Plant Transformation, Plant Sciences Institute, Iowa State University, G405 Agronomy Hall, Ames, IA, 50011-1010, USA

    Anjanasree K. Neelakandan & Kan Wang

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  1. Anjanasree K. Neelakandan
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  2. Kan Wang
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Correspondence to Kan Wang.

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Communicated by R. Reski.

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Neelakandan, A.K., Wang, K. Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31, 597–620 (2012). https://doi.org/10.1007/s00299-011-1202-z

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  • DOI: https://doi.org/10.1007/s00299-011-1202-z

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