New insights into plant somatic embryogenesis: an epigenetic view

Adu-Gyamfi R, Wetten A, Rodríguez L, Carlos M (2016) Effect of cryopreservation and post-cryopreservation somatic embryogenesis on the epigenetic fidelity of cocoa (Theobroma cacao L.). PLoS One 11:e0158857 Alvarez ME, Nota F, Cambiagno DA (2010) Epigenetic control of plant immunity. Mol Plant 11:563–576 Álvarez-Venegas R, De-la-Peña C (2016) Editorial: recent advances of epigenetics in crop biotechnology. Front Plant Sci 7:413 Angaji SA, Hedayati S, Poor RH, Madani S (2010) Application of RNA interference in plants. Plant Omics 3:77–84 Arnold SV, Sabala I, Bozhkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tissue Organ Cult 69:233–249 Arroyo-Herrera A, Gonzalez AK, Moo RC, Quiroz-Figueroa FR, Loyola-Vargas VM, Rodriguez-Zapata LC, Burgeff D’Hondt C, Suárez-Solís VM, Castaño E (2008) Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell Tissue Organ Cult 94:171–180 Avivi Y, Morad V, Ben-Meir H, Zhao J, Kashkush K, Tzfira T, Citovsky V, Grafi G (2004) Reorganization of specific chromosomal domains and activation of silent genes in plant cells acquiring pluripotentiality. Dev Dyn 230:12–22 Barraza A, Cabrera-Ponce JL, Gamboa-Becerra R, Luna-Martinez F, Winkler R, Álvarez-Venegas R (2015) The Phaseolus vulgaris PvTRX1h gene regulates plant hormone biosynthesis in embryogenic callus from common bean. Front Plant Sci 6:577 Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297 Bednarek P, Orlowska R, Koebner R, Zimny J (2007) Quantification of the tissue-culture induced variation in barley (Hordeum vulgare L.). BMC Plant Biol 7:10 Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A (2009) An operational definition of epigenetics. Genes Dev 23:781–783 Berr A, Ménard R, Heitz T, Shen WH (2012) Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack. Cell Microbiol 14:829–839 Bhalla PL, Singh MB (2006) Molecular control of stem cell maintenance in shoot apical meristem. Plant Cell Rep 25:249–256 Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AAM, Miki BLA, Custers JBM, Campagne MML (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749 Bouyer D, Roudier F, Heese M, Andersen E, 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:e1002243 Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619 Braybrook SA, Stone SL, Park S, Bui AQ, Le BH, Fischer RL, Goldberg RB, Harada JJ (2006) Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci USA 103:3468–3473 Brown PTH, Kyozuka J, Sukekiyo Y, Kimura Y, Shimamoto K, Lörz H (1990) Molecular changes in protoplast-derived rice plants. Mol Gen Genet 223:324–328 Butler PJ (1983) The folding of chromatin. CRC Crit Rev Biochem 15:57–91 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 Catoni M, Lucioli A, Doblas-Ibáñez P, Accotto GP, Vaira AM (2013) From immunity to susceptibility: virus resistance induced in tomato by a silenced transgene is lost as TGS overcomes PTGS. Plant J 75:941–953 Chakrabarty D, Yu KW, Paek KY (2003) Detection of DNA methylation changes during somatic embryogenesis of Siberian ginseng (Eleutherococcus senticosus). Plant Sci 165:61–68 Chávez-Hernández EC, Alejandri-Ramírez ND, Juárez-González VT, Dinkova TD (2015) Maize miRNA and target regulation in response to hormone depletion and light exposure during somatic embryogenesis. Front Plant Sci 6:555 Chen SK, Kurdyukov S, Kereszt A, Wang XD, Gressho PM, Rose RJ (2009) The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula. Planta 230:827–840 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 Chen CJ, Liu Q, Zhang YC, Qu LH, Chen YQ, Gautheret D (2011) Genome-wide discovery and analysis of microRNAs and other small RNAs from rice embryogenic callus. RNA Biol 8:538–547 Chugh A, Khurana P (2002) Gene expression during somatic embryogenesis—recent advances. Curr Sci 86:715–730 Corley RHV, Lee CH, Law LH, Wong CY (1986) Abnormal flower development in oil palm clones. Planter (Kuala Lumpur) 62:233–240 Cristofolini C, do Nascimento Vieira L, de Freitas Fraga H, da Costa I, Guerra M, Pescador R (2014) DNA methylation patterns and karyotype analysis of off-type and normal phenotype somatic embryos of feijoa. Theor Exp Plant Physiol 26:217–224 Curaba J, Moritz T, Blervaque R, Parcy F, Raz V, Herzog M, Vachon G (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDONS2 and FUS3 in Arabidopsis. Plant Physiol 136:3660–3669 Currais L, Loureiro J, Santos C, Canhoto JM (2013) Ploidy stability in embryogenic cultures and regenerated plantlets of tamarillo. Plant Cell Tissue Organ Cult 114:149–159 De-la-Peña C, Nic-Can GI, Galaz-Avalos RM, Avilez-Montalvo R, Loyola-Vargas VM (2015) The role of chromatin modifications in somatic embryogenesis in plants. Front Plant Sci 6:635 Diaz-Sala C, Rey M, Boronat A, Besford R, Rodriguez R (1995) Variations in the DNA methylation and polypeptide patterns of adult hazel (Corylus avellana L.) associated with sequential in vitro subcultures. Plant Cell Rep 15:218–221 Ding B, Wang GL (2015) Chromatin versus pathogens: the function of epigenetics in plant immunity. Front Plant Sci 6:675 Domon JM, Meyer Y, Faye L, David A, David H (1994) Extracellular (g1yco) proteins in embryogenic and non-embryogenic cell lines of Caribbean pine. Comparison between phenotypes of stage one somatic embryos. Plant Physiol Biochem 32:1–11 Duan CG, Wang CH, Guo HS (2012) Application of RNA silencing to plant disease resistance. Silence 3:5 Dunwell JM (1998) Cupins: a new superfamily of functionally diverse proteins that include germins and plant storage proteins. Biotechnol Genet Eng Rev 15:1–32 Dunwell J, Khuri S, Gane P (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin super-family. Microbiol Mol Biol Rev 64:153–179 Dunwell JM, Culham A, Carter CE, Sosa-Aguirre CR, Goodenough PW (2001) Evolution of functional diversity in the cupin superfamily. Trends Biochem Sci 26:740–746 El Ouakfaoui S, 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 Elhiti M, Stasolla C, Wang A (2013) Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev Biol Plant 49:631–642 Elmeer KES (2013) Factors regulating somatic embryogenesis in plants. In: Junaid A, Srivastava PS, Sharma MP (eds) Somatic embryogenesis and gene expression. Narosa Publishing House, New Delhi, pp 56–81 Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The shoot meristemless gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979 Exner V, Hennig L (2008) Chromatin rearrangements in development. Curr Opin Plant Biol 11:64–69 Fehér A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta 1849:385–402 Fehér A, Pasternak T, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228 Fiuk A, Bednarek PT, Rybczyński JJ (2010) Flow cytometry, HPLC-RP, and metAFLP analyses to assess genetic variability in somatic embryo-derived plantlets of Gentiana pannonica Scop. Plant Mol Biol Rep 28:413–420 Florez SL, Erwin RL, Maximova SN, Guiltinan MJ, Curtis WR (2015) Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol 15:121 Fraga HPF, Vieira LN, Caprestano CA, Steinmacher DA, Micke GA, Spudeit DA, Rosete Pescador R, Guerra MP (2012) 5-Azacytidine combined with 2,4-D improves somatic embryogenesis of Acca sellowiana (O. Berg) Burret by means of changes in global DNA methylation levels. Plant Cell Rep 31:2165–2176 Gaj MD, Zhang S, Harada JJ, Lemaux P (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988 Gallois JL, Nora FR, Mizukami Y, Sablowski R (2004) WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem. Genes Dev 18:375–380 Gao X, Yang D, Cao D, Ao M, Sui X, Wang Q, Kimatu J, Wang L (2010) In vitro micropropagation of Freesia hybrida and the assessment of genetic and epigenetic stability in regenerated plantlets. J Plant Growth Regul 29:257–267 Garg R, Chevala VVSN, Shankar R, Jain M (2015) Divergent DNA methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. Sci Rep 5:14922 Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7:373–385 Gillis K, Gielis J, Peeters H, Dhooghe E, Oprins J (2007) Somatic embryogenesis from mature Bambusa balcooa Roxburgh as basis for mass production of elite forestry bamboos. Plant Cell Tissue Organ Cult 91:115–123 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 Guan Y, Li SG, Fan XF, Su ZH (2016) Application of somatic embryogenesis in woody plants. Front Plant Sci 7:938 Haig D (2004) The (dual) origin of epigenetics. Cold Spring Harb Symp Quant Biol 69:67–70 Han SK, Wu MF, Cui S, Wagner D (2015) Roles and activities of chromatin remodeling ATPases in plants. Plant J 83:62–77 Hanani LR, Floh EIS, Fungaro MHP, Santa-Catarina C, Matias de Paula F, Viana AM, Vieira MLC (2010) Methylation patterns revealed by MSAP profiling in genetically stable somatic embryogenic cultures of Ocotea catharinensis (Lauraceae). In Vitro Cell Dev Biol Plant 46:368–377 Hao YJ, Wen XP, Deng XX (2004) Genetic and epigenetic evaluations of citrus calluses recovered from slow-growth culture. J Plant Physiol 161:479–484 Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J Plant Physiol 158:405–409 He X, Chen T, Zhu J (2011) Regulation and function of DNA methylation in plants and animals. Cell Res 21:442–465 Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, 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 Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing. Plant Cell 7:1271–1282 Heringer AS, Steinmacher DA, Fraga HP, Vieira LN, Ree JF, Guerra MP (2013) Global DNA methylation profiles of somatic embryos of peach palm (Bactris gasipaes Kunth) are influenced by cryoprotectants and droplet-vitrification cryopreservation. Plant Cell Tissue Organ Cult 114:365–372 Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158:35–43 Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cells and host defense response against fungal infection. Planta 222:107–117 Huang X, Lu XY, Zhao JT, Chen JK, Dai XM, Xiao W, Chen YP, Chen YF, Huang XL (2010) MaSERK1 gene expression associated with somatic embryogenic competence and disease resistance response in banana (Musa spp.). Plant Mol Biol Rep 28:309–316 Ikeuchi M, Iwase A, Rymen B, Harashima H, Shibata M, Ohnuma M, Breuer C, Morao AK, de Lucas M, de Veylder L, Goodrich J, Brady SM, Roudier F, Sugimoto K (2015) PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis. Nat Plants 1:15089 Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. Development 143:1442–1451 Jaligot E, Beulé T, Baurens FC, Billotte N, Rival A (2004) Search for methylation-sensitive amplification polymorphisms associated with the ‘mantled’ variant phenotype in oil palm (Elaeis guineensis Jacq.). Genome 47:224–228 Jarillo JA, Pineiro M, Cubas P, Martınez-Zapater JM (2009) Chromatin remodeling in plant development. Int J Dev Biol 53:1581–1596 Ji J, Strable J, Shimizu R, Koening D, Sinha N, Scanlon MJ (2010) WOX4 promotes procambial development. Plant Physiol 152:1346–1356 Jia X, Yan J, Tang G (2011) MicroRNA-mediated DNA methylation in plants. Front Biol 6:133–139 Jiménez VM (2005) Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis. Plant Growth Regul 47:91–110 Jiménez VM, Bangerth F (2001) Endogenous hormone concentrations and embryogenic callus development in wheat. Plant Cell Tissue Organ Cult 67:37–46 Jones-Rhoades WM, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53 Joshi R, Joshi PR, Aramod Kumar PK (2013) Regulation of somatic embryogenesis in crops: a review. Agric Rev 34:1–20 Junker A, Mönke G, Rutten T, Keilwagen J, Seifert M, Thi TMN, Renou JP, Balzergue S, Viehöver P, Hähnel U, Ludwig-Müller J, Altschmied L, Conrad U, Weisshaar B, Bäumlein H (2012) Elongation-related functions of LEAFY COTYLEDON1 during the development of Arabidopsis thaliana. Plant J 71:427–442 Kaeppler SM, Phillips RL (1993) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci USA 90:8773–8776 Klimaszewska K, Noceda C, Pelletier G, Label P, Rodriguez R, Lelu-Walter MA (2009) Biological characterization of young and aged embryogenic cultures of Pinus pinaster (Ait.). In Vitro Cell Dev Biol Plant 45:20–33 Kulinska-Lukaszek K, Tobojka M, Adamiok A, Kurczynska EU (2012) Expression of the BBM gene during somatic embryogenesis of Arabidopsis thaliana. Biol Plant 56:389–394 Kumar V, Moyo M, Van Staden J (2015a) Somatic embryogenesis of Pelargonium sidoides DC. Plant Cell Tissue Organ Cult 121:571–577 Kumar R, Anunanthini P, Sathishkumar R (2015b) Epigenetic silencing in transgenic plants. Front Plant Sci 6:693 Kumar V, Moyo M, Van Staden J (2016) Enhancing plant regeneration of Lachenalia viridiflora, a critically endangered ornamental geophyte with high floricultural potential. Sci Hortic 211:263–268 Kumar V, Moyo M, Van Staden J (2017) Somatic embryogenesis in Hypoxis hemerocallidea: an important African medicinal plant. South Afr J Bot 108:331–336 Kwong RM, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18 Lafos M, Kroll P, Hohenstatt ML, Thorpe FL, Clarenz O, Schubert D (2011) Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet 7:e1002040 Landey RB, Cenci A, Guyot R, Bertrand B, Georget F, Dechamp E, Herrera JC, Aribi J, Lashermes P, Etienne H (2015) Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica. Plant Cell Tissue Organ Cult 122:517–531 Laux T, Mayer KFX, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96 Lee Y, Jeon K, Lee JT, Kim S, Kim VN (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670 Leljak-Levanic D, Bauer N, Mihaljevic S, Jelaska S (2004) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23:120–127 Leva AR, Petruccelli R, Rinaldi LMR (2012) Somaclonal variation in tissue culture: a case study with olive. In: Leva AR, Rinaldi LMR (eds) Recent advances in plant in vitro culture. INTECH Open Access Publisher, Croatia, pp 123–150 Levanic DL, Mihaljevic S, Jelaska S (2009) Variations in DNA methylation in Picea omorika (Panc) Purk. embryogenic tissue and the ability for embryo maturation. Prop Orn Plants 9:3–9 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 Tissue Organ Cult 90:153–168 Li H, Zhao X, Dai H, Wu W, Mao W, Zhang Z (2012a) Tissue culture responsive microRNAs in strawberry. Plant Mol Biol Rep 30:1047–1054 Li T, Chen J, Qiu S, Zhang Y, Wang P, Yang L, Lu Y, Shi J (2012b) Deep sequencing and microarray hybridization identify conserved and species-specific microRNAs during somatic embryogenesis in hybrid yellow poplar. PLoS One 7:e43451 Lin Y, Lai Z (2013) Comparative analysis reveals dynamic changes in miRNAs and their targets and expression during somatic embryogenesis in longan (Dimocarpus longan Lour.). PLoS One 8:e60337 Lin Y, Lai Z, Tian Q, Lin L, Lai R, Yang M, Zhang D, Chen Y, Zhang Z (2015) Endogenous target mimics down-regulate miR160 mediation of ARF10, -16 and -17 cleavage during somatic embryogenesis in Dimocarpus longan Lour. Front Plant Sci 6:956 Lippert D, Zhuang J, Ralph S, Ellis DE, Gilbert M, Olafson R, Ritland K, Ellis B, Douglas CJ, Bohlmann J (2005) Proteome analysis of early somatic embryogenesis in Picea glauca. Proteomics 5:461–473 Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305 Liu J, Feng L, Li J, He Z (2015) Genetic and epigenetic control of plant heat responses. Front Plant Sci 6:267 Lo Schiavo F, Pitto L, Giuliano G, Torti G, Nuti Ronchi V, Marazzati D, Vergara R, Orselli S, Terzi M (1989) DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiations, hormones and hypomethylating drugs. Theor Appl Genet 77:325–331 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 Lotan T, Ohto M, Matsudaira YK, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205 Loyola-Vargas VM, De-la-Peña C, Galaz-Avalos RM, Quiroz-Figueroa FR (2008) Plant tissue culture. An intemporal set of tools. In: Walker JM, Rapley R (eds) Protein and cell biomethods handbook. Humana Press, Totowa, pp 875–904 Luerssen H, Kirik V, Herrman P, Misera S (1998) FUSCA3encodesa protein with a conserved Vp1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764 Luo YC, Zhou H, Li Y, Chen JY, Yang JH, Chen YQ, Qu LH (2006) Rice embryogenic calli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant postembryogenic development. FEBS Lett 580:5111–5116 Machczyńska J, Zimny J, Bednarek PT (2015) Tissue culture-induced genetic and epigenetic variation in triticale (×Triticosecale spp. Wittmack ex A. Camus 1927) regenerants. Plant Mol Biol 89:279–292 Mahdavi-Darvari F, Noor NM, Ismanizan I (2015) Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tissue Organ Cult 120:407–422 Manavalan LP, Chen X, Clarke J, Salmeron J, Nguyen HT (2012) RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J Exp Bot 63:163–175 Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang XD, 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 Marum L (2009) Genetic and epigenetic approaches to evaluate stability during in vitro propagation of Pinus pinaster Ait. PhD Thesis. Instituto de Tecnologia Química e Biológica Universidade Nova de Lisboa 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 Matzke MA, Primig M, Trnovsky J, Matzke AJM (1989) Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J 8:643–649 Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815 Meinke DW, Franzmann LH, Nickle TC, Yeung EC (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064 Menéndez-Yuffá A, Barry-Etienne D, Bertrand B, Georget F, Etienne H (2010) A comparative analysis of the development and quality of nursery plants derived from somatic embryogenesis and from seedlings for large-scale propagation of coffee (Coffea arabica L.). Plant Cell Tissue Organ Cult 102:297–307 Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62:3713–3725 Milutinovic S, Zhuang Q, Niveleau A, Szyf M (2003) Epigenomic stress response Knockdown of DNA methyltransferase 1 triggers an intra-S-phase arrest of DNA replication and induction of stress response genes. J Biol Chem 278:14985–14995 Mordhorst AP, Toonen MA, de Vries SC, Meinke D (1997) Plant embryogenesis. Crit Rev Plant Sci 16:535–576 Munksgaard D, Mattsson O, Okkles FT (1995) Somatic embryo development in carrot is associated with an increase in levels of S-adenosylmethionine, S-adenosylhomocysteine and DNA methylation. Physiol Plant 93:5–10 Naseer S, Mahmood T (2014) Tissue culture and genetic analysis of somaclonal variations of Solanum melongena L. cv. Nirrala. Cent Eur J Biol 9:1182–1195 Neelakandan AK, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620 Neutelings G, Domon JM, Membre N, Bernier F, Meyer Y, David A, David H (1998) Characterization of a germin-like protein gene expressed in somatic and zygotic embryos of pine (Pinus caribaea Morelet). Plant Mol Biol 38:1179–1190 Nic-Can GI, De-la-Peña C (2014) Epigenetic advances on somatic embryogenesis of agronomical and important crops. Epigenetics in plants of agronomic importance: fundamentals and applications. Springer, New York, pp 91–109 Nic-Can GI, López-Torres A, Barredo-Pool FA, Wrobel K, Loyola-Vargas VM, Rojas-Herrera R, De-la-Peña C (2013) New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS One 8:e72160 Noceda C, Salaj T, Pérez M, Viejo M, Cañal J, Salaj J, Rodriguez R (2009) DNA methylation and decrease on free polyamines is associated with the embryogenic capacity of Pinus nigra Arn. Cell Cult Trees 23:1285–1293 Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24:2678–2692 Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230 Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–94 Palmgren G, Mattsson O, Okkels FT (1991) Specific levels of DNA methylation in various tissues, cell lines, and cell types of Daucus carota. Plant Physiol 95:174–178 Parcy F, Valon C, Kohara A, Miśera S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277 Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495 Paul S, Datta SK, Datta K (2015) miRNA regulation of nutrient homeostasis in plants. Front Plant Sci 6:232 Pérez M, Cañal MJ, Toorop PE (2015a) Expression analysis of epigenetic and abscisic acid-related genes during maturation of Quercus suber somatic embryos. Plant Cell Tissue Organ Cult 121:353–366 Pérez M, Viejo M, LaCuesta M, Toorop P, Cañal MJ (2015b) Epigenetic and hormonal profile during maturation of Quercus suber L. somatic embryos. J Plant Physiol 173:51–61 Pilarska M, Malec P, Salaj J, Bartnicki F, Konieczny R (2016) High expression of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE coincides with initiation of various developmental pathways in in vitro culture of Trifolium nigrescens. Protoplasma 253:345–355 Pogson BJ, Davies C (1995) Characterization of a cDNA encoding the protein moiety of a putative arabinogalactan protein from Lycopersicon esculentum. Plant Mol Biol 28:347–352 Poon S, Heath RL, Clarke AE (2012) A chimeric arabinogalactan protein promotes somatic embryogenesis in cotton cell culture1,[W][OA]. Plant Physiol 160:684–695 Qiao M, Xiang F (2013) A set of Arabidopsis thaliana miRNAs involve shoot regeneration in vitro. Plant Signal Behav 8:e23479 Quiroz-Figueroa FR, Rojas-Herrera R, Galaz-Avalos RM, Loyola Vargas VM (2006) Embryo production through somatic embryogenesis ca be used to study cell differentiation in plants. Plant Cell Tissue Organ Cult 86:285–301 Reinert J (1959) Über die Kontrolle der Morphogenese und die Induktion von Adventivembryonen an Gewebekulturen aus Karotten. Planta 53:318–333 Reyes JC (2006) Chromatin modifiers that control plant development. Curr Opin Plant Biol 9:21–27 Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520 Rojas-Herrera R, Quiroz-Figueroa FR, Monforte-González M, Sánchez-Teyer F, Loyola-Vargas VM (2002) Differential gene expression during somatic embryogenesis in Coffea arabica L., revealed by RT-PCR differential display. Mol Biotechnol 21:43–50 Rupps A, Raschke J, Rümmler M, Linke B, Zoglauer K (2016) Identification of putative homologs of Larix decidua to BABYBOOM (BBM), LEAFY COTYLEDON1 (LEC1), WUSCHEL-related HOMEOBOX2 (WOX2) and SOMATIC EMBRYOGENESIS RECEPTOR-like KINASE (SERK) during somatic embryogenesis. Planta 243:473–488 Salaj J, Recklinghausen IR, Hecht V, de Vries SC, Schel JHN, van Lammeren AAM (2008) AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiol Biol 46:709–714 Santa-Catarina C, Hanai LR, Dornelas MC, Viana AM, Floh EIS (2004) SERK gene homolog expression, polyamines and amino acids associated with somatic embryogenic competence of Ocotea catharinensis Mez. (Lauraceae). Plant Cell Tissue Organ Cult 79:53–61 Santos D, Fevereiro P (2002) Loss of DNA methylation affects somatic embryogenesis in Medicago truncatula. Plant Cell Tissue Organ Cult 70:155–161 Santos MO, Romanoa E, Yotoko KSC, Tinoco MLP, Dias BBA, Aragao FJL (2005) Characterization of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Sci 168:723–729 Savona M, Mattioli R, Nigro S, Falasca G, Della Rovere F, Costantino P, De Vries S, Ruffoni B, Trovato M, Altamura MM (2012) Two SERK genes are markers of pluripotency in Cyclamen persicum Mill. J Exp Bot 63:471–488 Schellenbaum P, Mohler V, Wenzel G, Walter B (2008) Variation in DNA methylation patterns of grapevine somaclones (Vitis vinifera L.). BMC Plant Biol 8:78 Schlögl PS, Wendt dos Santos AL, Vieira LN, Floh EIS, Guerra MP (2012a) Gene expression during early somatic embryogenesis in Brazilian pine (Araucaria angustifolia (Bert) O. Ktze). Plant Cell Tissue Organ Cult 108:173–180 Schlögl PS, Wendt dos Santos AL, Vieira LN, Floh EIS, Guerra MP (2012b) Cloning and expression of embryogenesis-regulating genes in Araucaria angustifolia (Bert.) O. Kuntze (Brazilian Pine). Genet Mol Biol 35:172–181 Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062 Schmitt F, Oakeley EJ, Jost JP (1997) Antibiotics induce genome-wide hypermethylation in cultured Nicotiana tabacum plants. J Biol Chem 272:1534–1540 Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644 Schrader S, Kaldenhoff R, Richter G (1997) Expression of novel genes during somatic embryogenesis of suspension-cultured carrot cells (Daucus carota). J Plant Physiol 50:63–68 Seefried WF, Willmann MRR, Clausen RL, Jenik PD (2014) Global regulation of embryonic patterning in Arabidopsis by micro-RNAs. Plant Physiol 165:670–687 Sharma S, Bryan G, Winfield M, Millam S (2007) Stability of potato (Solanum tuberosum L.) plants regenerated via somatic embryos axillary bud proliferated shoots, microtubers and true potato seeds: a comparative phenotypic, cytogenetic and molecular assessment. Planta 226:1449–1458 Sharma SK, Millam S, Hein I, Bryan GJ (2008) Cloning and molecular characterization of a potato SERK gene transcriptionally induced during initiation of somatic embryogenesis. Planta 228:319–330 Shen Y, Jiang Z, Yao X, Zhang Z, Lin H, Zhao M, Liu H, Peng H, Li S, Pan G (2012) Genome expression profile analysis of the immature maize embryo during dedifferentiation. PLoS One 7:e32237 Shen Y, Jiang Z, Lu S, Lin H, Gao S, Peng H, Yuan G, Liu L, Zhang Z, Zhao M, Rong T, Pan G (2013) Combined small RNA and degradome sequencing reveals microRNA regulation during immature maize embryo dedifferentiation. Biochem Biophys Res Commun 441:425–430 Shimada T, Hirabayashi T, Endo T, Fujii H, Kita M, Omura M (2005) Isolation and characterization of the somatic embryogenesis receptor-like kinase gene homologue (CitSERK1) from Citrus unshiu Marc. Sci Hortic 103:233–238 Silva AT, Barduche D, Gabriella do Livramento K, Paiva LV (2015) A putative BABY BOOM-like gene (CaBBM) is expressed in embryogenic calli and embryogenic cell suspension culture of Coffea arabica L. In Vitro Cell Dev Biol Plant 51:93–101 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 Sirohi G, Pandey BK, Deveshwar P, Giri J (2016) Emerging trends in epigenetic regulation of nutrient deficiency response in plants. Mol Biotechnol 58:159–171 Somleva MN, Schmidt EDL, de Vries SC (2000) Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression. Plant Cell Rep 19:718–726 Stasolla C, Bozhkov PV, Chu TM, Van Zyl L, Egertsdotter U, Suarez MF, Craig D, Wolfinger RD, Von Arnold S, Sederoff RR (2004) Variation in transcript abundance during somatic embryogenesis in gymnosperms. Tree Physiol 24:1073–1085 Stewards FC, Mapbs MO, Mears K (1958) Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cells. Am J Bot 45:705–708 Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh TF, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci USA 105:3151–3156 Su YH, Liu YB, Zhou C, Li XM, Zhang XS (2015) The microRNA167 controls somatic embryogenesis in Arabidopsis through regulating its target genes ARF6 and ARF8. Plant Cell Tissue Organ Cult 124:405–417 Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23:3247–3259 Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411 Thompson EW, Lane BG (1980) Relation of protein synthesis in imbibing wheat embryos to the cell-free translational capacities of bulk mRNA from dry and imbibing embryos. J Biol Chem 255:5965–5970 Tsuwamoto R, Yokoi S, Takahata Y (2010) Arabidopsis EMBRYOMAKER encoding an AP2domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 73:481–492 Uddin MR (1993) Somatic embryogenesis in gymnosperms. US 5187092 A Vashisht D, Nodine MD (2014) MicroRNA functions in plant embryos. Biochem Soc Trans 42:352–357 Verbsky ML, Richards EJ (2001) Chromatin remodeling in Plants. Curr Opin Plant Biol 4:494–500 Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:243–252 Viejo M, Rodríguez R, Valledor L, Pérez M, Cañal MJ, Hasbún R (2010) DNA methylation during sexual embryogenesis and implications on the induction of somatic embryogenesis in Castanea sativa Miller. Sex Plant Rep 23:315–323 Waites R, Simon R (2000) Signaling cell fate in plant meristems: three clubs on one tousle. Cell 103:835–838 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 Wang X, Niu QW, Teng C, Li C, Mu J, Chua NH, Zuo J (2009) Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res 19:224–235 Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614 Williams EG, Maheswaran G (1986) Somatic embryogenesis: factors influencing coordinated behaviour of cells as an embryogenic group. Ann Bot 57:443–462 Williams L, Zhao J, Morozova N, Li Y, Avivi Y, Grafi G (2003) Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev Dyn 128:113–120 Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155:1871–1884 Wójcik AM, Gaj MD (2016) miR393 contributes to the embryogenic transition induced in vitro in Arabidopsis via the modification of the tissue sensitivity to auxin treatment. Planta 244:231–243 Wu XM, Liu MY, Ge XX, Xu Q, Guo WW (2011) Stage and tissue specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 233:495–505 Wurtele S, Wang H, Durgerian S, Nikolau BJ, Ulrich TH (1993) Characterization of a gene that is expressed early in somatic embryogenesis of Daucus carota. Plant Physiol 102:303–312 Xu M, Li X, Korban S (2004) DNA-methylation alterations and exchanges during in vitro cellular differentiation in rose (Rosa hybrida L.). Theor Appl Genet 109:899–910 Yang X, Zhang X (2010) Regulation of somatic embryogenesis in higher plants. Crit Rev Plant Sci 29:36–57 Yang X, Wang L, Yuan D, Lindsey K, Zhang X (2013) Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. J Exp Bot 64:1521–1536 Yeung EC (1995) Structural and development patterns in somatic embryogenesis. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer, Netherlands, pp 205–247 Zhai L, Xu L, Wang Y, Zhu X, Feng H, Li C, Luo X, Everlyne MM, Liu L (2016) Transcriptional identification and characterization of differentially expressed genes associated with embryogenesis in radish (Raphanus sativus L). Sci Rep 6:21652 Zhang C, Hsieh TF (2013) Heritable epigenetic variation and its potential applications for crop improvement. Plant Breed Biotechnol 1:307–319 Zhang S, Liu X, Lin Y, Xie G, Fu F, Liu H, Wang J, Gao S, Lan H, Rong T (2011) Characterization of a ZmSERK gene and its relationship to somatic embryogenesis in a maize culture. Plant Cell Tissue Organ Cult 105:29–37 Zhang C, Cao L, Rong L, An Z, Zhou W, Ma J, Shen WH, Zhu Y, Dong A (2015a) The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development. Plant J 82:655–668 Zhang F, Dong W, Huang L, Song A, Wang H, Fang W, Chen F, Teng N (2015b) Identification of microRNAs and their targets associated with embryo abortion during Chrysanthemum cross breeding via high-throughput sequencing. PLoS One 10:e0124371 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 Zheng Q, Zheng Y, Perry SE (2013) AGAMOUS-Like15 promotes somatic embryogenesis in Arabidopsis and Soybean in part by the control of ethylene biosynthesis and response. Plant Physiol 161:2113–2127 Zheng W, Zhang X, Yang Z, Wu J, Li F, Duan L, Liu C, Lu L, Zhang C, Li F (2014) AtWuschel promotes formation of the embryogenic callus in Gossypium hirsutum. PLoS One 9:e87502 Zhu QH, Shan WX, Ayliffe MA, Wang MB (2016) Epigenetic mechanisms: an emerging player in plant-microbe interactions. Mol Plant Microbe Interact 29:187–196 Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359