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Molecular regulation of plant somatic embryogenesis

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Abstract

In vitro embryogenesis is an asexual reproduction process by which embryos are produced from either gametophytic (androecium/gynoecium) or sporophytic (somatic) tissues. Regardless of the type of explant used, the hallmark of this process is that the explant cells undergo dedifferentiation and acquire meristematic identity. The developmental program of such meristematic cells can then be redirected to form somatic embryos, depending on the imposed culture environment. Analysis of proteomes and transcriptomes has led to the molecular identification and functional characterization of many genes involved in the initiation and development of somatic embryos. These genes can be classified into three categories: embryonic induction, embryonic, and maturation. So far, few genes involved in early somatic embryogenesis have been characterized because isolation of early pure embryonic tissue is very difficult. This review focuses on genes regulating the induction process. Furthermore, we employed bioinformatic tools and pathway databases to identify genes that may play roles in regulating early somatic embryogenesis. A total of 51 proteins were identified that may function in early somatic embryogenesis. These proteins are predicted to be involved in hormone signal transduction, chromatin remodeling, cell cycle regulation, cellulose biosynthetic and metabolic activity, GTPase signal transduction, transcription regulation, meristem formation and maintenance, and/or apoptosis and microtubule organization. This review will help advance knowledge and promote research on molecular regulation of early somatic embryogenesis.

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References

  • Abid G, Jacquemin JM, Sassi K, Muhovski Y, Toussaint A, Baudoin JP (2010) Gene expression and genetic analysis during higher plants embryogenesis. Biotechnol Agron Soc Environ 14:667–680

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Almeida AM, Parreira JR, Santos R, Duque AS, Francisco R, Tome DFA, Ricardo CP, Coelho AV, Fevereiro P (2012) A proteomics study of the induction of somatic embryogenesis in Medicago truncatula using 2DE and MALDI-TOF/TOF. Physiol Plant 146:236–249

    Article  PubMed  CAS  Google Scholar 

  • Azpetia A, Chan JL, Saenz L, Oropeza C (2003) Effect of 22(S), 23(S)-homobrassinolide on somatic embryogenesis in plumule explants of Cocos nucifera L. cultured in vitro. J Hort Sci Biotechnol 78:591–596

    Google Scholar 

  • Belmonte M, Elhiti M, Waldner B, Stasolla C (2010) Depletion of cellular brassinolide decreases embryo production and disrupts the architecture of the apical meristems in Brassica napus microspore-derived embryos. J Exp Bot 61:2779–2794

    Article  PubMed  CAS  Google Scholar 

  • Benson EE (2000) Do free radicals have a role in plant tissue culture recalcitrance? In Vitro Cell Dev Biol Plant 36:163–170

    Article  CAS  Google Scholar 

  • Bhojwani S, Razdan M (1996) Plant tissue culture: theory and practice. Elsevier, Amsterdam, pp 125–166

    Google Scholar 

  • Birnbaum KD, Alvarado AS (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710

    Article  PubMed  CAS  Google Scholar 

  • Bozhkov PV, Filonova LH, Suarez MF (2005) Programmed cell death in plant embryogenesis. Curr Top Dev Biol 67:135–179

    PubMed  CAS  Google Scholar 

  • Bratzel F, Lopez-Torrejon G, Koch M, Del Pozo JC, Calonje M (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20:1853–1859

    Article  PubMed  CAS  Google Scholar 

  • Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8:394–401

    Article  PubMed  CAS  Google Scholar 

  • Cerdido A, Medina FJ (1995) Subnucleolar location of fibrillarin and variation in its levels during the cell cycle and during differentiation of plant cells. Chromosoma 103:625–634

    Article  PubMed  CAS  Google Scholar 

  • Chanvivattana Y, Bishopp A, Schubert A, 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 

  • Chen SK, Kurdyukov S, Kereszt A, Wang XD, Gresshoff PM, Rose RJ (2009) 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 

  • Clark S, Williams R, Meyerowitz E (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    Article  PubMed  CAS  Google Scholar 

  • Clouse S (2002) Brassinosteroids. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, pp 1–23

    Google Scholar 

  • Cortes MM, Paredes FR, Burgeff C, Nunez TP, Cordova I, Oropeza C, Verdeil JL, Saenz L (2010) Characterisation of a cyclin-dependent kinase (CDKA) gene expressed during somatic embryogenesis of coconut palm. Plant Cell Tissue Organ Cult 102:251–258

    Article  Google Scholar 

  • Costa S, Shaw P (2007) ‘Open minded’ cells: how cells can change fate. Trends Cell Biol 17:101–106

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Lau S, Mayer U, Jürgens G (2010) Embryogenesis—the humble beginnings of plant life. Plant J 61:959–970

    Article  PubMed  Google Scholar 

  • Del Pozo JC, Lopez-Matas MA, Ramirez-Parra E, Gutierrez C (2005) Hormonal control of the plant cell cycle. Physiol Plant 123:173–183

    Article  Google Scholar 

  • Dharmasiri N, Estelle M (2002) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    Article  Google Scholar 

  • Dodsworth (2009) A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol 336:1–9

    Article  PubMed  CAS  Google Scholar 

  • Dovzhenko A, Dal Bosco C, Meurer J, Koop HU (2003) Efficient regeneration from cotyledon protoplasts in Arabidopsis thaliana. Protoplasma 222:107–111

    Article  PubMed  CAS  Google Scholar 

  • Elhiti M, Stasolla C (2011) Ectopic expression of the Brassica SHOOTMERISTEMLESS attenuates the deleterious effects of the auxin transport inhibitor TIBA on somatic embryo number and morphology. Plant Sci 180:383–390

    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, Yang C, Chan A, Durnin DC, Belmonte MF, Ayele BT, Tahir M, Stasolla C (2012) Altered seed oil and glucosinolate levels in transgenic plants overexpressing the Brassica napus SHOOTMERISTEMLESS gene. J Exp Bot 63:4447–4461

    Article  PubMed  CAS  Google Scholar 

  • Elhiti M, Hebelstrup KH, Wang A, Li C, Cui Y, Hill RD, Stasolla C (2013) Function of the type-2 Arabidopsis hemoglobin in the auxin-mediated formation of embryogenic cells during morphogenesis. Plant J 74:946–958

    Article  PubMed  CAS  Google Scholar 

  • Elhiti MA (2010) Molecular characterization of several brassica shoot apical meristem genes and the effect of their altered expression during in vitro morphogenesis. Ph.D. thesis, Faculty of Graduate Studies, University of Manitoba

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

    Article  CAS  Google Scholar 

  • Feng Z, Sun X, Wang G, Liu H, Zhu J (2012) LBD29 regulates the cell cycle progression in response to auxin during lateral root formation in Arabidopsis thaliana. Ann Bot 160:2–10

    Google Scholar 

  • Filonova LH, Bozhkov PV, Brukhin VB, Daniel G, Zhivotovsky B, von Arnold S (2000a) Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. J Cell Sci 113:4399–4411

    PubMed  CAS  Google Scholar 

  • Filonova LH, Bozhkov PV, von Arnold S (2000b) Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking. J Exp Bot 51:249–264

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  PubMed  CAS  Google Scholar 

  • Gaudino RJ, Pikaard CS (1997) Cytokinin induction of RNA polymerase I transcription in Arabidopsis thaliana. J Biol Chem 272:6799–6804

    Article  PubMed  CAS  Google Scholar 

  • Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16534

    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 

  • Grafi G, Chalifa-Caspi V, Nagar T, Plaschkes I, Barak S, Ransbotyn V (2011) Plant response to stress meets dedifferentiation. Planta 233:433–438

    Article  PubMed  CAS  Google Scholar 

  • Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J Plant Physiol 158:405–409

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 8:1271–1282

    Google Scholar 

  • Hemerly AS, Ferreira PC, Van Montagu M, Engler G, Inze D (2000) Cell division events are essential for embryo patterning and morphogenesis: studies on dominant negative cdc2aAt mutants of Arabidopsis. Plant J 23:123–130

    Article  PubMed  CAS  Google Scholar 

  • Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson MJ, Saxena PK (1996) Acetylsalicylic acid enhances and synchronizes thidiazuron-induced somatic embryogenesis in geranium (Pelargonium x hortorum Bailey) tissue cultures. Plant Cell Rep 15:512–515

    Article  PubMed  CAS  Google Scholar 

  • Ishiguro S, Watanabe Y, Ito N, Nonaka H, Takeda N, Sakai T, Kanaya H, Okada K (2002) SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J 21:898–908

    Article  PubMed  CAS  Google Scholar 

  • Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45:819–831

    Article  PubMed  CAS  Google Scholar 

  • Janosevic D, Budimir S (2006) Shoot apical meristem structure and STM expression in has mutant of Arabidopsis thaliana. Biol Plant 50:193–197

    Article  CAS  Google Scholar 

  • Kapros T, Bogre L, Nemeth K, Lasz Bako L, Gyorgyey J, Wu SC, Dudits D (1992) Differential expression of histone H3 gene variants during cell cycle and somatic embryogenesis in alfalfa. Plant Physiol 98:621–625

    Article  PubMed  CAS  Google Scholar 

  • Karami O, Aghavaisi B, Pour AM (2009) Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol 2:177–190

    Article  PubMed  Google Scholar 

  • Koltunow AM (1993) Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5:1425–1437

    PubMed  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 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Liu HI, Wang GC, Feng Z, Zhu J (2010) Screening of genes associated with dedifferentiation and effect of LBD29 on pericycle cells in Arabidopsis thaliana. Plant Growth Regul 62:127–136

    Article  CAS  Google Scholar 

  • Long J, Moan E, Medford J, Barton M (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69

    Article  PubMed  CAS  Google Scholar 

  • Luo JP, Jiang ST, Pan LJ (2001) Enhanced somatic embryogenesis by salicylic acid of Astragalus adsurgens Pall.: relationship with H2O2 production and H2O2-metabolizing enzyme activities. Plant Sci 161:125–132

    Article  CAS  Google Scholar 

  • Malik M, Wang F, Dirpaul J, Zhou N, Polowick P, Ferrie A, Krochko J (2007) Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiol 144:134–154

    Article  PubMed  CAS  Google Scholar 

  • Mayer K, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    Article  PubMed  CAS  Google Scholar 

  • Mitsuhashi W, Toyomasu T, Masui H, Katho T, Nakaminami K, Kashiwagi Y, Akutsu M, Kenmoku H, Sassa T, Yamaguchi S, Kamiya Y, Kamada H (2003) Gibberellin is essentially required for carrot (Daucus carota L.) somatic embryogenesis: dynamic regulation of gibberellin 3-oxidase gene expressions. Biosci Biotechnol Biochem 76:2438–2447

    Article  Google Scholar 

  • Mordhorst AP, Voerman KJ, Hartog MV, Meijer EA, van Went J, Koornneef M, de Vries SC (1998) Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. Genetics 149:549–563

    PubMed  CAS  Google Scholar 

  • Mussig C (2005) Brassinosteroid-promoted growth. Plant Biol 7:110–117

    Article  PubMed  CAS  Google Scholar 

  • Nogler G (1984) Gametophytic apomixis. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 475–518

    Chapter  Google Scholar 

  • Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67

    Article  PubMed  CAS  Google Scholar 

  • Passardi F, Theiler G, Zamocky M, Cosio C, Rouhier N, Teixera F, Margis-Pinheiro M, Ioannidis V, Penel C, Falquet L, Dunand C (2007) PeroxiBase: the peroxidase database. Phytochemistry 68:1605–1611

    Article  PubMed  CAS  Google Scholar 

  • Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, Dudits D, Feher A (2002) The role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129:1807–1819

    Article  PubMed  CAS  Google Scholar 

  • Patnaik D, Khurana P (2005) Identification of a phosphoprotein expressed during somatic embryogenesis in wheat leaf base cultures. J Plant Biochem Biotechnol 14:149–154

    Article  CAS  Google Scholar 

  • Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168

    Article  PubMed  CAS  Google Scholar 

  • Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M (2004) Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16:2785–2794

    Article  PubMed  CAS  Google Scholar 

  • Piyatrakul P, Putranto RA, Martin F, Rio M, Dessailly F, Leclercq J, Dufayard JF, Lardet L, Montoro P (2012) Some ethylene biosynthesis and AP2/ERF genes reveal a specific pattern of expression during somatic embryogenesis in Hevea brasiliensis. BMC Plant Biol 12:244

    Article  PubMed  CAS  Google Scholar 

  • Puigderrajols P, Jofre A, Mir G, Pla M, Verdaguer D, Huguet G, Molinas M (2002) Developmentally and stress-induced small heat shock proteins in cork oak somatic embryogenesis. J Exp Bot 3:1445–1452

    Article  Google Scholar 

  • Raghavan V (2000) Developmental biology of flowering plants. Springer, New York

    Book  Google Scholar 

  • Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol 43:439–463

    Article  CAS  Google Scholar 

  • Rudus I, Weiler EW, Kepczynska E (2009) Do stress-related phytohormones, abscisic acid and jasmonic acid play a role in the regulation of Medicago sativa L. somatic embryogenesis? Plant Growth Regul 59:159–169

    Article  CAS  Google Scholar 

  • Santos MO, Aragao FJL (2009) Role of SERK genes in plant environmental response. Plant Signal Behav 4:1111–1113

    Article  PubMed  CAS  Google Scholar 

  • Sentoku N, Sato Y, Kurata N, Ito Y, Kitano H, Matsuoka M (1999) Regional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development. Plant Cell 11:1651–1663

    PubMed  CAS  Google Scholar 

  • Sieberer T, Hauser MT, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842

    Article  PubMed  CAS  Google Scholar 

  • Song S, Lee M, Clark S (2006) POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells. Development 133:4691–4698

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Su YH, Zhang XS (2009) Auxin gradients trigger de novo formation of stem cells during somatic embryogenesis. Plant Signal Behavior 4:574–576

    Article  CAS  Google Scholar 

  • Sugiyama M (1999) Organogenesis in vitro. Curr Opin Plant Biol 2:61–64

    Article  PubMed  CAS  Google Scholar 

  • Verdeil JL, 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 

  • Wang H, Li J, Bostock RM, Gilchrist DG (1996) Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8:375–391

    PubMed  CAS  Google Scholar 

  • Wasternack C, Hause B (2002) Jasmonates and octadecanoids: signals in plant stress responses and development. Prog Nucleic Acid Res Mol Biol 72:165–221

    PubMed  CAS  Google Scholar 

  • Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614

    Article  PubMed  CAS  Google Scholar 

  • Yeung E (2002) The canola microspore-derived embryo as a model system to study developmental processes in plants. J Plant Biol 45:119–133

    Article  Google Scholar 

  • Yeung EC, Meinke DW (1993) Embryogenesis in angiosperms: development of the suspensor. Plant Cell 5:1371–1381

    PubMed  Google Scholar 

  • Zeng F, Zhang X, Jin S, Cheng L, Liang S, Hu L, Guo X, Nie Y, Cao J (2007) Chromatin reorganization and endogenous auxin/cytokinin dynamic activity during somatic embryogenesis of cultured cotton cell. Plant Cell Tissue Organ Cult 90:63–70

    Article  CAS  Google Scholar 

  • Zhang CX, Li Q, Kong L (2007) Induction, development and maturation of somatic embryos in Bunge’s pine (Pinus bungeana Zucc. ex Endl.). Plant Cell Tissue Organ Cult 91:273–280

    Article  Google Scholar 

  • Zhang G, Song C, Zhao MM, Li B, Guo SX (2012) Characterization of an A-type cyclin-dependent kinase gene from Dendrobium candidum. Biologia 67:360–368

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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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Acknowledgements

This research was supported in part by grants from Agriculture and Agri-Food Canada (AAFC) and the Natural Sciences and Engineering Research Council of Canada (NSERC) to AW and by an NSERC grant to CS.

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Correspondence to Aiming Wang.

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Editor: Prakash Lakshmanan

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Elhiti, M., Stasolla, C. & Wang, A. Molecular regulation of plant somatic embryogenesis. In Vitro Cell.Dev.Biol.-Plant 49, 631–642 (2013). https://doi.org/10.1007/s11627-013-9547-3

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