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The Life and Death Signalling Underlying Cell Fate Determination During Somatic Embryogenesis

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Applied Plant Cell Biology

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 22))

Abstract

Somatic embryogenesis (SE) is a sequence of stereotypical morphological transformations, which results in differentiation of cells into a plant body bypassing the fusion of gametes. As such, it represents a very powerful tool in biotechnology to propagate species with long reproductive cycles or low seed set and the production of genetically modified plants with improved traits. The initiation of SE can be divided into five major stages: (i) perception of extracellular signals or stress stimuli, (ii) transduction of the extracellular signal through the cytoplasm into the nucleus, (iii) induction of gene transcription required for embryogenesis, (iv) reorganisation of cytoplasm and (v) onset of embryonic development. The further embryonic development during SE resembles its zygotic counterpart and begins with the establishment of apical-basal asymmetry. The apical domain, the embryo proper, proliferates and eventually gives rise to the plantlet, while the basal part, the embryo suspensor, becomes a subject of terminal differentiation and gradually degrades via vacuolar programmed cell death (PCD). This PCD is essential for normal development of the apical domain. Some signalling events in the apical and basal domains share homologous components. Here, we describe our current knowledge on the control of life and death processes during SE.

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References

  • Ameisen JC (2002) On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 9:367–393

    CAS  PubMed  Google Scholar 

  • Anil VS, Rao KS (2000) Calcium mediated signalling during sandalwood somatic embryogenesis. Role for exogenous calcium as second messenger. Plant Physiol 123:1301–1311

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aquea F, Arce-Johnson P (2008) Identification of genes expressed during early somatic embryogenesis in Pinus radiata. Plant Physiol Biochem 46:559–568

    CAS  PubMed  Google Scholar 

  • Aravind L, Dixit VM, Koonin EV (1999) The domains of death: evolution of the apoptosis machinery. Trends Biochem Sci 24:47–53

    CAS  PubMed  Google Scholar 

  • Aravind L, Dixit VM, Koonin EV (2001) Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 291:1279–1284

    CAS  PubMed  Google Scholar 

  • Arroyo-Herrera A, Gonzalez AK, Moo RC, Quiroz-Figueroa FR, Loyola-Vargas VM, Rodriguez-Zapata LC, D’Hondt CB, Suarez-Solis VM, Castano E (2008) Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell Tiss Org Cult 94:171–180

    Google Scholar 

  • Baehrecke EH (2002) How death shapes life during development. Nat Rev Mol Cell Biol 3:779–787

    CAS  PubMed  Google Scholar 

  • Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–1488

    CAS  PubMed  Google Scholar 

  • Becraft PW (1998) Receptor kinases in plant development. Trends Plant Sci 3:384–388

    Google Scholar 

  • Belmonte MF, Tahir M, Schroeder D, Stasolla C (2007) Overexpression of HBK3, a class I KNOX homeobox gene, improves the development of Norway spruce (Picea abies) somatic embryos. J Exp Bot 58:2851–2861

    CAS  PubMed  Google Scholar 

  • Binarova P, Cihalikova C, Dolezel J, Gilmer S, Fowke LC (1996) Actin distribution in somatic embryos and embryogenic protoplasts of white spruce (Picea glauca). In Vitro Cell Dev Biol Plant 32:59–65

    CAS  Google Scholar 

  • Boren M, Hoglund AS, Bozhkov P, Jansson C (2006) Developmental regulation of a VEIDase caspase–like proteolytic activity in barley caryopsis. J Exp Bot 57:3747–3753

    CAS  PubMed  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C-M, 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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bozhkov PV, Lam E (2011) Green death: revealing programmed cell death in plants. Cell Death Differ 18:1239–1240

    CAS  PubMed  Google Scholar 

  • Bozhkov PV, Fílonova LH, Suarez MF, Helmersson A, Smertenko AP, Zhivotovsky B, von Arnold S (2004) VEIDase is a principal caspase–like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ 11:175–182

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bozhkov PV, Suarez MF, Fílonova LH, Daniel G, Zamyatnin AA, Rodriguez-Nieto S, Zhivotovsky B, Smertenko A (2005b) Cysteine protease mcll-Pa executes programmed cell death during plant embryogenesis. Proc Natl Acad Sci U S A 102:14463–14468

    CAS  PubMed Central  PubMed  Google Scholar 

  • Braybrook SA, Stone SL, Park S (2006) Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci U S A 103:3468–3473

    CAS  PubMed Central  PubMed  Google Scholar 

  • Butowt R, Niklas A, Rodrigues-Garcia MI, Majewska-Sawka A (1999) Involvement of JIM13 and JIM8–responsive carbohydrate epitopes in early stages of cell wall formation. J Plant Res 112:107–116

    Google Scholar 

  • Button J, Kochba J, Bornman CH (1974) Fine structure of and embryoid development from embryogenic ovular callus of ‘Shamouti’ orange (Citrus sinensis Osb). J Exp Bot 25:446–457

    Google Scholar 

  • Çaliskan M, Turet M, Cuming AC (2004) Formation of wheat (Triticum aestivum L.) embryogenic callus involves peroxide-generating germin-like oxalate oxidase. Planta 219:132–140

    PubMed  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 U S A 99:16491–16498

    CAS  PubMed Central  PubMed  Google Scholar 

  • Casson S, Lindsey K (2006) The turnip mutant of Arabidopsis reveals that LEAFY COTYLEDON1 expression mediates the effect of Auxin and sugars to promote embryonic cell identity. Plant Physiol 142:526–541

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chapman A, Blervacq A-S, Vasseur J, Hilbert J-L (2000) Arabinogalactan proteins in Cichorium somatic embryogenesis: effect of β–glucosyl Yariv reagent and epitope localisation during embryo development. Planta 211:305–314

    CAS  PubMed  Google Scholar 

  • Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI, Kim SH, Kalkum M, Hong TB, Gorshkova EN, Torrance L, Vartapetian AB, Taliansky M (2010) Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J 29:1149–1161

    CAS  PubMed  Google Scholar 

  • Chinchilla D, Frugier F, Raices M, Merchan F, Giammaria V, Gargantini P, Gonzalez-Rizzo S, Crespi M, Ulloa R (2008) A mutant ankyrin protein kinase from Medicago sativa affects Arabidopsis adventitious roots. Funct Plant Biol 35:92–101

    CAS  Google Scholar 

  • ÄŒihák A (1974) Biological effects of 5-Azacytidine in eukaryotes. Oncology 30:405–422

    PubMed  Google Scholar 

  • Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1–16

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280

    CAS  PubMed  Google Scholar 

  • Darvill A, Augur C, Bergmann C, Carlson RW, Cheong JJ, Eberhard S, Hahn MG, Lo VM, Marfa V, Meyer B, Mohnen D, Oneill MA, Spiro MD, Vanhalbeek H, York WS, Albersheim P (1992) Oligosaccharins – oligosaccharides that regulate growth, development and defence responses in plants. Glycobiology 2:181–198

    CAS  PubMed  Google Scholar 

  • De Jong AJ, Cordewener J, Lo Shiavo F, Terzi M, Vandekerckhove J, van Kammen A, de Vries SC (1992) A Daucus carota somatic embryo mutant is rescued by chitinase. Plant Cell 4:425–433

    PubMed Central  PubMed  Google Scholar 

  • De Jong AJ, Schmidt EDL, de Vries S (1993) Early events in higher plant embryogenesis. Plant Mol Biol 22:367–377

    PubMed  Google Scholar 

  • De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant Cell Environ 35:234–244

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • De Vries SC, Booij H, Meyerink P, Huisman G, Wilde DH, Thomas TL, van Kammen A (1988) Acquisition of embryogenic potential in carrot cell-suspension culture. Planta 176:196–204

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Dietz K-J, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signaling. Protoplasma 245:3–14

    CAS  PubMed  Google Scholar 

  • Dodeman VL, Ducreux G, Kreis M (1997) Zygotic embryogenesis versus somatic embryogenesis. J Exp Bot 48:1493–1509

    CAS  Google Scholar 

  • Domon JM, Neutelings G, Roger D, Daid A, David H (1995) Three glycosylated polypeptides secreted by several embryogenic cell cultures of pine show highly specific serological affinity to antibodies directed against the wheat germin apoprotein monomer. Plant Physiol 108:141–148

    CAS  PubMed Central  PubMed  Google Scholar 

  • Domon JM, Neutelings G, Roger D, David A, David H (2000) A basic chitinases-like protein secreted by embryogenic tissues of Pinus caribaea acts on arabinogalactan proteins extracted from the same cell lines. J Plant Physiol 156:33–39

    CAS  Google Scholar 

  • Downie AJ, Walker SA (1999) Plant responses to nodulation factors. Cur Opin Plant Biol 2:483–489

    CAS  Google Scholar 

  • Dubas E, Custers J, Kieft H, WÄ™dzony M, van Lammeren AA (2011) Microtubule configurations and nuclear DNA synthesis during initiation of suspensor–bearing embryos from Brassica napus cv. Topas microspores. Plant Cell Rep 30:2105–2116

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dunwell JM, Gibbings JG, Mahmood T, Naqvi SMS (2008) Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci 27:342–375

    CAS  Google Scholar 

  • Dure L, Crouch M, Harada J, Ho THD, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino-acid sequence domains among the LEA proteins of higher-plants. Plant Mol Biol 12:475–486

    CAS  PubMed  Google Scholar 

  • Dyachok JV, Tobin AE, Price NPJ, von Arnold S (2000) Rhizobial Nod factors stimulate somatic embryo development in Picea abies. Plant Cell Rep 19:290–297

    CAS  Google Scholar 

  • Dyachok JV, Wiweger M, Kenne L, von Arnold S (2002) Endogenous nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol 128:523–533

    CAS  PubMed Central  PubMed  Google Scholar 

  • Earnshaw WC, Manrtins LM, Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68:383–424

    CAS  PubMed  Google Scholar 

  • Edwards D, Murray JAH, Smith AG (1998) Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis. Plant Physiol 117:1015–1022

    CAS  PubMed Central  PubMed  Google Scholar 

  • Egertsdotter U, von Arnold S (1995) Importance of arabinogalactan proteins for the development of somatic embryos of Norway spruce (Picea abies). Physiol Plant 93:334–345

    CAS  Google Scholar 

  • Egertsdotter U, von Arnold S (1998) Development of somatic embryos of Norway spruce (Picea abies). J Exp Bot 49:155–162

    CAS  Google Scholar 

  • 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

    PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Emons AMC (1994) Somatic embryogenesis: cell biological aspects. Acta Bot Neerl 43:1–14

    Google Scholar 

  • Feher A, Pasternak TP, Duduts D (2003) Transition of somatic plant cells to embryogenic state. Plant Cell Tiss Org Cult 74:201–228

    CAS  Google Scholar 

  • Fernandez DE, Heck GR, Perry SE, Patterson SE, Bleecker AB, Fang SC (2000) The embryo MADS domain factor AGL15 acts postembryonically: inhibition of perianth senescence and abscission via constitutive expression. Plant Cell 12:183–197

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fílonova 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  Google Scholar 

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

    PubMed  Google Scholar 

  • Fílonova LH, von Arnold S, Daniel G, Bozhkov PV (2002) Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ 9:1057–1062

    PubMed  Google Scholar 

  • Fischer C, Neuhaus G (1996) Influence of auxin on the establishment of bilateral symmetry in monocots. Plant J 9:659–669

    CAS  Google Scholar 

  • Fowke LC, Attree SM, Wang H, Dunstan DI (1990) Microtubule organization and cell-division in embryogenic protoplast cultures of white spruce (Picea–glauca). Protoplasma 158:86–94

    Google Scholar 

  • Francois J, Lallemand M, Fleurat-Lessard P, Laquitaine L, Delrot S, Coutos-Thevenot P, Gomez E (2008) Overexpression of the VvLTP1 gene interferes with somatic embryo development in grapevine. Funct Plant Biol 35:394–402

    CAS  Google Scholar 

  • Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Curr Biol 108:661–673

    CAS  Google Scholar 

  • Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PBF, Ljung K, Sandberg G, Hooykaas PJJ, Palme K, Offrinbga R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Gallois JL, Woodward C, Reddy GV, Sablowski R (2002) Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129:3207–3217

    CAS  PubMed  Google Scholar 

  • Galon Y, Finkler A, Fromm H (2010) Calcium-regulated transcription in plants. Mol Plant 3:653–669

    CAS  PubMed  Google Scholar 

  • 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 4:373–385

    Google Scholar 

  • Gervais C, Newcomb W, Simmonds DH (2000) Rearrangement of the actin filament and microtubule cytoskeleton during induction of microspore embryogenesis in Brassica napus L. cv. Topas. Protoplasma 213:194–202

    Google Scholar 

  • Gou X, Yin H, He K, Du J, Yi J, Xu S, Lin H, Clouse SD, Li J (2012) Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet 8:e1002452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haccius B (1978) Question of unicellular origin of non–zygotic embryos in callus cultures. Phytomorphology 28:373–385

    Google Scholar 

  • Haecker A, Laux T (2001) Cell-cell signaling in the shoot meristem. Curr Opin Plant Biol 4:441–446

    CAS  PubMed  Google Scholar 

  • Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668

    CAS  PubMed  Google Scholar 

  • Han JJ, Lin W, Oda Y, Cui KM, Fukuda H, He XQ (2012) The proteasome is responsible for caspases-3-like activity during xylem development. Plant J 72:129–141

    CAS  PubMed  Google Scholar 

  • Hara-Nishimura I, Hatsugai N (2011) The role of vacuole in plant cell death. Cell Death Differ 18:1298–1304

    CAS  PubMed  Google Scholar 

  • Harding EW, Tang WN, 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hari V (1980) Effect of cell density changes and conditioned media on carrot somatic embryogenesis. Z Pflanzenphysiol 96:227–231

    Google Scholar 

  • Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Shinya Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858

    CAS  PubMed  Google Scholar 

  • Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I (2009) A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23:2496–2506

    CAS  PubMed  Google Scholar 

  • Hatzopolos P, Fong F, Sung ZR (1990) Abscisic acid regulation of DC8, a carrot embryogenic gene. Plant Physiol 94:690–695

    Google Scholar 

  • Hay A, Tsiantis M (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–3165

    CAS  PubMed  Google Scholar 

  • Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, Schulze WX (2008) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36:D1015–D1021

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutlilier J, 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7:1271–1282

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Helmersson A, von Arnold S, Bozhkov PV (2008) The level of free intracellular zinc mediates programmed cell death/cell survival decisions in plant embryos. Plant Physiol 147:1158–1167

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hirt H, Pay A, Gyorgyey J, Bako L, Nemeth K, Bogre L, Schweyen RJ, Heberle-Bors E, Dudits D (1991) Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologues to p34cdc2. Proc Natl Acad Sci U S A 88:552–558

    Google Scholar 

  • Hjortswang HI, Larsson AS, Bharathan G, Bozhkov PV, von Arnold S, Vahala T (2002) KNOTTED1-like homeobox genes of a gymnosperm, Norway spruce, expressed during somatic embryogenesis. Plant Physiol Biochem 40:837–843

    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

    CAS  PubMed  Google Scholar 

  • Ikeda-Iwai M, Umehara M, Satoh S, Kamada H (2003) Stress induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J 34:107–114

    CAS  PubMed  Google Scholar 

  • Jansen MAK, Booij H, Schel JHN, de Vries SC (1990) Calcium increases the yield of somatic embryos in carrot embryogenic suspension cultures. Plant Cell Rep 9:221–223

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Jeong S, Palmer TP, Lukowitz W (2011) The RWP–RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signalling. Curr Biol 21:1268–1276

    CAS  PubMed  Google Scholar 

  • Jimenez VM (2005) Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis. Plant Growth Regul 47:91–110

    CAS  Google Scholar 

  • Jones PL, Wolffe AP (1999) Relationships between chromatic organisation and DNA methylation in determining gene expression. Semin Cancer Biol 9:33–347

    Google Scholar 

  • Joosen R, Cordewener J, Supena EDJ, Vorst O, Lammers M, Maliepaard C, Zeilmaker T, Miki B, America T, Custers J, Boutilier K (2007) Combined transcriptome and proteome analysis identifies pathways and markers associated with the establishment of rapeseed microspore-derived embryo development. Plant Physiol 144:155–172

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kader JC (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47:627–654

    CAS  PubMed  Google Scholar 

  • Karami O, Saidi A (2010) The molecular basis for stress–induced acquisition of somatic embryogenesis. Mol Biol Rep 37:2493–2507

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karlova R, Boern S, van Dongen W, Kwaitaal M, Aker J, Vervoort J, de Vries S (2009) Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics 9:368–379

    CAS  PubMed  Google Scholar 

  • Kawashima T, Goldberg RB (2010) The suspensor: not just suspending the embryo. Trends Plant Sci 15:23–30

    CAS  PubMed  Google Scholar 

  • Kiselev KV, Gorpenchenko TY, Tchernoded GK, Dubrovina AS, Grishchenko OV, Bulgakov VP, Zhuravlev YN (2008) Calcium-dependent mechanism of somatic embryogenesis in Panax ginseng cell cultures expressing the rolC oncogene. Cell Mol Biol 42:243–252

    CAS  Google Scholar 

  • Klimaszewska K, Pelletier G, Overton C, Stewart D, Rutledge RG (2010) Hormonally regulated overexpression of Arabidopsis WUS and conifer LEC1 (CHAP3A) in transgenic white spruce: implications for somatic embryo development and somatic seedling growth. Plant Cell Rep 29:723–734

    CAS  PubMed  Google Scholar 

  • Konieczny R, Bohdanowicz J, Czaplicki AZ, Przywara L (2005) Extracellular matrix surface network during plant regeneration in wheat anther culture. Plant Cell Tiss Org Cult 83:201–208

    Google Scholar 

  • Koonin EV, Aravind L (2002) Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ 9:394–404

    CAS  PubMed  Google Scholar 

  • Kreuger M, van Holst GJ (1995) Arabinogalactan-protein epitopes in somatic embryogenesis of Daucus carota L. Planta 197:135–141

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Larsson E, Sitbon F, Ljung K, von Arnold S (2008) Inhibited polar auxin transport results in aberrant embryo development in Norway spruce. New Phytol 177:356–366

    CAS  PubMed  Google Scholar 

  • Larsson E, Sitbon F, von Arnold S (2012) Differential regulation of Knotted1-like genes during establishment of the shoot apical meristem in Norway spruce (Picea abies). Plant Cell Rep 31:1053–1060

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ledwon A, Gaj MD (2011) LEAFY COTYLEDON1, FUSCA3 expression and auxin treatment in relation to somatic embryogenesis induction in Arabidopsis. Plant Growth Regul 65:157–167

    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

    CAS  PubMed  Google Scholar 

  • Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis. Nature 379:66–69

    CAS  PubMed  Google Scholar 

  • Lotan T, Ohto M, Yee KM (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    CAS  PubMed  Google Scholar 

  • Luerssen H, Kirik V, Herrmann P, Miséra S (1998) FUSCA3 encodes a protein with a conserve VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764

    CAS  PubMed  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

    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 postembryogenic development. FEBS Lett 580:5111–5116

    CAS  PubMed  Google Scholar 

  • Ma HC, McMullen MD, Finer JJ (1994) Identification of a homeobox–containing gene with enhanced expression during soybean (Glycine max L.) somatic embryo development. Plant Mol Biol 24:465–473

    CAS  PubMed  Google Scholar 

  • Magioli C, Barroco RM, Rocha CAB, de Santiago-Fernandes LD, Mansur E, Engler G, Margis-Pinheiro M, Sachetto-Martins G (2001) Somatic embryo formation in Arabidopsis and eggplant is associated with expression of a glycine–rich protein gene (Atgrp–5). Plant Sci 161:559–567

    CAS  Google Scholar 

  • Maheswaran G, Williams EG (1985) Origin and development of somatic embryoids formed directly on immature embryos of Trifolium repens in vitro. Ann Bot 56:619–630

    Google Scholar 

  • Maillet F, Poinsot V, Andre O, Puech-Page V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Andres Martinez E, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63

    CAS  PubMed  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9

    CAS  PubMed Central  PubMed  Google Scholar 

  • Malinowski R, Filipecki M (2002) The role of cell wall in plant embryogenesis. Cell Mol Biol Lett 7:1137–1151

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maraschin SDF, Gaussand G, Pulido A, Olmedilla A, Lamers GE, Korthout H, Spaink HP, Wang M (2005) Programmed cell death during the transition from multicellular structures to globular embryos in barley androgenesis. Planta 221:459–470

    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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • McCabe PF, Valentine TA, Forsberg LS, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9:2225–2241

    CAS  PubMed Central  PubMed  Google Scholar 

  • McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The viviparous–1 developmental gene of maize encodes a novel transcriptional activator. Cell 66:895–905

    CAS  PubMed  Google Scholar 

  • Meinke DW (1992) A homoeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science 258:1647–1650

    CAS  PubMed  Google Scholar 

  • Meinke DW, Franzmann LH, Nickle TC, Yeung EC (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064

    CAS  PubMed Central  PubMed  Google Scholar 

  • Merkele SA, Parrott WA, Flinn BS (1995) Morphogenic aspects of somatic embryogenesis. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer, Dordrecht/Boston/London, pp 155–203

    Google Scholar 

  • Michalczuk L, Cooke TJ, Cohen JD (1992a) Auxin levels at different stages of carrot somatic embryogenesis. Phytochemistry 31:1097–1103

    CAS  Google Scholar 

  • Michalczuk L, Ribnicky DM, Cooke TJ, Cohen HD (1992b) Regulation of indole-3-acetic acid biosynthetic pathways in carrot cell cultures. Plant Physiol 100:1346–1353

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mordhorst AP, Hartog MV, El Tamer MK, Laux T, de Vries SC (2002) Somatic embryogenesis from Arabidopsis shoot apical meristem mutants. Planta 214:829–836

    CAS  PubMed  Google Scholar 

  • Nagata T, Ishida S, Hasezawa S, Takahashi Y (1994) Genes involved in the dedifferentiation of plant cells. Int J Dev Biol 38:321–327

    CAS  PubMed  Google Scholar 

  • Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17:1908–1925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Neutelings G, Domon JM, Membré 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nolan KE, Kurdyukov S, Rose RJ (2011) Characterisation of the legume SERK–NIK gene superfamily including splice variants: Implications for development and defence. BMC Plant Biol 11:44

    CAS  PubMed Central  PubMed  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 U S A 96:13839–13844

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oh SH, Steiner HY, Dougall DK, Roberts DM (1992) Modulation of calmodulin levels, calmodulin methylation, and calmodulin binding proteins during carrot cell growth and embryogenesis. Arch Biochem Biophys 297:28–34

    CAS  PubMed  Google Scholar 

  • Overvoorde PJ, Grimes HD (1994) The role of calcium and calmodulin in carrot embryogenesis. Plant Cell Physiol 35:135–144

    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

    CAS  PubMed  Google Scholar 

  • Palovaara J, Hallberg H, Stasolla C, Hakman I (2010) Comparative expression pattern analysis of WUSCHEL-related homeobox 2 (WOX2) and WOX8/9 in developing seeds and somatic embryos of the gymnosperm Picea abies. New Phytol 188:122–135

    CAS  PubMed  Google Scholar 

  • Parcy F, Valon C, Kohara A, Misera 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Passarinho PA, Van Hengel AJ, Fransz PF, De Vries SC (2001) Expression pattern of the Arabidopsis thaliana AtEP3/AtchilV endochitinase gene. Planta 212:556–567

    CAS  PubMed  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

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perry SF, Nichols KW, Fernandez DE (1996) The MADS domain protein AGL15 localizes to the nucleus during early stages of seed development. Plant Cell 8:2488–2495

    Google Scholar 

  • Petrussa E, Bertolini A, Casolo V, Krajnakova J, Macri F, Vianello A (2009) Mitochondrial bioenergetics linked to the manifestation of programmed cell death during somatic embryogenesis of Abies alba. Planta 231:93–107

    CAS  PubMed  Google Scholar 

  • Poon S, Heath RL, Clarke AE (2012) A chimeric arabinogalactan protein promotes somatic embryogenesis in cotton cell culture. Plant Physiol 160:684–695

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pullman GS, Zhang Y, Phan BH (2003) Brassinolide improves embryogenic tissue initiation in conifers and rice. Plant Cell Rep 22:96–104

    CAS  PubMed  Google Scholar 

  • Raghavan V (1976) Adventive embryogenesis: induction of diploid embryoids. In: Experimental embryogenesis in vascular plants. Academic, London, pp 349–381, Chapter 14

    Google Scholar 

  • Reinert J (1958) Untersuchungen über die Morphogenese an Gewebekulturen. Ber Dtsch Bot Ges 71:15

    Google Scholar 

  • Rensing SA, Lang D, Schumann E, Reski R, Hohe A (2005) EST sequencing from embryogenic Cyclamen periscum cell cultures identifies a high proportion of transcripts homologous to plant genes involved in somatic embryogenesis. J Plant Growth Regul 24:102–115

    CAS  Google Scholar 

  • Rounsley SD, Ditta GS, Yanofsky MF (1995) Diverse roles for MADS box genes in Arabidopsis development. Plant Cell 7:1259–1269

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rumyantseva NI, Samaj J, Ensikat HJ, Salnikov VV, Kostyukova Y, Baluska G, Volkman D (2003) Changes in the extracellular matrix surface network during cyclic reproduction of proembryogenic cell complex in the Fagopyrum tataricum (L.) Gaertn callus. Dokl Biol Sci 391:375–378

    CAS  PubMed  Google Scholar 

  • Sagare AP, Lee YL, Lin TC, Chen CC, Tsay HS (2000) Cytokinin-induced somatic embryogenesis and plant regeneration in Corydalis yanhusuo (Fumariaceae) – a medicinal plant. Plant Sci 160:139–147

    CAS  PubMed  Google Scholar 

  • Salaj J, von Recklinghausen IR, Hecht V, de Vries SC, Schel JHN, van Lammeren AM (2008) AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiol Biochem 46:709–714

    CAS  PubMed  Google Scholar 

  • Sanders D, Brownlee C, Harper JF (1999) Communicating with calcium. Plant Cell 11:691–706

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sato A, Yamamoto KT (2008) Overexpression of the non-canonical Aux/IAA genes causes auxin-related aberrant phenotypes in Arabidopsis. Physiol Plant 133:397–405

    CAS  PubMed  Google Scholar 

  • Sato S, Toya T, Kawahara R, Whittier RF, Fukuda H, Komamine A (1995) Isolation of a carrot gene expressed specifically during early-stage somatic embryogenesis. Plant Mol Biol 28:39–46

    CAS  PubMed  Google Scholar 

  • Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Schrick K, Fujioka S, Takatsuto S, Stierhof YD, Stransky H, Yoshida S, Jurgens G (2004) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38:227–243

    CAS  PubMed  Google Scholar 

  • Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, Jenuwein T, Goodrich J (2006) Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J 25:4638–4649

    CAS  PubMed  Google Scholar 

  • Schwarzerová K, Vondraková Z, Fischer L, Boriková P, Bellinvia E, Eliasová K, Havelková L, FiÅ¡erová J, Vagner M, Opatrný Z (2010) The role of actin isoforms in somatic embryogenesis in Norway spruce. BMC Plant Biol 10:89

    PubMed Central  PubMed  Google Scholar 

  • Senger S, Mock HP, Conrad U, Manteuffel R (2001) Immunomodulation of ABA function affects early events in somatic embryo development. Plant Cell Rep 20:112–120

    CAS  Google Scholar 

  • Shah K, Gadella TW Jr, van Erp H, Hecht V, de Vries SC (2001) Subcellular localization and oligomerization of the Arabidopsis thaliana somatic embryogenesis receptor kinase 1 protein. J Mol Biol 309:641–655

    CAS  PubMed  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 50 –upstream region. Gene 437:22–31

    CAS  PubMed  Google Scholar 

  • Simmonds DH, Keller WA (1999) Significance of preprophase bands of microtubules in the induction of microspore embryogenesis of Brassica napus. Planta 208:383–391

    CAS  Google Scholar 

  • Singh H (1978) Embryology of gymnosperms. Bornträger, Berlin

    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 5:677–692

    Google Scholar 

  • Smertenko A, Franklin-Tong VE (2011) Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death Differ 18:1263–1270

    CAS  PubMed  Google Scholar 

  • Smertenko AP, Bozhkov PV, Fílonova LH, von Arnold S, Hussey PJ (2003) Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J 33:813–824

    CAS  PubMed  Google Scholar 

  • Smith JA, Sung ZR (1985) Increase in regeneration of plant cells by cross feeding with regenerating Daucus carota cells. In: Terzi N, Pitto L, Sung ZR (eds) Somatic embryogenesis. Incremento Produttivita Risorse Agricole, Rome, pp 133–136

    Google Scholar 

  • Somleva MN, Schmidt ED, 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

    CAS  Google Scholar 

  • Spaink HP, Sheeley DM, Van Brussel AAN, Glushka H, York WS, Tak T, Geiger O, Kennedy EP, Reinohld VN, Lugtenberg BJJ (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354:125–130

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sterk P, Booij H, Schellekens G, Van Kammen A, De Vries S (1991) Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3:907–921

    CAS  PubMed Central  PubMed  Google Scholar 

  • Steward FC, Mapes MO, Hears K (1958) Growth and organize development of cultured cells II Growth and division of freely suspended cells. Am J Bot 45:705–708

    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 U S A 98:11806–11811

    CAS  PubMed Central  PubMed  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 U S A 105:3151–3156

    CAS  PubMed Central  PubMed  Google Scholar 

  • Street HE, Withers LA (1974) The anatomy of embryogenesis in culture. In: Street HE (ed) Tissue culture and plant science. Academic, London

    Google Scholar 

  • Suarez MF, Fílonova LH, Smertenko A, Savenkov EI, Clapham DH, von Arnold S, Zhivotovsky B, Bozhkov PV (2004) Metacaspase–dependent programmed cell death is essential for plant embryogenesis. Curr Biol 14:R339–R340

    CAS  PubMed  Google Scholar 

  • Sundstrom JF, Vaculova A, Smertenko AP, Savenkov EI, Golovko A, Minina E, Tiwari BS, Rodriguez-Nieto S, Zamyatnin AA, Valineva T, Saarikettu J, Frilander MJ, Suarez MF, Zavialov A, Stahl U, Hussey PJ, Silvennoinen O, Sundberg E, Zhivotovsky B, Bozhkov PV (2009) Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat Cell Biol 11:1347–1354

    PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Svetek J, Yadav MP, Nothnagel EA (1999) Presence of glycosylphosphatidylinositol lipid anchor on rose arabinogalactan proteins. J Biol Chem 274:14724–14733

    CAS  PubMed  Google Scholar 

  • Tang XC, Liu Y, He YQ, Ma LG, Sun MX (2013) Exine dehiscing induces rape microspore polarity, which results in different daughter cell fate and fixes the apical–basal axis of the embryo. J Exp Bot 64:215–228

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thibaud-Nissen F, Shealy RT, Khanna A, Vodkin J (2003) Clustering of microarray data reveals transcript patterns associated with somatic embryogenesis in soybean. Plant Physiol 132:118–136

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thoma S, Hecht U, Kippers A, Botella J, De Vries S, Somerville C (1994) Tissue-specific expression of gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol 105:35–45

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson HJM, Knox JP (1998) Stage-specific responses of embryogenic carrot cell suspension cultures to arabinogalactan protein-binding β-glucosyl Yariv reagent. Planta 205:32–38

    CAS  Google Scholar 

  • Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281:1312–1316

    CAS  PubMed  Google Scholar 

  • Timmers ACJ, Reiss HD, Bohsung J, Traxel K, Schel JHN (1996) Localization of calcium during somatic embryogenesis of carrot (Daucus carota L.). Protoplasma 190:107–118

    Google Scholar 

  • Tisserat B, Esan EB, Murashige T (1979) Somatic embryogenesis in angiosperms. Hortic Rev 1:1–78

    Google Scholar 

  • Toonen MA, Hendriks T, Schmidt EDL, Verhoeven HA, van Kammen A, de Vries SC (1994) Description of somatic-embryo-forming single cells in carrot suspension–cultures employing video cell tracking. Planta 194:565–572

    CAS  Google Scholar 

  • Toonen MA, Verhees JA, Schmidt EDL, van Kammen A, de Vries SC (1997) AtLTP1 luciferase expression during carrot somatic embryogenesis. Plant J 12:1213–1221

    CAS  PubMed  Google Scholar 

  • Trigiano RN, Gray DJ, Conger BM, McDaniel JK (1989) Origin of direct somatic embryos from cultured leaf segments of Dactylis glomerata. Bot Gaz 150:72–77

    Google Scholar 

  • Truchet G, Roche P, Lerouge P, Vasse J, Camut S, de Billy F, Prome JC, Denarie J (1991) Sulfated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670–673

    CAS  Google Scholar 

  • Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV (2011) Metacaspases. Cell Death Differ 8:1279–1288

    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

    CAS  PubMed  Google Scholar 

  • Uddenberg D, Valladares S, Abrahamsson M, Sundström JF, SundÃ¥s-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 234:527–539

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uren AG, O'Rourke K, Aravind L, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (2000) Identification of paracaspases and metacaspases, Two ancient families of caspase–like proteins, one of which plays a key role in MALT lymphoma. Mol Cell 6:961–967

    CAS  PubMed  Google Scholar 

  • van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LAJ, Petersen M, Smertenko A, Taliansky M, van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246

    PubMed  Google Scholar 

  • Van Hengel AJ, Guzzo F, van Kammen A, de Vries SC (1998) Expression pattern of the carrot EP3 endochitinase genes in suspension cultures and in developing seeds. Plant Physiol 117:34–53

    Google Scholar 

  • Van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, Van Kammen A, De Vries SC (2001) N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol 117:43–53

    Google Scholar 

  • Van Zyl L, Bozhkov PV, Clapham DH, Sederoff RR, von Arnold S (2003) Up, down and up again is a signature global gene expression pattern at the beginning of gymnosperm embryogenesis. Gene Expr Patterns 3:83–91

    PubMed  Google Scholar 

  • Vartapetian AB, Tuzhikov AI, Chichkova NV, Taliansky M, Wolpert TJ (2011) A plant alternative to animal caspases: subtilisin–like proteases. Cell Death Differ 18:1289–1297

    CAS  PubMed  Google Scholar 

  • Vasil IK, Vasil V (1980) Clonal propagation. Int Rev Cytol Suppl 11A:145–173

    Google Scholar 

  • Vercammen D, van de Cotte B, de Jaeger G, Eekhout D, Casteels P, Vandepoele K, Vandenberghe I, van Veeumen J, Inze D, van Breusegem F (2004) Type-II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 279:45329–45336

    CAS  PubMed  Google Scholar 

  • Vernon DM, Meinke DW (1994) Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis. Dev Biol 165:566–573

    CAS  PubMed  Google Scholar 

  • Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243

    CAS  PubMed  Google Scholar 

  • von Arnold S, Sabala I, Bozhkov P, Dyachok J, Fílonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tiss Org Cult 69:233–249

    Google Scholar 

  • Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K (2011) The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 21:1277–1281

    CAS  PubMed  Google Scholar 

  • Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345:743

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • West M, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6:1731–1745

    CAS  PubMed Central  PubMed  Google Scholar 

  • William DA, Su YH, Smith MR, Lu M, Baldwin DA, Wagner D (2004) Genomic identification of direct target genes of LEAFY. Proc Natl Acad Sci U S A 101:1775–1780

    CAS  PubMed Central  PubMed  Google Scholar 

  • Williams EG, Maheswaran G (1986) Somatic embryogenesis: factors influencing coordinated behaviour of cells as an embryogenic group. Ann Bot 57:443–462

    Google Scholar 

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

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wojtaszek P, Pislewska M, Bolwell GP, Stobiecki M (1998) Secretion of stress–related proteins by suspension–cultured Lupinus albus cells. Acta Biochim Pol 45:281–285

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Xu XH, Briere C, Vallee N, Borin C, van Lammeren AAM, Albert G, Souvre A (1999) In vivo labeling of sunflower embryonic tissues by fluorescently labeled phenylalkylamine. Protoplasma 210:52–58

    Google Scholar 

  • Yadegari R, de Pavia GR, Laux T, Koltunow AM, Apuya N, Zimmerman J, Fisher RL, Harada JJ, Goldberd RB (1994) Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell 6:1713–1729

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto N, Kobayashi H, Togashi T, Mori Y, Kikuchi K, Kuriyama K, Tokuji Y (2005) Formation of embryogenic cell clumps from carrot epidermal cells is suppressed by 5–azacytidine, a DNA methylation inhibitor. J Plant Physiol 162:47–54

    CAS  PubMed  Google Scholar 

  • Yang X, Zhang X (2010) Regulation of somatic embryogenesis in higher plants. Crit Rev Plant Sci 29:36–57

    CAS  Google Scholar 

  • Yeung EC (1995) Structural and developmental patterns in somatic embryogenesis. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer, Dordrecht/Boston/London, pp 205–247

    Google Scholar 

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

    PubMed Central  PubMed  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

    CAS  PubMed  Google Scholar 

  • Zhang JZ, Somerville CR (1997) Suspensor driven polyembryony caused by altered expression of valyl-tRNA synthase in the twin2 mutant of Arabidopsis. Proc Natl Acad Sci U S A 94:7349–7355

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Qi L (2010) 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

    CAS  PubMed  Google Scholar 

  • Zhao JP, Simmonds DH, Newcomb W (1996) Induction of embryogenesis with colchicine instead of heat in microspores of Brassica napus L. cv. Topas. Planta 198:433–439

    CAS  Google Scholar 

  • Zhao P, Zhou XM, Zhang LY, Wang W, Ma LG, Yang LB, Peng XB, Bozhkov PV, Sun MX (2013) A bipartite molecular module controls cell death activation in the basal cell lineage of plant embryos. PLoS Biol 11(9):e1001655

    CAS  PubMed Central  PubMed  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 21:2536–2577

    Google Scholar 

  • Zhu C, Perry SE (2005) Control of expression and autoregulation of AGL15, a member of the MADS-box family. Plant J 41:583–594

    PubMed  Google Scholar 

  • Zhu HG, Tu LL, Jin SX, Xu L, Tan JF, Deng FL, Zhang XL (2008) Analysis of genes differentially expressed during initial cellular dedifferentiation in cotton. Chin Sci Bull 23:3666–3676

    Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Biological Chemistry, Washington State University, Pullman, WA, 99164-6340, USA

    Andrei Smertenko

  2. Department of Plant Biology and Forest Genetics, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 750 07, Uppsala, Sweden

    Peter Bozhkov

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  1. Andrei Smertenko
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  2. Peter Bozhkov
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Correspondence to Andrei Smertenko .

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Editors and Affiliations

  1. Botanical Institute, University of Karlsruhe, Karlsruhe, Germany

    Peter Nick

  2. Charles University, Prague, Czech Republic

    Zdeněk Opatrny

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Smertenko, A., Bozhkov, P. (2014). The Life and Death Signalling Underlying Cell Fate Determination During Somatic Embryogenesis. In: Nick, P., Opatrny, Z. (eds) Applied Plant Cell Biology. Plant Cell Monographs, vol 22. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-41787-0_5

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