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Transition of somatic plant cells to an embryogenic state

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Abstract

Under appropriate in vivo or in vitro conditions, certain somatic plant cells have the capability to initiate embryogenic development (somatic embryogenesis). Somatic embryogenesis provides an unique experimental model to understand the molecular and cellular bases of developmental plasticity in plants. In the last few years, the application of modern experimental techniques, as well as the characterization of Arabidopsis embryogenesis mutants, have resulted in the accumulation of novel data about the acquisition of embryogenic capabilities by somatic plant cells. In this review, we summarize relevant experimental observations that can contribute to the description and definition of a transitional state of somatic cells induced to form totipotent, embryogenic cells. During this somatic-to-embryogenic transition, cells have to dedifferentiate, activate their cell division cycle and reorganize their physiology, metabolism and gene expression patterns. The roles of stress, endogenous growth regulators and chromatin remodelling in the coordinated reorganization of the cellular state are especially emphasized.

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References

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

    Google Scholar 

  • Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M & Feijo JA (2000) A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants. Proc. Natl. Acad. Sci. USA 97: 10643–10648

    Google Scholar 

  • Baldan B, Guzzo F, Filippini F, Gasparian M, LoSchiavo F, Vitale A, deVries SC, Mariani P & Terzi M (1997) The secretory nature of the lesion of carrot cell variant ts 11, rescuable by endochitinase. Planta 203: 381–389

    Google Scholar 

  • Basu S, Sun H, Brian L, Quatrano RL & Muday GK (2002) Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol. 130: 292–302

    Google Scholar 

  • Beeckman T, Burssens S & Inze D (2001) The peri-cell-cycle in Arabidopsis. J. Exp. Bot. Suppl. 52: 403–411

    Google Scholar 

  • Belanger KD & Quatrano RS (2000) Polarity: the role of localized secretion. Curr. Opin. Plant Biol. 3: 67–72

    Google Scholar 

  • Bibikova TN, Jacob T, Dahse I & Gilroy S (1998) Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 125: 2925–2934

    Google Scholar 

  • Blervacq AS, Dubois T, Dubois J & Vasseur J (1995) First divisions of somatic embryogenic cells in Cichorium hybrid '474'. Protoplasma 186: 163–168

    Google Scholar 

  • Boutilier K, Offringa R, Fukuoka H, Sharma V, Kieft H, van Lammeren AAM, Ouellett T & van Lookeren C (2000) Ectopic expression of the Brassica napus baby boom gene triggers a homeotic conversion of vegetative tissues into embryos and cotyledons (Abstract). Plant Mol. Biol. Rep. 18: s11–s14

    Google Scholar 

  • Bögre L, Stefanov I, Ábrahám M, Somogyi I & Dudits D (1990) Differences in the responses to 2,4-dichlorophenoxyacetic acid (2,4-D) treatment between embryogenic and non-embryogenic lines of alfalfa. In: Nijkamp HJJ, van der Plas LHW & Van Aartrijk J (eds) Progress in Plant Cellular and Molecular Biology (pp. 427–436). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Busch M, Mayer U & Jurgens G (1996) Molecular analysis of the Arabidopsis pattern formation gene GNOM: gene structure and intragenic complementation. Mol. Gen. Genet. 250: 681–691

    Google Scholar 

  • Capitanio G, Baldan B, Filippini F, Terzi M, LoSchiavo F & Mariani P (1997) Morphogenetic effects of Brefeldin A on embryogenic cell cultures of Daucus carota L. Planta 203: 121–128

    Google Scholar 

  • Chapman A, Blervacq AS, Vasseur J & Hilbert JL (2000) Arabinogalactan-proteins in Cichorium somatic embryogenesis: effect of beta-glucosyl Yariv reagent and epitope localization during embryo development. Planta 211: 305–314

    Google Scholar 

  • Charrière F, Sotta B, Miginiac É & Hahne G (1999) Induction of adventitious or somatic embryos on in vitro cultured zygotic embryos of Helianthus annuus: Variation of endogenous hormone levels. Plant Physiol. Biochem. 37: 751–757

    Google Scholar 

  • Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES & Peacock WJ (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94: 4223–4228

    Google Scholar 

  • Chaudhury AM, Koltunow A, Payne T, Luo M, Tucker MR, Dennis ES & Peacock WJ (2001) Control of early seed development. Annu. Rev. Cell Dev. Biol. 17: 677–699

    Google Scholar 

  • Choi YE, Kim HS, Soh WY & Yang DC (1997) Developmental and structural aspects of somatic embryos formed on medium containing 2,3,5-triiodobenzoic acid. Plant Cell Rep. 16: 738–744

    Google Scholar 

  • Choi YE, Yang DC, Park JC, Soh WY & Choi KT (1998) Regenerative ability of somatic single and multiple embryos from cotyledons of Korean ginseng on hormone-free medium. Plant Cell Rep. 17: 544–551

    Google Scholar 

  • Coca MA, Almoguera C & Jordano J (1994) Expression of sunflower low-molecular-weight heat-shock proteins during embryogenesis and persistence after germination: localization and possible functional implications. Plant Mol. Biol. 25: 479–492

    Google Scholar 

  • Cove DJ (2000) The generation and modification of cell polarity. J. Exp. Bot. 51: 831–838

    Google Scholar 

  • Criqui MC, Plesse B, Durr A, Marbach J, Parmentier Y, Jamet E & Fleck J (1992) Characterization of genes expressed in mesophyll protoplasts of Nicotiana sylvestris before the re-initiation of the DNA replicational activity. Mech. Dev. 38: 121–132

    Google Scholar 

  • Criqui MC, Parmentier Y, Derevier A, Shen WH, Dong AW & Genschik P (2000) Cell cycle-dependent proteolysis and ectopic overexpression of cyclin B1 in tobacco BY2 cells. Plant J. 24: 763–773

    Google Scholar 

  • Davletova S, Mészáros T, Miskolczi P, Oberschall A, Török K, Magyar Z, Dudits D & Deák M (2001) Auxin and heat shock activation of a novel member of the calmodulin like domain protein kinase gene family in cultured alfalfa cells. J. Exp. Bot. 52: 215–221

    Google Scholar 

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

    Google Scholar 

  • den Boer BG & Murray JA (2000) Triggering the cell cycle in plants. Trends Cell Biol. 10: 245–250

    Google Scholar 

  • Denchev PD, Velcheva MR & Atanassov AI (1991) A new approach to direct somatic embryogenesis in Medicago. Plant Cell Rep. 10: 338–341

    Google Scholar 

  • Deshpande S & Hall JC (2000) Auxinic herbicide resistance may be modulated at the auxin-binding site in wild mustard (Sinapis arvensis L.): A light scattering study. Pestic. Biochem. Physiol. 66: 41–48

    Google Scholar 

  • Dijak M & Simmonds DH (1988) Microtubule organization during early direct embryogenesis from mesophyll protoplasts of Medicago sativa L. Plant Sci. 58: 183–191

    Google Scholar 

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

    Google Scholar 

  • Dong JZ & Dunstan DI (1996) Expression of abundant mRNAs during somatic embryogenesis of white spruce [Picea glauca (Moench) Voss]. Planta 199: 459–466

    Google Scholar 

  • Dong JZ & Dunstan DI (1999) Cloning and characterization of six embryogenesis associated cDNAs from somatic embryos of Picea glauca and their comparative expression during zygotic embryogenesis. Plant Mol. Biol. 39: 859–864

    Google Scholar 

  • Dubois T, Guedira M, Dubois J & Vasseur J (1990) Direct somatic embryogenesis in roots of Cichorium. Is callose an early marker? Ann. Bot. 65: 539–545

    Google Scholar 

  • Dubois T, Guedira M, Dubois J & Vasseur J (1991) Direct somatic embryogenesis in leaves of Cichorium. A histological and S.E.M. study of early stages. Protoplasma 162: 120–127

    Google Scholar 

  • Dudits D, Bogre L & Györgyey J (1991) Molecular and cellular approaches to the analysis of plant embryo development from somatic cells in vitro. J. Cell Sci. 99: 475–484

    Google Scholar 

  • Dudits D, Györgyey J, Bögre L & Bakó L (1995) Molecular biology of somatic embryogenesis. In: Thorpe TA (ed) In Vitro Embryogenesis in Plants (pp. 267–308). Kluwer Academic Publisher, Dordrecht

    Google Scholar 

  • Dudits D, Magyar Z, Deak M, Mészáros T, Miskolczi P, Fehér A, Brown S, Kondorosi E, Athanasiadis A, Pongor S, Bako L, ¨ Koncz C & Györgyey J (1998) Cyclin and calcium dependent kinase families: response of cell division cycle to hormone and stress signals. In: Francis D, Dudits D & Inze D (eds) Plant Cell Division (pp. 21–47). Portland Press, London, UK

    Google Scholar 

  • Eastmond PJ & Rawsthorne S (1998) Comparison of the metabolic properties of plastids isolated from developing leaves or embryos of Brassica napus L. J. Exp. Bot. 49: 1105–1111

    Google Scholar 

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

    Google Scholar 

  • Fargasova A (1994) Comparative study of plant growth hormone (herbicide) toxicity in various biological subjects. Ecotoxicol. Environ. Saf. 29: 359–364

    Google Scholar 

  • Faure JE & Dumas C (2001) Fertilization in flowering plants. New approaches for an old story. Plant Physiol. 125: 102–104

    Google Scholar 

  • Fehér A, Pasternak T, Miskolczi P, Ayaydin F & Dudits D (2001) Induction of the embryogenic pathway in somatic plant cells. Acta Hort. 560: 293–298

    Google Scholar 

  • Fehér A, Pasternak T, Ötvös K, Miskolczi P & Dudits D (2002) Induction of embryogenic competence in somatic plant cells: a review. Biologia 57: 5–12

    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

    Google Scholar 

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

    Google Scholar 

  • Fleck J & Durr A (1980) Comparison of proteins synthetized in vivo and in vitro by mRNA of isolated protoplasts. Planta 148: 453–454

    Google Scholar 

  • Fletcher JC & Meyerowitz EM (2000) Cell signaling within the shoot meristem. Curr. Opin. Plant Biol. 3: 23–30

    Google Scholar 

  • Fowler JE & Quatrano RS (1997) Plant cell morphogenesis: Plasma membrane interactions with the cytoskeleton and cell wall. Annu. Rev. Cell Dev. Biol. 13: 697–743

    Google Scholar 

  • Fowler MR, Ong LM, Russinova E, Atanassov AI, Scott NW, Slater A & Elliott MC (1998) Early changes in gene expression during direct somatic embryogenesis in alfalfa revealed by RAP-PCR. J. Exp. Bot. 49: 249–253

    Google Scholar 

  • Frelin C, Vigne P, Ladoux A & Lazdunski M (1988) The regulation of the intracellular pH in cells from vertebrates. Eur. J. Biochem. 174: 3–14

    Google Scholar 

  • Gao CY & Zelenka PS (1997) Cyclins, cyclin-dependent kinases and differentiation. Bioessays 19: 307–315

    Google Scholar 

  • Geldner N, Friml J, Stierhof YD, Jurgens G & Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425–428

    Google Scholar 

  • Genschik P, Criqui MC, Parmentier Y, Derevier A & Fleck J (1998) Cell cycle-dependent proteolysis in plants: Identification of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor MG132. Plant Cell 10: 2063–2075

    Google Scholar 

  • Gianazza E, De Ponti P, Scienza A, Villa P & Martinelli L (1992) Monitoring by two-dimensional electrophoresis somatic embryogenesis in leaf and petiole explants from Vitis. Electrophoresis 13: 203–209

    Google Scholar 

  • Giroux RW & Pauls KP (1997) Characterization of somatic embryogenesis-related cDNAs from alfalfa (Medicago sativa L.). Plant Mol. Biol. 33: 393–404

    Google Scholar 

  • Goldsworthy A & Mina MG (1991) Electrical patterns of tobacco cells in media containing indole-3-acetic acid or 2,4-dichloro-phenoxyacetic acid. Planta 183: 386–373

    Google Scholar 

  • Gray WM & Estelle M (2000) Function of the ubiquitin–protea-some pathway in auxin response. Trends Biochem. Sci. 25: 133–138

    Google Scholar 

  • Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby WL, Yang M, Ma H & Estelle M (1999) Identification of an SCF ubiquitin–ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev. 13: 1678–1691

    Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O & Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414: 271–276

    Google Scholar 

  • Gross JD, Bradbury J, Kay RR & Peacey MJ (1983) Intracellular pH and the control of cell differentiation in Dictyostelium discoideum. Nature 303: 244–245

    Google Scholar 

  • Grosset J, Marty I, Chartier Y & Meyer Y (1990) mRNAs newly synthetized by tobacco mesophyll protoplasts are wound inducible. Plant Mol. Biol. 15: 485–496

    Google Scholar 

  • Grossmann K (2000) Mode of action of auxinic herbicides: a new ending to a long, drawn out story. Trends Plant Sci. 5: 506–508

    Google Scholar 

  • Grossniklaus U, Vielle-Calzada JP, Hoeppner MA & Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280: 446–450

    Google Scholar 

  • Grossniklaus U, Spillane C, Page DR & Kohler C (2001) Genomic imprinting and seed development: endosperm formation with and without sex. Curr. Opin. Plant Biol. 4: 21–27

    Google Scholar 

  • Gutierrez C (1998) The retinoblastoma pathway in plant cell cycle and development. Curr. Opin. Plant Biol. 1: 492–497

    Google Scholar 

  • Györgyey J, Nemeth K, Magyar Z, Kelemen Z, Alliotte T, Inze D & Dudits D (1997) Expression of a novel-type small proline rich protein gene of alfalfa is induced by 2,4-dichlorophenoxiacetic acid in dedifferentiated callus cells. Plant Mol. Biol. 34: 593–602

    Google Scholar 

  • Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U & de Vries SC (2001) The Arabidopsis somatic embryogenesis receptor kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 127: 803–816

    Google Scholar 

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

    Google Scholar 

  • Helleboid S, Hendriks T, Bauw G, Inze D, Vasseur J & Hilbert JL (2000b) Three major somatic embryogenesis related proteins in Cichorium identified as PR proteins. J. Exp. Bot. 51: 1189–1200

    Google Scholar 

  • Hemerly AS, Ferreira P, de Almeida EJ, Van Montagu M, Engler G & Inze D (1993) cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5: 1711–1723

    Google Scholar 

  • Hemerly AS, Ferreira PCG, Van Montagu M & Inze D (1999) Cell cycle control and plant morphogenesis: is there an essential link? Bioessays 21: 29–37

    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

    Google Scholar 

  • Hendriks T, Scheer I, Quillet MC, Randoux B, Delbreil B, Vasseur J & Hilbert JL (1998) A non-symbiotic hemoglobin gene is expressed during somatic embryogenesis in Cichorium. Biochim. Biophys. Acta 1443: 193–197

    Google Scholar 

  • Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. USA 97: 2405–2407

    Google Scholar 

  • Hirt H, Pay A, Györgyey 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 homologous to p34cdc2. Proc. Natl. Acad. Sci. USA 88: 1636–1640

    Google Scholar 

  • Holk A, Kaldenhoff R & Richter G (1996) Regulation of an embryogenic carrot gene (DC 2.15) and identification of its active promoter sites. Plant Mol. Biol. 31: 1153–1161

    Google Scholar 

  • Huang L, Franklin AE & Hoffman NE (1993) Primary structure and characterization of an Arabidopsis thaliana calnexin like protein. J. Biol. Chem. 268: 6560–6566

    Google Scholar 

  • Hulskamp M & Schnittger A (1998) Spatial regulation of trichome formation in Arabidopsis thaliana. Semin. Cell. Dev. Biol. 9: 213–220

    Google Scholar 

  • Huntley R, Healy S, Freeman D, Lavender P, de Jager S, Green wood J, Makker J, Walker E, Jackman M, Xie Q, Bannister AJ, Kouzarides T, Gutierrez C, Doonan JH & Murray JA (1998) The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol. Biol. 37: 155–169

    Google Scholar 

  • Ingram R, Charrier B, Scollan C & Meyer P (1999) Transgenic tobacco plants expressing the Drosophila Polycomb (Pc) chromodomain show developmental alterations: possible role of Pc chromodomain proteins in chromatin-mediated gene regulation in plants. Plant Cell 11: 1047–1060

    Google Scholar 

  • Ingvardsen C & Veierskov B (2001) Ubiquitin and proteasome dependent proteolysis in plants. Physiol. Plant. 112: 451–459

    Google Scholar 

  • Ivanova A, Velcheva M, Denchev P, Atanassov A & Van Onckelen H (1994) Endogenous hormone levels during direct somatic embryogenesis in Medicago falcata. Physiol. Plant. 92: 85–89

    Google Scholar 

  • Jack T (2001a) Plant development going MADS. Plant Mol. Biol. 46: 515–520

    Google Scholar 

  • Jack T (2001b) Relearning our ABCs: new twists on an old model. Trends Plant Sci. 6: 310–316

    Google Scholar 

  • Jackson CL & Casanova JE (2000) Turning on ARF: the Sec7family of guanine–nucleotide-exchange factors. Trends Cell Biol. 10: 60–67

    Google Scholar 

  • Jamet E, Durr A, Parmentier Y, Criqui MC & Fleck J (1990) Is ubiquitin involved in the dedifferentiation of higher plant cells? Cell. Differ. Dev. 29: 37–46

    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

    Google Scholar 

  • Jimenez VM & Bangerth F (2001a) Endogenous hormone concentrations and embryogenic callus development in wheat. Plant Cell Tiss. Org. Cult. 67: 37–46

    Google Scholar 

  • Jimenez VM & Bangerth F (2001b) Endogenous hormone levels in explants and in embryogenic and non-embryogenic cultures of carrot. Physiol. Plant. 111: 389–395

    Google Scholar 

  • Jimenez VM & Bangerth F (2001c) Hormonal status of maize initial explants and of the embryogenic and non-embryogenic callus cultures derived from them as related to morphogenesis in vitro. Plant Sci. 160: 247–257

    Google Scholar 

  • John PC (1996) The plant cell cycle: conserved and unique features in mitotic control. Prog. Cell Cycle Res. 2: 59–72

    Google Scholar 

  • Jurgens G (1992) Pattern formation in the flowering plant embryo. Curr. Opin. Genet. Dev. 2: 567–570

    Google Scholar 

  • Jurgens G (2001) Apical–basal pattern formation in Arabidopsis embryogenesis. EMBO J. 20: 3609–3616

    Google Scholar 

  • Jurgens G, Mayer U, Torres R, Berleth T & Misera S (1991) Genetic analysis of pattern formation in the Arabidopsis embryo. Development Suppl. 1: 27–38

    Google Scholar 

  • Jurgens G, Grebe M & Steinmann T (1997) Establishment of cell polarity during early plant development. Curr. Opin. Cell Biol. 9: 849–852

    Google Scholar 

  • Kairong C, Gengsheng X, Lin Q, Xinmin L & Yafu W(1999) The analysis of differential gene expression in early somatic embryogenesis on Lycium barbarum. Plant Cell Tiss. Org. Cult. 59: 169–174

    Google Scholar 

  • Kamada H, Kobayashi K, Kiyosue T & Harada H (1989) Stress induced somatic embryogenesis in carrot and its application to synthetic seed production. In Vitro Cell Dev. Biol. 25: 1163–116

    Google Scholar 

  • Kamada H, Ishikawa K, Saga H & Harada H (1993) Induction of somatic embryogenesis in carrot by osmotic stress. Plant Tiss. Cult. Lett. 10: 38–44

    Google Scholar 

  • Kitamiya E, Suzuki S, Sano T & Nagata T (2000) Isolation of two genes that were induced upon the initiation of somatic embryogenesis on carrot hypocotyls by high concentrations of 2,4-D. Plant Cell Rep. 19: 551–557

    Google Scholar 

  • Kiyosue T, Takano K, Kamada H & Harada H (1990) Induction of somatic embryogenesis in carrot by heavy metal ions. Can. J. Bot. 68: 2301

    Google Scholar 

  • Knox JP (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int. Rev. Cytol. 171: 79–120

    Google Scholar 

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

    Google Scholar 

  • Koltunow AM, Bicknell RA & Chaudhury AM (1995) Apomixis: Molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiol. 108: 1345–1352

    Google Scholar 

  • Kranz E (1999) In vitro fertilization with isolated single gametes. Methods Mol. Biol. 111: 259–267

    Google Scholar 

  • Kreuger M & van Holst GJ (1993) Arabinogalactan proteins are essential in somatic embryogenesis of Daucus carota L. Planta 189: 243–248

    Google Scholar 

  • Kropf DL, Bisgrove SR & Hable WE (1999) Establishing a growth axis in fucoid algae. Trends Plant Sci. 4: 490–494

    Google Scholar 

  • Kurkdjian A & Guern J (1989) Intracellular pH: measurement and importance in cell activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 277–303

    Google Scholar 

  • Lakshmanan P & Taji A (2000) Somatic embryogenesis in leguminous plants. Plant Biol. 2: 136–148

    Google Scholar 

  • Larkin JC, Marks MD, Nadeau J & Sack F (1997) Epidermal cell fate and patterning in leaves. Plant Cell 9: 1109–1120

    Google Scholar 

  • Leyser O (2001) Auxin signalling: the beginning, the middle and the end. Curr. Opin. Plant Biol. 4: 382–386

    Google Scholar 

  • Lichtenthaler HK (1998) The stress concept in plants: an introduction. Ann. NY Acad. Sci. 851: 187–198

    Google Scholar 

  • Lin X, Hwang GJ & Zimmerman JL (1996) Isolation and characterization of a diverse set of genes from carrot somatic embryos. Plant Physiol. 112: 1365–1374

    Google Scholar 

  • Lloyd AM, Schena M, Walbot V & Davis RW (1994) Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid inducible regulator. Science 266: 436–439

    Google Scholar 

  • Lloyd CW, Lowe SB & Peace GW (1980) The mode of action of 2,4-D in counter acting the elongation of carrot cells grown in culture. J. Cell Sci. 195: 309–312

    Google Scholar 

  • Lo Schiavo F, Giuliano G, deVries SC, Genga A, Bollini R, Pitto L, Cozzani F, Nuti-Ronchi V & Terzi M (1990) A carrot cell variant temperature sensitive for somatic embryogenesis reveals a defect in the glycosylation of extracellular proteins. Mol. Gen. Genet. 223: 385–393

    Google Scholar 

  • Lotan T, Ohto M, Yee KM, 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

    Google Scholar 

  • Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ & Chaudhury AM (1999) Genes controlling fertilization independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 296–301

    Google Scholar 

  • Luo Y & Koop HU (1997) Somatic embryogenesis in cultured immature zygotic embryos and leaf protoplasts of Arabidopsis thaliana ecotypes. Planta 202: 387–396

    Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 127–158

    Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11: 587–600

    Google Scholar 

  • Marty I, Brugidou C, Chartier Y & Meyer Y(1993) Growth related gene expression in Nicotiana tabacum mesophyll protoplasts. Plant J. 4: 265–278

    Google Scholar 

  • Matsue T, Koike S & Uchida I (1993) Microamperometric estimation of photosynthesis inhibition in a single algal protoplast. Biochem. Biophys. Res. Commun. 197: 1283–1287

    Google Scholar 

  • Mayer U & Jurgens G (1998) Pattern formation in plant embryogenesis: a reassessment. Semin. Cell. Dev. Biol. 9: 187–193

    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

    Google Scholar 

  • Meijer M & Murray JA (2001) Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4: 44–49

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Mészáros T, Miskolczi P, Ayaydin F, Pettkó-Szandtner A, Magyar Z, Horváth VG, Bakó L, Fehér A & Dudits D (2000) Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Plant Mol. Biol. 43: 595–605

    Google Scholar 

  • Michalczuk L & Druart P (1999) Indole-3-acetic acid metabolism in hormone-autotrophic, embryogenic callus of Inmil (R) cherry rootstock (Prunus incisa×serrula 'GM 9') and in hormone-dependent, non-embryogenic calli of Prunus incisaserrula and Prunus domestica. Physiol. Plant. 107: 426–432

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Mironov V, De Veylder L, Van Montagu M & Inze D (1999) Cyclin-dependent kinases and cell division in plants – The nexus. Plant Cell 11: 509–521

    Google Scholar 

  • Mordhorst AP, Toonen MAJ & de Vries SC (1997) Plant embryogenesis. Crit. Rev. Plant Sci. 16: 535–576

    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

    Google Scholar 

  • Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12: 3788–3796

    Google Scholar 

  • Mu JH, Lee HS & Kao TH (1994) Characterization of a pollen-expressed receptor like kinase gene of Petunia inflata and the activity of its encoded kinase. Plant Cell 6: 709–721

    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

    Google Scholar 

  • Nishiwaki M, Fujino K, Koda Y, Masuda K & Kikuta Y (2000) Somatic embryogenesis induced by the simple application of abscisic acid to carrot (Daucus carota L.) seedlings in culture. Planta 211: 756–759

    Google Scholar 

  • Nomura K & Komamine A (1985) Identification and isolation of single cells that produce somatic embryos at a high frequency in a carrot cell suspension culture. Plant Physiol. 79: 988–991

    Google Scholar 

  • Nomura K & Komamine A (1995) Physiological and biological aspects of somatic embryogenesis. In: Thorpe TA (ed) In Vitro Embryogenesis in Plants (pp. 249–266). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Ober SS & Pardee AB (1987) Intracellular pH is increased after transformation of Chinese hamster embryo fibroblasts. Proc. Natl. Acad. Sci. USA 84: 2766–2770

    Google Scholar 

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

    Google Scholar 

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

    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

    Google Scholar 

  • Ohad N, Margossian L, Hsu Y, Williams C, Repetti P & Fischer RL (1996) A mutation that allows endosperm development without fertilization. Proc. Natl. Acad. Sci. USA 93: 5319–5324

    Google Scholar 

  • Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB & Fischer RL (1999) Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 11: 407–416

    Google Scholar 

  • Osuga K, Masuda H & Komamine A (1999) Synchronization of somatic embryogenesis at high frequency using carrot suspension cultures: model systems and application in plant develop ment. Methods Cell Sci. 21: 129–140

    Google Scholar 

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

    Google Scholar 

  • Palme K & Gälweiler L (1999) PIN-pointing the molecular basis of auxin transport. Curr. Opin. Plant Biol. 2: 375–381

    Google Scholar 

  • Pasternak T, Miskolczi P, Ayaydin F, Mészáros T, Dudits D & Fehér A (2000) Exogenous auxin and cytokinin dependent activation of CDKs and cell division in leaf protoplast-derived cells of alfalfa. Plant Growth Regul. 32: 129–141

    Google Scholar 

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

    Google Scholar 

  • Pedroso MC & Pais MS (1995) Factors controlling somatic embryogenesis – Cell wall changes as an in vivo marker of embryogenic competence. Plant Cell Tiss. Org. Cult. 43: 147–154

    Google Scholar 

  • Pennell RI, Janniche L, Scofield GN, Booij H, de Vries SC & Roberts K (1992) Identification of a transitional cell state in the developmental pathway to carrot somatic embryogenesis. J. Cell Biol. 119: 1371–1380

    Google Scholar 

  • Pennell RI, Cronk QC, Forsberg LS, Stohr C, Snogerup L, Kjel-lbom P & McCabe PF (1995) Cell-context signalling. Phil. Trans. R. Soc. Lond. Biol. Sci. 350: 87–93

    Google Scholar 

  • Perera IY & Zielinski RE (1992) Structure and expression of the Arabidopsis CaM-3 calmodulin gene. Plant Mol. Biol. 19: 649–664

    Google Scholar 

  • Perry SE, Lehti MD & Fernandez DE (1999) The MADS-domain protein AGAMOUS-like 15 accumulates in embryonic tissues with diverse origins. Plant Physiol. 120: 121–129

    Google Scholar 

  • Pichon O & Desbiez MO (1994) Is cytoplasmic pH involved in the regulation of cell cycle in plants? Physiol. Plant. 92: 261–265

    Google Scholar 

  • Poulsen GB, Frugis G, Albrechtsen M & Mariotti D (1996) Synthesis of extracellular proteins in embryogenic and non-embryogenic cell cultures of alfalfa. Plant Cell Tiss. Org. Cult. 44: 257–260

    Google Scholar 

  • Pu R & Robinson KR (1998) Cytoplasmic calcium gradients and calmodulin in the early development of the fucoid alga Pelvetia compressa. J. Cell Sci. 111: 3197–3207

    Google Scholar 

  • Rajasekaran K, Hein MB, Davis GC, Carnes MG & Vasil IK (1987) Exogenous growth regulators in leaves and tissue cultures of Pennisetum purpureum Schum. J. Plant Physiol. 130: 13–25

    Google Scholar 

  • Ratajczak R (2000) Structure, function and regulation of the plant vacuolar H(+)-translocating ATPase. Biochim. Biophys. Acta 1465: 17–36

    Google Scholar 

  • Reynolds TL (1997) Pollen embryogenesis. Plant Mol. Biol. 33: 1–10

    Google Scholar 

  • Ribnicky DM, Cohen JD, Hu WS & Cooke TJ (2001) An auxin surge following fertilization in carrots: a mechanism for regulating plant totipotency. Planta DOI 10.1007/s004250100639

  • Riou-Khamlichi C, Huntley R, Jacqmard A & Murray JA (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544

    Google Scholar 

  • Robinson KR & Miller BJ (1997) The coupling of cyclic GMP and photopolarization of Pelvetia zygotes. Dev. Biol. 187: 125–130

    Google Scholar 

  • Robinson KR, Lorenzi R, Ceccarelli N & Gualtieri P (1998) Retinal identification in Pelvetia fastigiata. Biochem. Biophys. Res. Commun. 243: 776–778

    Google Scholar 

  • Robinson KR, Wozniak M, Pu R & Messerli M (1999) Symmetry breaking in the zygotes of the fucoid algae: controversies and recent progress. Curr. Top. Dev. Biol. 44: 101–125

    Google Scholar 

  • Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, Hwang D & Goldberg AL (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78: 761–771

    Google Scholar 

  • Rogg LE & Bartel B (2001) Auxin Signaling. Derepression through regulated proteolysis. Dev. Cell. 1: 595–604

    Google Scholar 

  • Roitsch T (1999) Source-sink regulation by sugar and stress. Curr. Opin. Plant Biol. 2: 198–206

    Google Scholar 

  • Russell SD (1993) The egg cell: Development and role in fertilization and early embryogenesis. Plant Cell 5: 1349–1359

    Google Scholar 

  • Russinova E, Shao C-Y, Fowler M, Iantcheva A, Atanassov AI, Scott NW, Elliott MC & Slater A (1998) The regulation of gene expression and cell division during direct somatic embryogenesis in alfalfa. (Abstract) 5th Plant EmbryogenesisWorkshop. 19–21 November 1998. Barcelona, Spain

  • Sabala I, Elfstrand M, Farbos I, Clapham D & von Arnold S (2000) Tissue-specific expression of Pa18, a putative lipid transfer protein gene, during embryo development in Norway spruce (Picea abies). Plant Mol. Biol. 42: 461–478

    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

    Google Scholar 

  • Sallandrouze A, Faurobert M, El Maataoui M & Espagnac H (1999) Two-dimensional electrophoretic analysis of proteins associated with somatic embryogenesis development in Cupressus sempervirens L. Electrophoresis 20: 1109–1119

    Google Scholar 

  • Samaj J, Baluska F, Bobak M & Volkmann D (1999) Extracellular matrix surface network of embryogenic units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep. 18: 369–374

    Google Scholar 

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

    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

    Google Scholar 

  • Schaefer J (1985) Regeneration in alfalfa tissue culture. Plant Physiol. 79: 584

    Google Scholar 

  • Schauf CL, Bringle B & Stillwell W (1987) Membrane-directed effects of the plant hormones abscisic acid, indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid. Biochem. Biophys. Res. Commun. 143: 1085–1091

    Google Scholar 

  • Scheres B & Benfey PN (1999) Asymmetric cell division in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 505–537

    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

    Google Scholar 

  • Schnittger A, Schellmann S & Hulskamp M (1999) Plant cells – young at heart? Curr. Opin. Plant Biol. 2: 508–512

    Google Scholar 

  • Schoffl F, Prandl R & Reindl A (1998) Regulation of the heat shock response. Plant Physiol. 117: 1135–1141

    Google Scholar 

  • Schomer M & Epel D (1999) The roles of changes in NADPH and pH during fertilization and artificial activation of the sea urchin egg. Dev. Biol. 216: 394–405

    Google Scholar 

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

    Google Scholar 

  • Servos J, Haase E & Brendel M (1993) Gene SNQ2 of Saccharomyces cerevisiae, which confers resistance to 4-nitroquinoline-N-oxide and other chemicals, encodes a 169 kDa protein homologous to ATP-dependent permeases. Mol. Gen. Genet. 236: 214–218

    Google Scholar 

  • Sharma KK & Thorpe TA (1995) Asexual embryogenesis in vascular plants in nature. In: Thorpe TA (ed) In Vitro Embryogenesis in Plants (pp. 17–72). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell. Mol. Life Sci. 58: 1399–1417

    Google Scholar 

  • Smith DL & Krikorian AD (1990a) pH control of carrot somatic embryogenesis. In: Nijkamp HJJ, Van der Plas LHW & Van Aartrijk J (eds) Progress in Plant Cellular and Molecular Biology (pp. 449–453). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Smith DL & Krikorian AD (1990b) Somatic proembryo production from excised, wounded zygotic carrot embryos on hormone-free medium: evaluation of the effects of pH, ethylene and activated charcoal. Plant Cell Rep. 9:34

    Google Scholar 

  • 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

    Google Scholar 

  • Song J, Sorensen EL & Liang GH (1990) Direct embryogenesis from single mesophyll protoplasts in alfalfa (Medicago sativa L.). Plant Cell Rep. 9: 21–25

    Google Scholar 

  • Souter M & Lindsey K (2000) Polarity and signalling in plant embryogenesis. J. Exp. Bot. 51: 971–983

    Google Scholar 

  • Stals H & Inze D (2001) When plant cells decide to divide. Trends Plant Sci. 6: 359–364

    Google Scholar 

  • Steenhoudt O & Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev. 24: 487–506

    Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K & Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286: 316–318

    Google Scholar 

  • Sterk P, Booij H, Schellekens GA, van Kammen A & de Vries SC (1991) Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3: 907–921

    Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB & Harada JJ (2001) LEAFY COTYLEDON2encodes a B3 domain transcription factor that induces embryo development. Proc. Natl. Acad. Sci. USA 98: 11806–11811

    Google Scholar 

  • Stricker SA (1999) Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211: 157–176

    Google Scholar 

  • Studzinski GP & Harrison LE (1999) Differentiation-related changes in the cell cycle traverse. Int. Rev. Cytol. 189: 1–58

    Google Scholar 

  • Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci. 5: 537–542

    Google Scholar 

  • Swann K & Whitaker MJ (1990) Second messengers at fertilization in sea-urchin eggs. J. Reprod. Fertil. Suppl. 42: 141–153

    Google Scholar 

  • Sylvester AW(2000) Division decisions and the spatial regulation of cytokinesis. Curr. Opin. Plant Biol. 3: 58–66

    Google Scholar 

  • Takahashi Y, Ishida S & Nagata T (1994) Function and modulation of expression of auxin-regulated genes. Int. Rev. Cytol. 152: 109–144

    Google Scholar 

  • Taylor RL (1967) The foliar embryos of Malaxis paludosa. Can. J. Bot. 45: 1553–1556

    Google Scholar 

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

    Google Scholar 

  • Thomas C, Bronner R, Molinier J, Prinsen E, Van Onckelen H & Hahne G (2002) Immuno-cytochemical localization of indole-3-acetic acid during induction of somatic embryogenesis in cultured sunflower embryos. Planta 215: 577–583

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Toonen MAJ, Schmidt EDL, Hendriks T, Verhoeven HA, van Kammen A & deVries SC (1996) Expression of the JIM8 cell wall epitope in carrot somatic embryogenesis. Planta 200: 167–173

    Google Scholar 

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

    Google Scholar 

  • Toonen MAJ, Schmidt EDL, van Kammen A & deVries SC (1997b) Promotive and inhibitory effects of diverse arabinogalactan proteins on Daucus carota L. somatic embryogenesis. Planta 203: 188–195

    Google Scholar 

  • Torres-Ruiz RA & Jurgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120: 2967–2978

    Google Scholar 

  • Touraev A, Pfosser M, Vicente O & HeberleBors E (1996) Stress as the major signal controlling the developmental fate of tobacco microspores: Towards a unified model of induction of microspore/ pollen embryogenesis. Planta 200: 144–152

    Google Scholar 

  • Udvardy A (1996) The role of controlled proteolysis in cell–cycle regulation. Eur. J. Biochem. 240: 307–313

    Google Scholar 

  • Vallee N (1997) Role Des Protons, Du Calcium Et Des Canaux Ioniques Dans La Division Des Protoplastes De Tournesol (Helianthus annuus L.)., PhD Thesis, L'Institute National Polytechnique de Toulouse, Toulouse, France

    Google Scholar 

  • van den Berg C, Willemsen V, Hendriks G, Weisbeek P & Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390: 287–289

    Google Scholar 

  • van den Berg C, Weisbeek P & Scheres B (1998) Cell fate and cell differentiation status in the Arabidopsis root. Planta 205: 483–491

    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. 125: 1880–1890

    Google Scholar 

  • Varga-Weisz PD & Becker PB (1998) Chromatin-remodeling factors: machines that regulate? Curr. Opin. Cell Biol. 10: 346–353

    Google Scholar 

  • Vernet T, Fleck J, Durr A, Fritsch C, Pinck M & Hirth L (1982) Expression of the gene coding for the small subunit for ribulose biphosphate carboxylase during differentiation of tobacco plant protoplasts. Eur. J. Biochem. 126: 489–494

    Google Scholar 

  • Vroemen CW, Langeveld S, Mayer U, Ripper G, Jurgens G, Van Kammen A & de Vries SC (1996) Pattern formation in the arabidopsis embryo revealed by position-specific lipid transfer protein gene expression. Plant Cell 8: 783–791

    Google Scholar 

  • Vroemen C, de Vries S & Quatrano R (1999) Signalling in plant embryos during the establishment of the polar axis. Semin. Cell Dev. Biol. 10: 157–164

    Google Scholar 

  • Walbot V (1996) Sources and consequences of phenotypic and genotypic plasticity in flowering plants. Trends Plant Sci. 1: 27–32

    Google Scholar 

  • Walker L & Estelle M (1998) Molecular mechanisms of auxin action. Curr. Opin. Plant Biol. 1: 434–439

    Google Scholar 

  • Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL & Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15: 501–510

    Google Scholar 

  • Warren GS (1980) A decrease in intercellular space accompanies auxin-induced abortion in somatic carrot embryos. Biochem. Soc. Trans. 8: 627–628

    Google Scholar 

  • Wei YD, Zheng HG & Hall JC (2000) Role of auxinic herbicide-induced ethylene on hypocotyl elongation and root / hypocotyl radial expansion. Pest. Manage. Sci. 56: 377–387

    Google Scholar 

  • Whitaker MJ (1990) Cell cycle control proteins are second messenger targets at fertilization in sea urchin eggs. J. Reprod. Fertil. Suppl. 42: 199–204

    Google Scholar 

  • Wink M (1993) The plant vacuole: a multifunctional compartment. J. Exp. Bot. 44: 231–246

    Google Scholar 

  • Xu N & Bewley JD (1992) Contrasting pattern of somatic and zygotic embryo development in alfalfa (Medicago sativa L.) as revealed by scanning electron microscopy. Plant Cell Rep. 11: 279–284

    Google Scholar 

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

    Google Scholar 

  • Yang WC, de Blank C, Meskiene I, Hirt H, Bakker J, van Kammen A, Franssen H & Bisseling T (1994) Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6: 1415–1426

    Google Scholar 

  • Yarbrough JA (1932) Anatomical and developmental studies of the foliarembryos of Bryophyllum calcynum. Am. J. Bot. 19: 443–453

    Google Scholar 

  • Yasuda H, Nakajima M, Ito T, Ohwada T & Masuda H (2001) Partial characterization of genes whose transcripts accumulate preferentially in cell clusters at the earliest stage of carrot somatic embryogenesis. Plant Mol. Biol. 45: 705–712

    Google Scholar 

  • Yeung EC (1995) Structural and developmental patterns in somatic embryogenesis. In: Thorpe TA (ed) In Vitro Embryogenesis in Plants (pp. 205–248). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Yu HJ, Moon MS, Lee HS, Mun JH, Kwon YM & Kim SG (1999) Analysis of cDNAs expressed during first cell division of petunia petal protoplast cultures using expressed sequence tags. Mol. Cell. 9: 258–264

    Google Scholar 

  • Zhao J, Morozova N, Williams L, Libs L, Avivi Y & Grafi G (2001) Two phases of chromatin decondensation during dedifferentiation of plant cells: distinction between competence for cell fate switch and a commitment for S-phase. J. Biol. Chem. 276: 22772–22778

    Google Scholar 

  • Zimmerman JL (1993) Somatic embryogenesis. Plant Cell 5: 1411–1423

    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

    Google Scholar 

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Fehér, A., Pasternak, T.P. & Dudits, D. Transition of somatic plant cells to an embryogenic state. Plant Cell, Tissue and Organ Culture 74, 201–228 (2003). https://doi.org/10.1023/A:1024033216561

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