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Developmental pathways of somatic embryogenesis

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Abstract

Somatic embryogenesis is defined as a process in which a bipolar structure, resembling a zygotic embryo, develops from a non-zygotic cell without vascular connection with the original tissue. Somatic embryos are used for studying regulation of embryo development, but also as a tool for large scale vegetative propagation. Somatic embryogenesis is a multi-step regeneration process starting with formation of proembryogenic masses, followed by somatic embryo formation, maturation, desiccation and plant regeneration. Although great progress has been made in improving the protocols used, it has been revealed that some treatments, coinciding with increased yield of somatic embryos, can cause adverse effects on the embryo quality, thereby impairing germination and ex vitro growth of somatic embryo plants. Accordingly, ex vitro growth of somatic embryo plants is under a cumulative influence of the treatments provided during the in vitro phase. In order to efficiently regulate the formation of plants via somatic embryogenesis it is important to understand how somatic embryos develop and how the development is influenced by different physical and chemical treatments. Such knowledge can be gained through the construction of fate maps representing an adequate number of morphological and molecular markers, specifying critical developmental stages. Based on this fate map, it is possible to make a model of the process. The mechanisms that control cell differentiation during somatic embryogenesis are far from clear. However, secreted, soluble signal molecules play an important role. It has long been observed that conditioned medium from embryogenic cultures can promote embryogenesis. Active components in the conditioned medium include endochitinases, arabinogalactan proteins and lipochitooligosaccharides.

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References

  • Attree SM& Fowke LC (1993) Embryogeny of gymnosperms: Advances in synthetic seed technology of conifers. Plant Cell Tiss. Org. Cult. 35: 1–35

    Google Scholar 

  • Bewley JD& Black M (1994) Seeds: physiology of development and germination. Plenum Press, New York

    Google Scholar 

  • Bowman JL& Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends in Plant Science 3: 110–115

    Google Scholar 

  • Bozhkov P, Filonova L& von Arnold S (1998) Polyethylene glycol promotes maturation but inhibits further development of Picea abies somatic embryos. Physiol. Plant. 104: 211–224

    Google Scholar 

  • Bozhkov P& von Arnold S (2002) A key developmental switch during Norway spruce somatic embryogenesis is induced by withdrawel of growth regulators and associated with cell death and extracellular acidification. Biotechnology and Bioengineering (in press)

  • 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 

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

    Google Scholar 

  • Clark SE, Jacobsen SE, Levin JZ& Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122: 1567–1575

    Google Scholar 

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

    Google Scholar 

  • Clouse SD (2000) Plant development: a role for sterols in embryo-genesis. Curr. Biol. 10: R601–R604

    Google Scholar 

  • Darvill A, Augur C, Bergmann C, Carlson RW, Cheong J-J, Eberhard S, Hahn MG, Lo V-M, Marfa V, Meyer B, Mohnen D, O'Neill MA, Spiro MD, van Halbeek H, York WS& Albersheim P (1992) Oligosaccharins - oligosaccharides that regulate growth, development and defence responses in plants. Glycobiology 2: 181–198

    Google Scholar 

  • Dawe RK& Freeling M (1991) Cell lineage and its consequences in higher plants. Plant J. 1: 3–8

    Google Scholar 

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

    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

    Google Scholar 

  • de Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, Lo Shiavo F, Terzi M, Bisseling T, vanKammen A& de Vries SC (1993) Rhizobium lipo-oligosacharides rescue a Daucus carota somatic embryo variant. Plant Cell 5: 615–620

    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

    Google Scholar 

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

    Google Scholar 

  • Dudits D, Gyorgyey J, Bogre L& Bako L (1995) Molecular biology of somatic embryogenesis. In: Thorpe TA (ed) In Vitro Embryo-genesis in Plants (pp 267–308). Kluwer Academic Publishers, Dordrecht, Boston, London

    Google Scholar 

  • Dure III L (1985) Embryogenesis and gene expression during seed formation. Ox. Surv. Plant Mol. Cell Biol. 2: 179–197

    Google Scholar 

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

    Google Scholar 

  • Dyachok JV, Wiweger M, Kenne L& van Arnold S (2002) Endogenous Nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol. (in press)

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Filonova L, Bozhkov P, Brukhin, V, Daniel G, Zhivotovsky B& von Arnold S (2000b) 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

    Google Scholar 

  • Finkelstein RR, Tenbarge KM& Shumway JE (1985) Role of ABA in maturation of rapeseed embryos. Plant Physiol. 78: 630–636

    Google Scholar 

  • Fischer C& Neuhaus G (1996) Influence of auxin on the establishment of bilateral symmetry in monocots. Plant J. 5: 621–630

    Google Scholar 

  • Fletcher JC, Brand U, Running MP, Simon R& Meyerowitz EM (1999) Signalling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems, Science 283: 1911–1914

    Google Scholar 

  • Fry SC (1995) Polysaccharide-modifying enzymes in the plant-cell wall. Annu. Rev. Plant Physiol. Mol. Biol. 46: 497–520.

    Google Scholar 

  • Gifford EM& Foster AS (1987) Morphology and evolution of vascular plants. Kennedy D& Park RB (eds). WH Freeman&Co, New York

    Google Scholar 

  • Goldberg RB, Barker SJ& Perez-Gran L (1989) Regulation of gene expression during plant embryogenesis. Cell 56: 149–160

    Google Scholar 

  • Goldberg RB, Depaiva G& Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266: 605–614

    Google Scholar 

  • Golds TJ, Babcizinsky J, Rauscher G& Koop H-U (1992) Computer-controlled tracking of single cell development in Nicotiana tabacum L. and Hordeum vulgare L. protoplasts embedded in agarose/alginate films. J. Plant Physiol. 140: 582–587

    Google Scholar 

  • Halperin W (1966) Alternative morphogenic events in cell suspensions. Am. J. Bot. 53: 443–453

    Google Scholar 

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

    Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT& Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signalling. Cell 101: 555–567

    Google Scholar 

  • Högberg K-A, Bozhkov PV, Grönroos R& von Arnold S (2001) Critical factors affecting ex vitro performance of somatic embryo plants of Picea abies. Scand. J. For. Res. 16: 295–304

    Google Scholar 

  • Ingouff M, Farbos I, Lagercrantz U& von Arnold S (2001) PaHBI is an evolutionary conserved HD-GL2 Homeobox gene expressed in the protoderm during Norway spruce embryo development. Genesis 30: 220–230

    Google Scholar 

  • Ingram G, Boisnard-Lorig C, Dumas C& Rogowsky PM (2000) Expression patterns of genes encoding HD-ZipIV homeodo-main proteins define specific domains in maize embryos and meristems. Plant J 22: 401–414

    Google Scholar 

  • Irish VF& Sussex IM (1992) A fate map of the Arabidopsis embryonic shoot apical meristems. Development 115: 745–753

    Google Scholar 

  • Kermode AR, Dumbroff EB& Bewley JD (1989) The role of maturation drying in the transition from seed to germination. VII Effects of partial and complete desiccation on abscisic acid levels and sensitivity in Ricinus communis L. seeds. J. Exp. Bot. 40: 303–313

    Google Scholar 

  • Komamine A, Matsumoto M, Tsukahara M, Fujiwara A, Kawahara R, Ito M, Smith J, Nomura K& Fujimura T (1990) Mechanisms of somatic embryogenesis in cell cultures - physiology, biochemistry and molecular biology. In: Nijkamp HJJ, Van der Plas LHW& Van Aartrijk J (eds) Progress in Plant Cellular and Molecular Biology (pp 307–313). Kluwer Academic Publishers, The Netherlands

    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 

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

    Google Scholar 

  • Kreuger M& van Holst GJ (1996) Arabinogalactan proteins and plant differentiation. Plant Mol. Biol. 30: 1077–1086

    Google Scholar 

  • Kurup S, Jones HD& Holdsworth MJ (2000) Interactions of the developmental regulator ABI1 with proteins identified from developing Arabidopsis seeds. Plant J. 21: 143–155

    Google Scholar 

  • Kutschera U (1994) The current status of the acid-growth hypothesis. New Phytol. 126: 549–569

    Google Scholar 

  • Laux T& Jurgens G (1997) Embryogenesis. A new start in life. Plant Cell 9: 989–1000.

    Google Scholar 

  • Li Z& Thomas TL (1998) PEI1, an embryo-specific finger protein gene required for heart-stage embryo formation in Arabidopsis. The Plant Cell 10: 383–398

    Google Scholar 

  • Lindsey K& Topping JF (1993) Embryogenesis: a question of patterns. J. Exp. Bot. 44: 359–374

    Google Scholar 

  • Litz RE& Gray DJ (1995) Somatic embryogenesis for agricultural improvement. World Journal of Microbiology and Biotechnology 11: 416–425

    Google Scholar 

  • Lo Schiavo F, Pitto L, Giuliano G, Torti G, Nuti-Ronchi V, Marazziti D, Veraga R, Orselli S& Terzi M (1989) DNA methylation of embryogenic carrot cell cultures and its variations as caused by maturation, differentiation, hormones and hypomethylation drugs. Theor. App. Genet. 77: 325

    Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MA, 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 

  • Lu P, Porat R, Nadeau JA& O'Neill SD (1996) Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryogenesis and defines a new class of homeobox genes. Plant Cell 8: 2155–2168

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Mayer U, Torrez-Ruiz RA, Berleth T, Misera S& Jurgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353: 402–407

    Google Scholar 

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

    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 

  • McKersie BD& Brown DCW (1996) Somatic embryogenesis and artificial seeds in forage legumes. Seed Sci. Res. 6: 109–126

    Google Scholar 

  • Meinke DW (1995) Molecular genetics of plant embryogenesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 369–394

    Google Scholar 

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

    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 

  • 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 suspension culture. Plant Physiol. 79: 988–991

    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 development. Plant Mol. Biol. 21: 129–140

    Google Scholar 

  • Parcy F, 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

    Google Scholar 

  • Pollock BM (1969) Imbibition temperature sensitivity of Lima beans controlled by initial seed moisture. Plant Physiol. 44: 907–911

    Google Scholar 

  • Rains DW (1989) Plant tissue and protoplast culture: applications to stress physiology and biochemistry. In: Jones HG, Flowers TJ.& Jones MB (eds) Plants and Stress (pp 181–196). Cambridge University Press. ISBN 0-521-34423-9

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

    Google Scholar 

  • Roberts DR, Sutton BCS& Flinn BS (1990) Synchronous and high frequency germination of interior spruce somatic embryos following partial drying at high relative humidity. Can. J. Bot. 68: 1086–1090

    Google Scholar 

  • 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 

  • 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 

  • Satoh N, Hong S-K, Nishimura A, Matsuoka M, Kitano H& Nagato Y (1999) Initiation of shoot apical meristem in rice: characterization of four SHOOTLESS genes. Development 126: 3629–3636

    Google Scholar 

  • Schoof H, Lenhard M, Haecker A, Mayer KFX, Jurgens G& Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635–644

    Google Scholar 

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

    Google Scholar 

  • Shellhammer J& Meinke DW (1990) Arrested embryos from the bio1 auxotroph Arabidopsis thaliana contain reduced levels of biotin. Plant Physiol. 93: 1162–1167

    Google Scholar 

  • Shevell DE, Leu W-M, Gillmor CS, Xia G, Feldmann KA& Chua N-H (1994) EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77: 1051–1062

    Google Scholar 

  • Singh H (1978) Embryology of gymnosperms. In: Zimmerman W, Carlquist Z, Ozenda P& Wulff HD (eds) Handbuch der Pflanzenanatomie (pp 187–241) Gebrüder Borntraeger, Berlin, Stuttgart

    Google Scholar 

  • Smith DL& Kirkorian AD (1990) 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: 468–470

    Google Scholar 

  • Smith LG, Jackson D& Hake S (1995) Expression of KNOTTED1 marks shoot meristem formation during maize embryogenesis. Dev. Gen. 16: 344–348

    Google Scholar 

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

    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 

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

    Google Scholar 

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

    Google Scholar 

  • Strehlow D& Gilbert W (1993) A fate map for the first cleavage of zebrafish. Nature 361: 351–453

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Thomas TL (1993) Gene expression during plant embryogenesis and germination: An overview. Plant Cell 5: 1401–1410.

    Google Scholar 

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

    Google Scholar 

  • Toonen MAJ, Hendriks T, Schmidth 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. Plants 194: 565–572

    Google Scholar 

  • Toonen MAJ& de Vries SC (1997) Use of video tracking to identify embryogenetic cultured cells. In: Lindsey K (ed) Plant Tissue Culture Manual (pp 1–45). Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Trotochaud AE, Jeong S& Clark SE (2000) CLAVATA3, a multimeric ligand for the CLAVATA1 receptor-kinase. Science 289: 613–617

    Google Scholar 

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

    Google Scholar 

  • Tsukahara M& Komamine A (1997) Separation and analyses of cell types involved in early stages of carrot somatic embryogenesis. Plant Cell Tiss. Org. Cult. 47: 145–151

    Google Scholar 

  • Van Hengel AJ, Guzzo F, Van Kammen A& De Vries SC (1998) Expression pattern of the carrot EP 3 endochitinase genes in suspension cultures and in developing seeds. Plant Physiol. 117: 43–53

    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. 125: 1880–1890

    Google Scholar 

  • Vertuccu CW (1989) The kinetics of seed imbibition: Controlling factors and relevance to seedling vigour. In: Stanwood PC& MacDonald MB (eds) Seed Moisture (pp 93–115). CSSA Special Publication no 14. Crop Science Society of America, Madison, WI. ISBN 0-89118-525-9

    Google Scholar 

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

    Google Scholar 

  • Vielle-Calzada, J-P, Baskar R & Grossniklaus (2000) Delayed activation of the paternal genome during seed development. Nature 404: 91–94

    Google Scholar 

  • Wehmeyer N& Vierling E (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiol. 122: 1099–1108

    Google Scholar 

  • West MAL& Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell 5: 1361–1369

    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 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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von Arnold, S., Sabala, I., Bozhkov, P. et al. Developmental pathways of somatic embryogenesis. Plant Cell, Tissue and Organ Culture 69, 233–249 (2002). https://doi.org/10.1023/A:1015673200621

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