Skip to main content
Log in

Embryo production through somatic embryogenesis can be used to study cell differentiation in plants

  • Review Paper
  • Published:
Plant Cell, Tissue and Organ Culture Aims and scope Submit manuscript

Abstract

Somatic embryogenesis is the process by which somatic cells, under induction conditions, generate embryogenic cells, which go through a series of morphological and biochemical changes that result in the formation of a somatic embryo. Somatic embryogenesis differs from zygotic embryogenesis in that it is observable, its various culture conditions can be controlled, and a lack of material is not a limiting factor for experimentation. These characteristics have converted somatic embryogenesis into a model system for the study of morphological, physiological, molecular and biochemical events occurring during the onset and development of embryogenesis in higher plants; it also has potential biotechnological applications. The focus of this review is on embryo development through somatic embryogenesis and especially the factors affecting cell and embryo differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ammirato PV (1983) Embryogenesis. In: Evans DA, Sharp WR, Ammirato PV, Yamada Y (eds) Handbook of plant cell culture, vol. I. Techniques for propagation and breeding. Macmillan, New York, pp 82–123

    Google Scholar 

  • Ammirato PV (1987) Organizational events during somatic embryogenesis. In: Green CE, Somers DA, Hackett WP, Biesboer DD (eds) Plant biology vol. 3. Plant tissue and cell culture. Alan R. Liss, Co., New York, pp 57–81

    Google Scholar 

  • Bajaj YPS (1995) Somatic embryogenesis and its applications for crop improvement. In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, vol. 30. Somatic embryogenesis and synthetic seed I. Springer-Verlag, Berlin, pp 105–125

    Google Scholar 

  • Baldan B, Guzzo F, Filippini F, Gasparian M, LoSchiavo F, Vitale A, De Vries SC, Mariani P, Terzi M (1997) The secretory nature of the lesion of carrot cell variant ts11, rescuable by endochitinase. Planta 203:381–389

    PubMed  CAS  Google Scholar 

  • Barry-Etienne D, Bertrand B, Schlönvoigt A, Etienne H (2002) The morphological variability within a population of coffee somatic embryos produced in a bioreactor affects the regeneration and the development of plants in the nursery. Plant Cell Tissue Organ Cult 68:153–162

    Google Scholar 

  • Baudino S, Hansen S, Brettschneider R, Hecht VFG, Dresselhaus T, Lörz H, Dumas C, Rogowsky PM (2001) Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta 213:1–10

    PubMed  CAS  Google Scholar 

  • Berger F (1999) Endosperm development. Curr Opin Plant Biol 2:28–32

    PubMed  CAS  Google Scholar 

  • Berger F, Taylor A, Brownlee C (1994) Cell fate determination by the cell wall in early fucus development. Science 263:1421–1423

    PubMed  Google Scholar 

  • Bhojwani SS, Razdan MK (1983) Plant tissue culture: theory and practice. Elsevier, Amsterdam

    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, Van Lookeren-Campagne MM (2002) Ectopic expression of baby boom triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    PubMed  CAS  Google Scholar 

  • Buchheim JA, Colburn SM, Ranch JP (1989) Maturation of soybean somatic embryos and the transition to plantlet growth. Plant Physiol 89:768–775

    PubMed  Google Scholar 

  • Carlberg I, Jonsson L, Bergenstrahle A, Soderhall K (1987) Purification of a trypsin inhibitor secreted by embryogenic carrot cells. Plant Physiol 84:197–290

    PubMed  CAS  Google Scholar 

  • Carlberg I, Söderhäll K, Glimelius K, Eriksson T (1984) Protease activities in non-embryogenic and embryogenic carrot cell strains during callus growth and embryo formation. Physiol. Plant 62:458–464

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Chung W, Pedersen H, Chin C-K (1992) Enhanced somatic embryo production by conditioned media in cell suspension cultures of Daucus carota. Biotechnol Lett 14:837–840

    CAS  Google Scholar 

  • Conger BV, Hanning GE, Gray DJ, McDaniel JK (1983) Direct embryogenesis from mesophyll cells of orchardgrass. Science 221:850–851

    PubMed  Google Scholar 

  • Cordewener J, Booij H, Van der Zandt H, Van Engelen FA, Van Kammen A, De Vries SC (1991) Tunicamycin-inhibited carrot somatic embryogenesis can be restored by secreted cationic peroxidase isoenzymes. Planta 184:478–486

    CAS  Google Scholar 

  • Coutos-Thevenot P, Maes O, Jouenne T, Mauro MC, Boulay M, Deloire A, Guern J (1992) Extracellular protein pattern of grapevine cell suspensions in embryogenic and non-embryogenic situations. Plant Sci 86:137–145

    CAS  Google Scholar 

  • Cuadrado Y, Guerra H, Martín AB, Gallego P, Hita O, Dorado A, Villalobos N (2001) Differences in invertase activity in embryogenic and non-embryogenic calli from Medicago arborea. Plant Cell Tissue Organ Cult 67:145–151

    CAS  Google Scholar 

  • Cvikrová M, Hrubcová M, Eder J, Binarová P (1996) Changes in the levels of endogenous phenolics, aromatic monoamines, phenylalanine ammonia-lyase, peroxidase and auxin oxidase activities during initiation of alfalfa embryogenic and nonembryogenic calli. Plant Physiol Biochem 34:853–861

    Google Scholar 

  • De Jong AJ, Cordewener J, Lo Schiavo F, 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

    PubMed  Google Scholar 

  • De Jong AJ, Hendriks T, Meijer EA, Penning M, Lo Schiavo F, Terzi M, Van Kammen A, De Vries SC (1995) Transient reduction in secreted 32 kD chitinase prevents somatic embryogenesis in the carrot (Daucus carota L.) variant ts11. Devel Genet 16:332–343

    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, David A, David H (2000) A basic chitinase-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 

  • Dos Santos AVP, Machado RD (1989) A scanning electron microscope study of Theobroma cacao somatic embryogenesis. Ann Bot 64:293–296

    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, Vasseur J (1991) Direct somatic embryogenesis in leaves of Cichorium. A histological and SEM study of early stages. Protoplasma 162:120–127

    Google Scholar 

  • Dudits D, Bögre L, Györgyey J (1991) Molecular and cellular approaches to the analysis of plant embryo development from somatic cells in vitro. J Cell Sci 99:473–482

    CAS  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. Kluwer Academic Publishers, Dordrecht, pp 267–308

    Google Scholar 

  • Egertsdotter U, Mo LH, Von Arnold S (1993) Extracellular proteins in embryogenic suspension cultures of Norway spruce (Picea abies). Physiol Plant 88:315–321

    CAS  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 

  • Faure O, Aarrouf J, Nougarede A (1996) Ontogenesis, differentiation and precocious germination in anther-derived somatic embryos of grapevine (Vitis vinifera L.): Proembryogenesis. Ann Bot 78:23–28

    Google Scholar 

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

    Google Scholar 

  • Fernandez S, Michaux-Ferrière N, Coumans M (1999) The embryogenic response of immature embryo cultures of durum wheat (Triticum durum Desf.): histology and improvement by AgNO3. Plant Growth Regul 28:147–155

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fridborg E (1978) The effect of activated charcoal on tissue cultures; adsorption of metabolites inhibiting morphogenesis. Physiol Plant 43:104–106

    CAS  Google Scholar 

  • Gaj MD (2001) Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana. Plant Cell Tissue Organ Cult 64:39–46

    Google Scholar 

  • Galiba G, Yamada Y (1988) A novel method increasing the frequency of somatic embryogenesis in wheat tissue culture by NaCl and KCl supplementation. Plant Cell Rep 7:55–58

    CAS  Google Scholar 

  • Gavish H, Vardi A, Fluhr R (1991) Extracellular proteins and early embryo development in Citrus nucellar cell cultures. Physiol Plant 82:606–616

    CAS  Google Scholar 

  • Gavish H, Vardi A, Fluhr R (1992) Suppression of somatic embryogenesis in Citrus cell cultures by extracellular proteins. Planta 186:511–517

    CAS  Google Scholar 

  • Gill R, Malik KA, Sanago MHM, Saxena PK (1998) Somatic embryogenesis and plant regeneration from seedling cultures of tomato (Lycopersicon esculentum Mill.). J Plant Physiol 147:273–276

    Google Scholar 

  • Giuliano G, Lo Schiavo F, Terzi M (1984) Isolation and developmental characterization of temperature-sensitive carrot cell variants. Theor Appl Genet 67:179–183

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Grotkass C, Lieberei R, Preil W (1995) Polyphenoloxidase-activity and –activation in embryogenic and non-embryogenic suspension cultures of Euphorbia pulcherrima. Plant Cell Rep 14:428–431

    CAS  Google Scholar 

  • Hakman I, Fowke LC, Von Arnold S, Eriksson T (1985) The development of somatic embryos in tissue cultures initiated from immature embryos of Picea abies (Norway Spruce). Plant Sci 38:53–59

    Google Scholar 

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

    Google Scholar 

  • Halperin W, Jensen WA (1967) Ultrastructural changes during growth and embryogenesis in carrot cell cultures. J Ultrastruct Res 18:428–443

    PubMed  CAS  Google Scholar 

  • Hanai H, Matsuno T, Yamamoto M, Matsubayashi Y, Kobayashi T, Kamada H, Sakagami Y (2000) A secreted peptide growth factor, phytosulfokine, acting as a stimulatory factor of carrot somatic embryo formation. Plant Cell Physiol 41:27–32

    PubMed  CAS  Google Scholar 

  • Harada JJ (1999) Signaling in plant embryogenesis. Curr Opin Plant Biol 2:23–27

    PubMed  CAS  Google Scholar 

  • Hatanaka T, Sawabe E, Azuma T, Uchida N, Yasuda T (1995) The role of ethylene in somatic embryogenesis from leaf disks of Coffea canephora. Plant Sci 107:199–204

    CAS  Google Scholar 

  • Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, De Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816

    PubMed  CAS  Google Scholar 

  • Herman EB (1991) Recent advances in plant tissue culture. regeneration, micropropagation and media 1988–1991. Agritech Consultants, Inc., USA

    Google Scholar 

  • Herman EB (1995) Recent advances in plant tissue culture III. Regeneration and micropropagation: techniques, systems and media 1991–1995. Agritech Consultants, USA

    Google Scholar 

  • Higashi K, Daita M, Kobayashi T, Sasaki K, Harada H, Kamada H (1998) Inhibitory conditioning for carrot somatic embryogenesis in high-cell-density cultures. Plant Cell Rep 18:2–6

    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

    PubMed  CAS  Google Scholar 

  • Huang B, Bird S, Kemble R, Simmonds D, Keller W, Mili B (1990) Effects of culture density, conditioned medium and feeder cultures on microspore embryogenesis in Brassica napus L. cv. topas. Plant Cell Rep 8:594–597

    Google Scholar 

  • Hutchinson MJ, Murr D, Krishnaraj S, Senaratna T, Saxena PK (1997) Does ethylene play a role in thidiazuron-regulated somatic embryogenesis of geranium (Pelargonium × Hortorum bailey) hypocotyl cultures? In vitro Cell Dev Biol Plant 33:136–141

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ibaraki Y, Matsushima R, Kurata K (2000) Analysis of morphological changes in carrot somatic embryogenesis by serial observation. Plant Cell Tissue Organ Cult 61:9–14

    Google Scholar 

  • Igasaki T, Akashi N, Ujino-Ihara T, Matsubayashi Y, Sakagami Y, Shinohara K (2003) Phytosulfokine stimulates somatic embryogenesis in Cryptomeria japonica. Plant Cell Physiol 44:1412–1416

    PubMed  CAS  Google Scholar 

  • Ikeda-Iwai M, Satoh S, Kamada H (2002) Establishment of a reproducible tissue culture system for the induction of Arabidopsis somatic embryos. J Exp Bot 53:1575–1580

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Jayasankar S, Bondada BR, Li Z, Gray DJ (2002) A unique morphotype of grapevine somatic embryos exhibits accelerated germination and early plant development. Plant Cell Rep 20:907–911

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kairong KR, Xing GS, Liu XM, Xing GM, Wang YF (1999) Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L. Plant Sci 146:9–16

    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 Plant 25:1163–1166

    Article  Google Scholar 

  • Kato H, Takeuchi M (1963) Morphogenesis in vitro starting from single cells of carrot root. Plant Cell Physiol 4:243–245

    Google Scholar 

  • Kawahara R, Komamine A (1995) Molecular basis of somatic embryogenesis. In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, vol. 30. Somatic embryogenesis and synthetic seed I. Springer-Verlag, Berlin, pp 30–40

    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

    CAS  Google Scholar 

  • Kiyosue T, Takano K, Kamada H, Harada H (1990) Induction of somatic embryogenesis in carrot by heavy metal ions. Can J Bot 68:2301–2303

    CAS  Google Scholar 

  • Kobayashi T, Eun CH, Hanai H, Matsubayashi Y, Sakagami Y, Kamada H (1999) Phytosulphokine-a, a peptidyl plant growth factor, stimulates somatic embryogenesis in carrot. J Exp Bot 50:1123–1128

    CAS  Google Scholar 

  • Kobayashi T, Higashi K, Sasaki K, Asami T, Yoshida S, Kamada H (2000) Purification from conditioned medium and chemical identification of a factor that inhibits somatic embryogenesis in carrot. Plant Cell Physiol 41:268–273

    PubMed  CAS  Google Scholar 

  • Komamine A, Murata N, Nomura K (2005) Mechanisms of somatic embryogenesis in carrot suspension cultures – morphology, physiology, biochemistry, and molecular biology. In vitro Cell Dev Biol Plant 41:6–10

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Krikorian AD, Simola LK (1999) Totipotency, somatic embryogenesis, and Harry Waris (1893–1973). Physiol Plant 105:348–355

    CAS  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    PubMed  CAS  Google Scholar 

  • Lee EK, Cho DY, Soh WY (2001) Enhanced production and germination of somatic embryos by temporary starvation in tissue cultures of Daucus carota. Plant Cell Rep 20:408–415

    CAS  Google Scholar 

  • Leslie CA, Romani RJ (1986) Salicylic acid: a new inhibitor of ethylene biosynthesis. Plant Cell Rep 5:144–146

    CAS  Google Scholar 

  • Letarte J, Simion E, Miner M, Kasha K (2006) Arabinogalactans and arabinogalactan-proteins induce embryogenesis in wheat Triticum aestivum L.) microspore culture. Plant Cell Rep 24:691–698

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Litz RE (1986) Effect of osmotic stress on somatic embryogenesis in Carica suspension cultures. J Am Soc Hortic Sci 111:969–972

    CAS  Google Scholar 

  • Lo Schiavo F, Giuliano G, De Vries 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

    PubMed  Google Scholar 

  • Lopes MA, Larkins BA (1993) Endosperm origin, development, and function. Plant Cell 1383–1399

  • Lorbiecke R, Steffens M, Tomm JM, Scholten S, von Wiegen P, Kranz E, Wienand U, Sauter M (2005) Phytosulphokine gene regulation during maize (Zea mays L.) reproduction. J Exp Bot 56:1805–1819

    PubMed  CAS  Google Scholar 

  • Lotan T, Ohto M, Matsudaira YK, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis leafy cotyledon1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Maës O, Coutos-Thévenot P, Jouenne T, Boulay M, Guern J (1997) Influence of extracellular proteins, proteases and protease inhibitors on grapevine somatic embryogenesis. Plant Cell Tissue Organ Cult 50:97–105

    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 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Maraschin SF, de Priester W, Spaink HP, Wang M (2005) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56:1711–1726

    PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Goto T, Sakagami Y (2004) Chemical nursing: phytosulfokine improves genetic transformation efficiency by promoting the proliferation of surviving cells on selective media. Plant Cell Rep 23:155–158

    PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Ogawa M, Moritam A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, physulfokine. Science 296:1470–1472

    PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93:7623–7627

    PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Yang H, Sakagami Y (2001) Peptide signals and their receptors in higher plants. Trends Plant Sci 6:573–577

    PubMed  CAS  Google Scholar 

  • Matthys-Rochon E (2005) Secreted molecules and their role in embryo formation in plants: a mini-review. Acta Biol Cracov Bot 47:23–29

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Meijer EGM, Brown DCW (1988) Inhibition of somatic embryogenesis in tissue cultures of Medicago sativa by aminoethoxyvinylglycine, amino-oxyacetic acid, 2, 4-dinitrophenol and salicylic acid at concentrations which do not inhibit ethylene biosynthesis and growth. J Exp Bot 39:263–270

    CAS  Google Scholar 

  • Mo LH, Egertsdotter U, Von Arnold S (1996) Secretion of specific extracellular proteins by somatic embryos of Picea abies is dependent on embryo morphology. Ann Bot 77:143–152

    CAS  Google Scholar 

  • Nabors MW, Heyser JW, Dykes TA, DeMott KJ (1983) Long-duration, high-frequency plant regeneration from cereal tissue cultures. Planta 157:385–391

    Google Scholar 

  • Nakamura T, Taniguchi T, Maeda E (1992) Studies on somatic embryogenesis of coffee by scanning electron microscope. Jpn J Crop Sci 61:476–486

    Google Scholar 

  • Nissen P (1994) Stimulation of somatic embryogenesis in carrot by ethylene: effects of modulators of ethylene biosynthesis and action. Physiol Plant 92:397–403

    CAS  Google Scholar 

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

    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

    PubMed  CAS  Google Scholar 

  • Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291

    Article  PubMed  CAS  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 96:13,839–13,844

    CAS  Google Scholar 

  • Oinam GS, Kothari SL (1995) Totipotency of coleoptile tissue in Indica rice (Oryza sativa L. cv. CH 1039). Plant Cell Rep 14:245–248

    CAS  Google Scholar 

  • Osuga K, Kamada H, Komamine A (1993) Cell density is an important factor for synchronization of the late stage of somatic embryogenesis at high frequency. Plant Tissue Cult Lett 10:180–183

    Google Scholar 

  • Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, 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. Plant Physiol 129:1807–1819

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Quiroz-Figueroa FR, Fuentes-Cerda CFJ, Rojas-Herrera R, Loyola-Vargas VM (2002a) Histological studies on the developmental stages and differentiation of two different somatic embryogenesis systems of Coffea arabica. Plant Cell Rep 20:1141–1149

    CAS  Google Scholar 

  • Quiroz-Figueroa FR, Méndez-Zeel M, Larqué-Saavedra A, Loyola-Vargas VM (2001) Picomolar concentrations of salycilates induce cellular growth and enhance somatic embryogenesis in Coffea arabica tissue culture. Plant Cell Rep 20:679–684

    CAS  Google Scholar 

  • Quiroz-Figueroa FR, Méndez-Zeel M, Sánchez-Teyer F, Rojas-Herrera R, Loyola-Vargas VM (2002b) Differential gene expression in embryogenic and non-embryogenic clusters from cell suspension cultures of Coffea arabica L. J Plant Physiol 159:1267–1270

    Google Scholar 

  • Quiroz-Figueroa FR, Rojas-Herrera R, Sánchez-Teyer F, Loyola-Vargas VM (2000) Compuestos excretados por los CTV y su papel en la embriogénesis somática. In: Bernal-Lugo I, Loza H (eds) Simposia académico en honor de la Dra. Estela Sánchez Quintanar, Facultad de Química. UNAM, México, pp 9–19

    Google Scholar 

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

    Google Scholar 

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

    CAS  Google Scholar 

  • Raskin I, Skubatz H, Tang W, Meeusen BJD (1990) Salicylic acid levels in thermogenic and nonthermogenic plants. Ann Bot 66:369–373

    CAS  Google Scholar 

  • Reinert J (1959) Uber die kontrolle der morphogenese und die induktion von adventivembryonen an gewebekulturen aus karotten. Planta 53:318–333

    Google Scholar 

  • Rojas-Herrera R, Quiroz-Figueroa FR, Monforte-González M, Sánchez-Teyer F, Loyola-Vargas VM (2002) Differential gene expression during somatic embryogenesis in Coffea arabica L., revealed by RT-PCR differential display. Mol Biotechnol 21:43–50

    CAS  Google Scholar 

  • Roustan JP, Latche A, Fallot J (1989a) Stimulation of Daucus carota somatic embryogenesis by inhibitors of ethylene synthesis: cobalt and nickel. Plant Cell Rep 8:182–185

    CAS  Google Scholar 

  • Roustan J-P, Latche A, Fallot J (1989b) Effet de l’acide salicylique et de l’acide acétylsalicylique sur la production d’éthylène et l’embryogenèse somatique de suspensions cellulaires de carotte (Daucus carota L.). CR Acad Sci (Paris) Sér III 308:395–399

    CAS  Google Scholar 

  • Russell SD (1992) Doble fertilization. Int Rev Cytol 140:357–388

    Google Scholar 

  • Ryan CA, Pearce G, Scheer J, Moura DS (2002) Polypeptide hormones. Plant Cell 14:S251–S264

    PubMed  CAS  Google Scholar 

  • Samaj J, Baluska F, Bobák 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

    CAS  Google Scholar 

  • Satoh S, Kamada H, Harada H, Fujii T (1986) Auxin-controlled glycoprotein release into the medium of embryogenic carrot cells. Plant Physiol 81:931–933

    Article  PubMed  CAS  Google Scholar 

  • Schiavone FM, Cooke TJ (1985) A geometric analysis of somatic embryo formation in carrot cell culture. Can J Bot 63:1573–1578

    Google Scholar 

  • Schmidt EDL, Guzzo F, Toonen MAJ, De Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062

    PubMed  CAS  Google Scholar 

  • Sharp WR, Söndahl MR, Caldas LS, Maraffa SB (1980) The physiology of in vitro asexual embryogenesis. Horticul Rev 268–310

  • Smith DL, Krikorian AD (1989) Release of somatic embryogenic potential from excised zygotic embryos of carrot and maintenance of proembryonic cultures in hormone-free medium. Am J Bot 76:1832–1843

    PubMed  CAS  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

    CAS  Google Scholar 

  • Stasolla C, Yeung EC (2003) Recent advances in conifer somatic embryogenesis: improving somatic embryo quality. Plant Cell Tissue Organ Cult 74:15–35

    CAS  Google Scholar 

  • Steward FC, Mapes MO, Mears K (1958) Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cells. Am J Bot 45:705–708

    Google Scholar 

  • Stirn S, Jacobsen H-J (1987) Marker proteins for embryogenic differentiation patterns in pea callus. Plant Cell Rep 6:50–54

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Stuart R, Street HE (1969) Studies on the growth in culture of plant cells IV. The initiation of division in suspensions of stationary-phase cells of Acer pseudoplatanus L. J Exp Bot 20:556–571

    Google Scholar 

  • Sundaresan V (2005) Control of seed size in plants. Proc Natl Acad Sci USA 102:17887–17888

    PubMed  CAS  Google Scholar 

  • Tan SK, Kamada H (2000) Initial identification of a phosphoprotein that appears to be involved in the induction of somatic embryogenesis in carrot. Plant Cell Rep 19:739–747

    CAS  Google Scholar 

  • Tchorbadjieva M, Kalmukova R, Pantchev I, Kyurkchiev S (2005) Monoclonal antibody against a cell wall marker protein for embryogenic potential of Dactylis glomerata L. suspension cultures. Planta 222:811–819

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

  • Tsukahara M, Komamine A (1997) Separation and analysis of cell types involved in early stages of carrot somatic embryogenesis. Plant Cell Tissue Organ Cult 47:145–151

    Google Scholar 

  • Umehara M, Ogita S, Sasamoto H, Koshino H, Asami T, Fujioka S, Yoshida S, Kamada H (2005) Identification of a novel factor, vanillyl benzyl ether, which inhibits somatic embryogenesis of Japanese larch (Larix leptolepis Gordon). Plant Cell Physiol 46:445–453

    PubMed  CAS  Google Scholar 

  • Van Engelen FA, De Vries SC (1992) Extracellular proteins in plant embryogenesis. Trends Genet 8:66–70

    PubMed  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

    PubMed  Google Scholar 

  • Van Hengel AJ, Van Kammen A, De Vries SC (2002) A relationship between seed development, arabinogalactan-proteins (AGP) and the AGP mediated promotion of somatic embryogenesis. Physiol Plant 114:637–644

    PubMed  Google Scholar 

  • Verdus M-C, Dubois T, Dubois J, Vasseur J (1993) Ultrastructural changes in leaves of Cichorium during somatic embryogenesis. Ann Bot 72:375–383

    Google Scholar 

  • Waris H (1957) A striking morphogenetic effect of amino acid in seed plant. Suom Kemistil 36B:121

    Google Scholar 

  • Warren GS, Fowler MW (1981) Physiological interactions during the initial stages of embryogenesis in cultures of Daucus carota L. New Phytol 87:481–486

    Google Scholar 

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

    PubMed  Google Scholar 

  • Wetherell DF (1984) Enhanced adventive embryogenesis resulting from plasmolysis of cultured wild carrot cells. Plant Cell Tissue Organ Cult 5:221–227

    Google Scholar 

  • Wilde HD, Nelson WS, Booij H, De Vries SC, Thomas TL (1988) Gene-expression programs in embryogenic and non-embryogenic carrot cultures. Planta 176:205–211

    CAS  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 

  • Yang HP, Matsubayashi Y, Hanai H, Sakagami Y (2000) Phytosulfokine-a, a peptide growth factor found in higher plants: its structure, functions, precursor and receptors. Plant Cell Physiol 41:825–830

    PubMed  CAS  Google Scholar 

  • Yeung EC (1995) Structural and development patterns in somatic embryogenesis. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer Academic Publishers, Netherlands, pp 205–247

    Google Scholar 

  • Yeung EC (1999) The use of histology in the study of plant tissue culture systems-some practical comments. In Vitro Cell Dev Biol Plant 35:137–143

    Google Scholar 

  • Zheng MY, Weng Y, Konzak CF (2002) The effect of ovary-conditioned medium on microspore embryogenesis in common wheat (Triticum aestivum L.). Plant Cell Rep 20:802–807

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:805–815

    Google Scholar 

Download references

Acknowledgements

The authors thank the help of Emily Wortman-Wunder and Dayakar Badri for the English correction of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Víctor M. Loyola-Vargas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Quiroz-Figueroa, F.R., Rojas-Herrera, R., Galaz-Avalos, R.M. et al. Embryo production through somatic embryogenesis can be used to study cell differentiation in plants. Plant Cell Tiss Organ Cult 86, 285–301 (2006). https://doi.org/10.1007/s11240-006-9139-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-006-9139-6

Keywords

Navigation