Plant Embryogenesis (Zygotic and Somatic)

Abstract

Zygotic embryogenesis in higher plants describes the developmental period in which the zygote undergoes a series of differentiation events, leading to the formation of a mature embryo. Establishment of the major embryonic organs and shoot and root apical meristems occur though partitioning events along the apical–basal axis, and many of these events are guided by the hormone auxin. Formation of the three embryonic tissue systems occurs along a radial axis perpendicular to the apical–basal axis. The mature zygotic embryo is generally developmentally arrested, metabolically quiescent and enclosed within maternal tissues of the seed. Somatic cells can be induced to divert from their normal fate and develop into embryos in a process termed somatic embryogenesis. Auxin and other plant hormones appear to play critical roles in inducing embryogenic competence. Zygotic and somatic embryogenesis represent parallel developmental programs in which cells acquire embryogenic cell fate and develop into mature embryos.

Key Concepts:

  • Embryo development can be divided into two phases: the morphogenesis phase in which the basic body plan of the embryo is established, and the maturation phase in which the embryo becomes tolerant of desiccation and accumulates storage macromolecules such as lipids, proteins and starch.

  • During its development, the embryo is divided into distinct domains along its apical–basal and radial axes.

  • Plant embryo formation represents a series of partitioning events in which organs and tissues are formed from larger domains.

  • Cell fate within the embryo is largely dependent on the position of the cell within the embryo body.

  • Plant cells are totipotent and have the ability to regenerate a fully differentiated organism.

  • Somatic embryos follow similar developmental patterns to their zygotic counterparts, and they occur naturally or are induced in culture.

  • Establishment of embryogenic competence occurs before the formation of the somatic embryo.

Keywords: apical–basal axis; auxin; meristems; patterning; radial axis; totipotency; zygote

Figure 1.

The ovule and representative stages of embryo development. (a) Ovule, (b) zygote, (c) two‐cell embryo, (d) two‐ or four‐cell embryo proper, (e) octant‐stage embryo, (f) 16‐cell embryo proper, (g) globular‐stage embryo proper, (h) transition‐stage embryo proper, (i) torpedo‐stage embryo proper, (j) bent cotyledon‐stage embryo and (k) mature‐stage embryo. Abbreviations: Ac, apical cell; An, antipodal cells; Ax, axis; Bc, basal cell; Cc, central cell; Ch, chalazal region; Co, cotyledons; Ec, egg cell; Fg, female gametophyte; Fu, funiculus; Gm, ground meristem; Hy, hypophysis; Ii, inner integument; Mi, micropyl region; O’, O’ line; Oi, outer integument; Pc, procambium; Pd, protoderm; Pn, polar nuclei; RAM, root apical meristem; Rc, root cap; SAM, shoot apical meristem; Su, suspensor and Sy, synergid cells.

Figure 2.

Apical–basal embryonic domains. Three embryonic domains, apical, central and basal, can be discerned in the octant‐stage embryo. The apical domain gives rise to the shoot apical meristem and most of the cotyledons. The central domain gives rise to part of the cotyledons, the hypocotyl, the root and most of the root apical meristem. The basal domain gives rise to part of the root apical meristem. Abbreviation: Su, suspensor.

Figure 3.

Auxin flux during early embryo development of Arabidopsis thaliana. From the two‐cell embryo stage to the pre‐globular stage, PIN‐FORMED7 (PIN7, purple) localises to the apical membrane of suspensor cells mediating auxin transport (green arrow) from the suspensor into the embryo proper, where an auxin maximum (blue) is created. By the globular stage, PIN1 and PIN7 localise to the basal membranes and establish apical‐to‐basal auxin flux. The activity of PIN1 localises to the basal membrane of the procambial cells. The activities of these transporters establish an auxin maximum in the hypophysis and the uppermost cells of the suspensor of the globular‐stage embryo (dark blue). The hypophysis then divides asymmetrically to eventually form the quiescent centre of the embryo. Adapted from Jenik et al. with permission of Annual Reviews.

Figure 4.

Radial patterning of embryonic tissues. The three embryonic tissue systems are the protoderm, the ground meristem and the procambium. In the embryonic root, the ground meristem gives rise to the cortex and the endodermis.

close

References

Abe M, Katsumata H, Komeda Y and Takahashi T (2003) Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130(4): 635–643.

Aida M, Beis D, Heidstra R et al. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119(1): 109–120.

Angelovici R, Galili G, Fernie AR and Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends in Plant Science 15(4): 211–218.

Baud S, Guyon V, Kronenberger J et al. (2003) Multifunctional acetyl‐CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant Journal 33(1): 75–86.

Berleth T and Jurgens G (1993) The role of the monopteros gene in organizing the basal body region of the Arabidopsis embryo. Development 118(2): 575–587.

Bewley JD (1997) Seed germination and dormancy. Plant Cell 9(7): 1055–1066.

Boutilier K, Offringa R, Sharma VK et al. (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14(8): 1737–1749.

Braybrook SA and Harada JJ (2008) LECs go crazy in embryo development. Trends in Plant Science 13(12): 624–630.

Breuninger H, Rikirsch E, Hermann M, Ueda M and Laux T (2008) Differential expression of WOX genes mediates apical‐basal axis formation in the Arabidopsis embryo. Developmental Cell 14(6): 867–876.

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

Friml J, Vieten A, Sauer M et al. (2003) Efflux‐dependent auxin gradients establish the apical‐basal axis of Arabidopsis. Nature 426(6963): 147–153.

Gaj MD, Trojanowska A, Ujczak A et al. (2006) Hormone‐response mutants of Arabidopsis thaliana (L.) Heynh. impaired in somatic embryogenesis. Plant Growth Regulation 49(2–3): 183–197.

Gaj MD, Zhang S, Harada JJ and Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222(6): 977–988.

Goldberg RB, de Paiva G and Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266(5185): 605–614.

Haecker A, Gross‐Hardt R, Geiges B et al. (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131(3): 657–668.

Ikeda‐Iwai M, Umehara M, Satoh S and Kamada H (2003) Stress‐induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant Journal 34(1): 107–114.

Jenik PD, Gillmor CS and Lukowitz W (2007) Embryonic patterning in Arabidopsis thaliana. Annual Review of Cell and Developmental Biology 23: 207–236.

Jiang K and Feldman LJ (2005) Regulation of root apical meristem development. Annual Review of Cell and Developmental Biology 21: 485–509.

Jurgens G (2001) Apical‐basal pattern formation in Arabidopsis embryogenesis. EMBO Journal 20(14): 3609–3616.

Kawashima T and Goldberg RB (2010) The suspensor: not just suspending the embryo. Trends in Plant Science 15(1): 23–30.

Kikuchi A, Sanuki N, Higashi K, Koshiba T and Kamada H (2006) Abscisic acid and stress treatment are essential for the acquisition of embryogenic competence by carrot somatic cells. Planta 223(4): 637–645.

Koltunow AM and Grossniklaus U (2003) Apomixi: a developmental perspective. Annual Review of Plant Biology 54(1): 547–574.

Koyama T, Furutani M, Tasaka M and Ohme‐Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary‐specific genes in Arabidopsis. Plant Cell 19(2): 473–484.

Lotan T, Ohto M, Yee KM et al. (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93(7): 1195–1205.

Lu P, Porat R, Nadeau JA and O'Neill SD (1996) Identification of a meristem L1 layer‐specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8(12): 2155–2168.

Maraschin SF, de Priester W, Spaink HP and Wang M (2006) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. Journal of Experimental Botany 56: 1711–1726.

Mayer KFX, Schoof H, Haecker A et al. (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95(6): 805–815.

Mayer U, Torres Ruiz RA, Berleth T, Miséra S and Jürgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353: 402–407.

Mayer UBG and Jurgens G (1993) Apical‐basal patterns formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117: 149–162.

McCabe PF, Valentine TA, Forsberg LS and Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9(12): 2225–2241.

Mordhorst AP, Hartog MV, El Tamer MK, Laux T and de Vries SC (2002) Somatic embryogenesis from Arabidopsis shoot apical meristem mutants. Planta 214(6): 829–836.

Mordhorst AP, Voerman KJ, Hartog MV et al. (1998) Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. Genetics 149(2): 549–563.

Natesh S and Rau MA (1984) The embryo. In: Johri BM (ed.) Embryology, pp. 377–444. Berlin: Springer‐Verlag.

Ogas J, Kaufmann S, Henderson J and Somerville C (1999) PICKLE is a CHD3 chromatin‐remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 96(24): 13839–13844.

Schmidt EDL, Guzzo F, Toonen MAJ and deVries SC (1996) A leucine‐rich repeat containing receptor‐like kinase marks somatic plant cells competent to form embryos. Development 124: 2049–2062.

Steeves TA (1983) The evolution and biological significance of seeds. Canadian Journal of Botany 61: 3550–3560.

Steinmann T, Geldner N, Grebe M et al. (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286(5438): 316–318.

Steward FC, Mapes MO and Mears K (1958) Growth and organized development of cultured cells. I. Growth and division of freely suspended cells. American Journal of Botany 45: 705–708.

Stone SL, Braybrook SA, Paula SL et al. (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proceedings of the National Academy of Sciences of the USA 105(8): 3151–3156.

Stone SL, Kwong LW, Yee KM et al. (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proceedings of the National Academy of Sciences of the USA 98(20): 11806–11811.

Szemenyei H, Hannon M and Long JA (2008) TOPLESS mediates auxin‐dependent transcriptional repression during Arabidopsis embryogenesis. Science 319(5868): 1384–1386.

Vanneste S and Friml J (2009) Auxin: a trigger for change in plant development. Cell 136(6): 1005–1016.

Vroemen CW, Mordhorst AP, Albrecht C, Kwaaitaal MA and de Vries SC (2003) The CUP‐SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15(7): 1563–1577.

Wang H, Caruso LV, Downie AB and Perry SE (2004) The embryo MADS domain protein AGAMOUS‐Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16(5): 1206–1219.

Wang X, Niu QW, Teng C et al. (2009) Overexpression of PGA37/MYB118 and MYB115 promotes vegetative‐to‐embryonic transition in Arabidopsis. Cell Research 19(2): 224–235.

Weijers D, Benkova E, Jager KE et al. (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO Journal 24(10): 1874–1885.

Weijers D and Jurgens G (2005) Auxin and embryo axis formation: the ends in sight? Current Opinion in Plant Biology 8(1): 32–37.

Yang X and Zhang X (2010) Regulation of somatic embryogenesis in higher plants. Critical Reviews in Plant Sciences 29: 36–57.

Zuo J, Niu QW, Frugis G and Chua NH (2002) The WUSCHEL gene promotes vegetative‐to‐embryonic transition in Arabidopsis. Plant Journal 30(3): 349–359.

Further Reading

Capron A, Chatfield S, Provart N and Berleth T (2009) Embryogenesis: pattern formation from a single cell. In: The Arabidopsis Book, pp. 1–28. Rockville, MD: The American Society of Plant Biologists.

De Smet I, Lau S, Mayer U and Jurgens G (2010) Embryogenesis – the humble beginnings of plant life. Plant Journal 61(6): 959–970.

Harada JJ (1997) Seed Maturation and Control of Germination, vol. 4. Dordrecht: Kluwer Academic.

Johri BM (1984) Embryology of Angiosperms. Berlin: Springer‐Verlag.

Kaplan DR and Cooke TJ (1997) Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9(11): 1903–1919.

Moller B and Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harbor Perspectives in Biology 1(5): a001545.

Raghavan V (1997) Molecular Embryology of Flowering Plants. Cambridge: Cambridge University Press.

Santos‐Mendoza M, Dubreucq B, Baud S et al. (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant Journal 54(4): 608–620.

Steeves TA and Sussex IM (1989) Patterns in Plant Development, 2nd edn. Cambridge: Cambridge University Press.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Harada, John J, Belmonte, Mark F, and Kwong, Raymond W(Oct 2010) Plant Embryogenesis (Zygotic and Somatic). In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002042.pub2]