Skip to main content
SpringerLink
Log in
Book cover

Somatic Embryogenesis pp 51–68Cite as

Comparison of Molecular Mechanisms of Somatic and Zygotic Embryogenesis

  • Chapter
  • First Online:

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 2))

Abstract

Somatic embryogenesis has been used as a model system to understand the mechanisms regulating plant embryogenesis. The morphological and physiological characteristics of somatic embryos are similar to those of zygotic embryos. However, what are the patterns of gene expression during somatic embryogenesis? Here, we review molecular events involved in embryogenesis. Four important transcription factors were isolated from a defective-embryo mutant (LEC1, LEC2, FUS3 and ABI3), and three factors were isolated using deferential screening (SERK, AGL15 and BBM); all are expressed during both somatic and zygotic embryo development. These genes may be important in regulating phytohormone synthesis and phytohormone response during somatic and zygotic embryogenesis. Regulation of embryo-specific LEA gene expression is similar in both somatic and zygotic embryos. Recent research involves examination of new mutants that form embryonic structures.

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

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

    Article  CAS  PubMed  Google Scholar 

  2. 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 Campage MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed  Google Scholar 

  3. Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34:67–75

    Article  CAS  PubMed  Google Scholar 

  4. Brocard-Gifford IM, Lynch TJ, Finkelstein RR (2003) Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol 131:78–92

    Article  CAS  PubMed  Google Scholar 

  5. Curaba J, Moritz T, Blervaque R, Parcy F, Raz V, Herzog M, Vachon G (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol 136:3660–3669

    Article  CAS  PubMed  Google Scholar 

  6. Ezcurra I, Wycliffe P, Nehlin L, Ellerstrom M, Rask L (2000) Transactivation of the Brassica napus napin promoter by ABI3 requires interaction of the conserved B2 and B3 domains of ABI3 with different cis-elements: B2 mediates activation through an ABRE, whereas B3 interacts with an RY/G-box. Plant J 24:57–66

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Franz G, Hatzopoulos P, Jones TJ, Krauss M, Sung ZR (1989) Molecular and genetic analysis of an embryonic gene, DC8, from Daucus carota L. Mol Gen Genet 218:143–151

    Article  CAS  PubMed  Google Scholar 

  9. Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7:373–385

    Article  CAS  PubMed  Google Scholar 

  10. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    Article  CAS  PubMed  Google Scholar 

  11. Guiltinan MJ, Marcotte WR, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 12:267–271

    Article  Google Scholar 

  12. Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-like 15. Plant Physiol 133:653–663

    Article  CAS  PubMed  Google Scholar 

  13. Hattori T, Terada T, Hamasuna S (1995) Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7:913–925

    Article  CAS  PubMed  Google Scholar 

  14. Hecht V, Vielle-Calzada J-P, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Helliwell CA, Chin-Atkins AN, Wilson IW, Chapple R, Dennis ES, Chaudhury A (2001) The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13:2115–2125

    Article  CAS  PubMed  Google Scholar 

  17. Henderson JT, Li H-C, Rider SD, Mordhorst AP, Romero-Severson J, Cheng J-C, Robey J, Sung ZR, de Vries SC (2004) PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134:995–1005

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. Kamada H (1980) Control of in vitro asexual embryogenesis in higher plants. Chem Reg Plants 15:62–78

    CAS  Google Scholar 

  21. Kamada H (1996) Physiological and molecular biological studies on somatic embryogenesis. Chem Reg Plants 31:1–11

    CAS  Google Scholar 

  22. Kiyosue T, Yamaguti-Shinozaki K, Shinozaki K, Higashi K, Satoh S, Kamada H, Harada H (1992) Isolation and characterization of a cDNA that encodes ECP31, an embryogenic-cell protein from carrot. Plant Mol Biol 19:239–249

    Article  CAS  PubMed  Google Scholar 

  23. Kiyosue T, Yamaguti-Shinozaki K, Shinozaki K, Kamada H, Harada H (1993a) cDNA cloning of ECP40, an embryogenic-cell protein in carrot, and its expression during somatic and zygotic embryogenesis. Plant Mol Biol 21:1053–1068

    Google Scholar 

  24. Kiyosue T, Satoh S, Kamada H, Harada H (1993b) Somatic embryogenesis in higher plants. J Plant Res 3:75–82

    Google Scholar 

  25. Ko S, Kamada H (2002) Isolation of carrot basic leucine zipper transcription factor using yeast one-hybrid screening. Plant Mol Biol Rep 20:1–8

    Article  Google Scholar 

  26. Ko S, Thitamadee S, Yang H, Eun C-H, Sage-ono K, Higashi K, Satoh S, Kamada H (2001a) Comparison and characterization of cis-regulatory region in some embryo-specific and ABA-responsive carrot genes, DcECPs. Plant Biotech 18:45–54

    Google Scholar 

  27. Ko S, Eun C-H, Satoh S, Kamada H (2001b) Analysis of cis-regulatory elements in carrot embryo-specific and ABA-responsive gene, DcECP31. Plant Biotech 18:55–60

    Google Scholar 

  28. Kroj T, Savino G, Valon C, Giraudat J, Parcy F (2003) Regulation of storage protein gene expression in Arabidopsis. Development 130:6065–6073

    Article  CAS  PubMed  Google Scholar 

  29. Lara P, Onate-Sanchez L, Abraham Z, Ferrandiz C, Diaz I, Carbonero P, Vicente-Carbajosa J (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278:21003–21011

    Article  CAS  PubMed  Google Scholar 

  30. Lee H, Fisher RL, Goldberg RB, Harada JJ (2003) Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor. Proc Natl Acad Sci USA 18:2152–2156

    Article  Google Scholar 

  31. Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua N-H (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    Article  CAS  PubMed  Google Scholar 

  32. Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fisher RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  34. Marcotte WR, Russell SH, Quatrano RS (1989) Abscisic acid-responsive sequences from the Em gene of wheat. Plant Cell 1:969–976

    Article  CAS  PubMed  Google Scholar 

  35. Mönke G, Altschmied L, Tewes A, Reidt W, Mock H-P, Bäumlein H, Conrad U (2004) Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 219:158–166

    Article  PubMed  CAS  Google Scholar 

  36. 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

    CAS  Google Scholar 

  37. Nakagawa H, Ohmiya K, Hattori T (1996) A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J 9:217–227

    Article  CAS  PubMed  Google Scholar 

  38. Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, Kamiya Y, Naito S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220:412–423

    Article  CAS  PubMed  Google Scholar 

  39. Nantel A, Quatrano R (1996) Characterization of three rice basic/leucine zipper factors, including two inhibitors of EmBP-1 DNA binding activity. J Biol Chem 271:31296–31305

    Article  CAS  PubMed  Google Scholar 

  40. Nogue N, Hocart H, Letham DS, Dennis ES, Chaudhury AM (2000) Cytokinin synthesis is higher in the Arabidopsis amp1 mutant. Plant Growth Reg 32:267–273

    Article  CAS  Google Scholar 

  41. Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  43. 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 23:13839–13844

    Article  Google Scholar 

  44. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: Roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582

    Article  CAS  PubMed  Google Scholar 

  45. Parcy F, Valon C, Kohara A, Misera S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. Raz V, Bergervost JHW, Koornneef M (2001) Sequential steps for development arrest in Arabidopsis seeds. Development 128:243–252

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  49. Rider SD, Henderson JT, Jerome RE, Edenberg HJ, Romero-Severson J, Ogas J (2003) Coordinated repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J 35:33–43

    Article  CAS  Google Scholar 

  50. Rider SD, Hemm MR, Hostetler HA, Li H-C, Chapple C, Ogas J (2004) Metabolic profiling of the Arabidopsis pkl mutant reveals selective derepression of embryonic traits. Planta 219:489–499

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  53. Shiota H, Satoh R, Watabe K, Harada H, Kamada H (1998) C-ABI3, the carrot homologue of the Arabidopsis ABI3, is expressed during both zygotic and somatic embryogenesis and functions in the regulation of embryo-specific ABA-inducible genes. Plant Cell Physiol 39:1184–1193

    CAS  Google Scholar 

  54. Shiota H, Tachikawa K, Watabe K, Kamada H (1999) Successful long-term preservation of abscisic-acid-treated and desiccated carrot somatic embryos. Plant Cell Rep 18:749–753

    Article  CAS  Google Scholar 

  55. 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

    Article  CAS  Google Scholar 

  56. 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

    Article  Google Scholar 

  57. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    Article  CAS  PubMed  Google Scholar 

  58. Suzuki M, Kao C-Y, Cocciolone S, McCarty DR (2001) Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant J 28:409–418

    Article  CAS  PubMed  Google Scholar 

  59. Suzuki M, Ketterling MG, Li Q-B, McCarty DR (2003) Viviparus1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol 132:1664–1677

    Article  CAS  PubMed  Google Scholar 

  60. Takahata K, Takeuchi M, Fujita M, Azuma J, Kamada H, Sato F (2004) Isolation of putative glycoprotein gene from early somatic embryo of carrot and its possible involvement in somatic embryo development. Plant Cell Physiol 45:1658–1668

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  62. Thomas C, Meyer D, Himber C, Steinmetz A (2004) Spatial expression of a sunflower SERK gene during induction of somatic embryogenesis and shoot organogenesis. Plant Physiol Biochem 42:35–42

    Article  CAS  PubMed  Google Scholar 

  63. Tsuchiya Y, Nambara E, Naito S, McCourt P (2004) The FUS3 transcription factor functions through the epidermal regulator TTG1 during embryogenesis in Arabidopsis. Plant J 37:73–81

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  65. Wobus U, Weber H (1999) Seed maturation: genetic programmes and control signals. Curr. Opin. Plant Biol 2:33–38

    CAS  Google Scholar 

  66. Vicient CM, Bies-Etheve N, Delseny M (2000) Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana L. J Exp Bot 51:995–1003

    Article  CAS  PubMed  Google Scholar 

  67. von Recklinghausen IR, Iwanowska A, Kieft H, Mordhorst AP, Schel JHN, van Lammeren AAM (2000) Structure and development of somatic embryos formed in Arabidopsis thaliana pt mutant callus cultures derived from seedlings. Protoplasma 211:217–224

    Article  Google Scholar 

  68. Yang H, Saitou T, Komeda Y, Harada H, Kamada H (1996) Late embryogenesis abundant protein in Arabidopsis thaliana homologous to carrot ECP31. Physiol Plant 98:661–666

    Article  CAS  Google Scholar 

  69. Yang H, Saitou T, Komeda Y, Harada H, Kamada H (1997) Arabidopsis thaliana ECP63 encoding a LEA protein is located in chromosome 4. Gene 184:83–88

    CAS  PubMed  Google Scholar 

  70. Yazawa K, Takahata K, Kamada H (2003) Isolation of the gene that encodes carrot leafy cotyledon 1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol Biochem 42:215–223

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  72. Zhang S, Wong L, Meng L, Lemaux PG (2002) Similarity of expression patterns of knotted1 and ZmLEC1 during somatic and zygotic embryogenesis in maize (Zea mays L.). Planta 215:191–194

    Article  CAS  PubMed  Google Scholar 

  73. Zhou C, Labbe H, Sridha S, Wang L, Tian L, Latoszek-Green M, Yang Z, Brown D, Miki B, Wu K (2004) Expression and function of HD2-type histone deacetylases in Arabidopsis development. Plant J 38:715–724

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  75. Zuo J, Niu Q-W, Frugis G, Chua N-H (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Gene Research Center, Institute of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Miho Ikeda

  2. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Hiroshi Kamada

Authors
  1. Miho Ikeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroshi Kamada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miho Ikeda .

Editor information

A. Mujib Jozef Šamaj

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

Ikeda, M., Kamada, H. Comparison of Molecular Mechanisms of Somatic and Zygotic Embryogenesis. In: Mujib, A., Šamaj, J. (eds) Somatic Embryogenesis. Plant Cell Monographs, vol 2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_027

Download citation

Publish with us

Policies and ethics

Search

Navigation