REGULATION OF SOMATIC EMBRYOGENESIS IN CROPS: A REVIEW

Article Id: ARCC242 | Page : 1-20
Citation :- REGULATION OF SOMATIC EMBRYOGENESIS IN CROPS: A REVIEW.Agricultural Reviews.2013.(34):1-20
Rohit Joshi and Paramod Kumar
Address : Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi- 110 012, India

Abstract

Somatic embryogenesis’ is a process whereby somatic cells differentiate into somatic embryos. It is regulated by several factors, including phytohormones, proteins, transcription factors, and other related substances during different stages of development. Somatic cells are not terminally differentiated and therefore regain totipotency to initiate embryo development. Although this phenomenon is well known, the detail mechanism of how hormones specify cell fate during in vitro organogenesis is still mysterious. To uncover this mechanism, several studies have been done using biochemical, biological and molecular approaches with embryo-defective mutants or somatic embryogenesis. Recent progress in plant molecular and developmental biology now allows us to establish new pathways for the transition of somatic cells to the embryogenic state. Hormone signaling plays an important role in the cell differentiation during different stages of embryogenesis. During somatic embryo induction, there is differential gene expression resulting in synthesis of new mRNAs and proteins. An array of genes activated or differentially expressed during somatic embryogenesis have been isolated. Few transcription factors have been identified from embryo-defective mutants and some regulatory factors (phenolic compounds and peptidyl growth factors) were detected from culture medium during somatic embryogenesis. In future, research on characterization of development-specific genes during somatic embryogenesis may elucidate a deeper insight in understanding the mechanisms involved during differentiation of somatic cells and phenotypic expression. This review summarizes current understanding of the cellular and molecular aspects of SE and various regulating factors affecting it.

Keywords

Somatic embryogenesis Protein regulation Gene expresssion.

References

  1. Aleith, F. and Richter, G. (1990). Gene expression during induction of somatic embryogenesis in carrot cell suspensions. Planta 183: 17–24.
  2. Ammirato, P.V. (1983). Embryogenesis. In: Evans, D.A., Sharp, W.R., Ammirato, P.V. and Yamada, Y. (Eds.). Hand Book of Plant Cell Culture. Vol. 1- techniques for propagation and breeding. Macmillan Publishing Company, New York.
  3. Bagani, N. and Fracassini, S. (1985). Involvement of Polyamines in the mechanism of Break of dormancy in Helianthus tuberrosus. Bull. Soc. Bot. France 132: 119-125.
  4. Bais, H.P. and Ravishanker, C.A. (2002). Role of polymines in the ontogeny of plants and their biotechnological applications. Plant Cell Tiss. Org. Cult. 69: 1-34.
  5. Baldwin, T.C., Domingo, C., Schindler, T., Seetharaman, G., Stacey, N. and Roberts, K. (2001). DcAGP1, a secreted arabinogalactan protein, is related to a family of basic proline-rich proteins. Plant Mol. Biol. 45: 425–435.
  6. Balestrazzi, A., Toscano, I., Bernacchia, G., Luo, M.Z., Otte, S. and Carbonera, D. (1996).
  7. Cloning of a cdna-encoding dna topoisomerase-I in Daucus carota and expression analysis in relation to cell- proliferation. Gene. 183: 183–190.
  8. Balestrazzi, A., Bernacchia, G., Pitto, L., Luccarini, G. and Carbonera, D. (2001). Spatial expression of DNA topoisomerase I genes during cell proliferation in Daucus carota. Eur. J. Histochem. 45: 31–38.
  9. Bassuner, B.M., Lam, R., Lukowitz, W. and Yeung, E.C. (2006). Auxin and root initiation in somatic embryos of Arabidopsis. Plant Cell Rep. 26: 1-11.
  10. Baudino, S., Hansen, S., Brettschneider, R., Hecht, V.F., Dresselhaus, T., Lorz, H., Dumas, C. and Rogowsky, P.M. (2001). Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta 213: 1-10.
  11. Baumbusch, L.O. (2006). Genetic control of plant embryogenesis and embryo dormancy in Arabidopsis. In: Teixeira da Silva JA (Ed) Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues (1st Edn, Vol I), Global Science Books, London. Pp 417-428.
  12. Baurle, I., Smith, L., Baulcombe, D.C. and Dean, C. (2007). Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318: 109–112.
  13. Bender, J. (2004). DNA methylation and epigenetics. Annu. Rev. Plant Biol. 55: 41–68.
  14. Blilou, I., Xu, J., Wildwate, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palm, K. and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis root. Nature 433: 39-44.
  15. Boyer, C., Hilbert, J.L. and Vasseur, J. (1993). Embryogenesis related protein synthesis and accumulation during early acquisition for somatic embryogenesis competence in Cichorium. Plant Sci. 93: 41–53.
  16. Bozhkov, P. and Von Arnold, S. (1998). Polyethylene glycol promotes maturation but inhibits further development of Picea abies somatic embryos. Physiol. Plant. 104: 211-224.
  17. Braybrook, S.A., Stone, S.L., Park, S., Bui, A.Q., Lee, B.H., Fischer, R.L., Goldberg, R.B. and Harada, J.J. (2006). Genes directly regulated by LEAFY COTYLEDON 2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc. Natl. Acad. Sci. USA 103: 3468–3473.
  18. Brocard-Gifford, I.M., Lynch, T.J. and Finkelstein, R.R. (2003). Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol. 131: 78-92.
  19. Busk, P.K. and Pages, M. (1998). Regulation of abscisic acid-induced transcription. Plant Mol. Biol. 37: 425–435.
  20. Chapman, A., Blervacq, A.S., Hendriks, T., Slomianny, C., Vasseur, J. and Hilbert, J.L. (2000). Cell wall differentiation during early somatic embryogenesis in plants. II. Ultrastructural study and pectin immunolocalization on chicory embryos. Can. J. Bot. 78: 824-831.
  21. Chawla, H.S. (2002). Introduction to Plant Biotechnology 2nd edition. Science Publishers, Inc. 383-386.
  22. Chen, C.G., Pu, Z.Y., Moritz, R.L., Simpson, R.J., Bacic, A., Clarke, A.E. and Mau, S.L. (1994). Molecular cloning of a gene encoding an arabinogalactan-protein from pear (Pyrus communis) cell suspension culture. Proc. Natl. Acad. Sci. USA 92: 10305–10309.
  23. Cheng, J.C., Seeley, K.A., Goupil, P. and Sung, Z.R. (1996). Expression of DC8 is associated with, but not dependent on embryogenesis. Plant Mol. Biol. 31: 127–141.
  24. Chi, G.I., Lin, W.S., Lee, J.E.E. and Pua, E.C. (1994). Role of polyamines on de novo shoot morphogenesis from cotyledons of Brassica campestris spp. Perkinensis (Lour.) Olsson in vitro. Plant Cell Rep. 13: 323-329.
  25. Chug, A. and Khurana, J.P. (2002). Gene expression during somatic embryogenesis-recent advances. Curr. Sci. 83: 715-730.
  26. Chugh, A. and Eudes, F. (2007). Isolated microspore embryogenesis in cereals: aspects and prospects In: Recent Advances in Plant Biotechnology (Edited by Ashwani Kumar & Sudhir K Sopory). IK International Publishing Pvt Ltd, New Delhi, India. pp 205-226.
  27. Corre, F., Henry, Y., Rode, A. and Hartmann, C. (1996). Em gene expression during somatic embryogenesis in the monocot Triticum aestivum L. Plant Sci. 117: 139–149.
  28. Covee, I., Hummel, I., Sulman, C., Gowsbet, G. and Amrani, A.E. (2004). Involvement of polyamines in root development. Plant Cell Tiss. Org. Cult. 76: 1-10.
  29. Darvill, A., Augur, C., Bergmann, C., Carlson, R.W., Cheong, J.J., Eberhard, S., Hahn, M.G., Lo, V.M., Marfa, V., Meyer, B., Mohnen, D., O’Neill, M.A., Spiro, M.D., Van Halbeek, H., York, W.S. and Albetsheim, P. (1992). Oligosaccharins-oligosaccharides that regulate growth, development and defence responses in plants. Glycobiology 2: 181-198.
  30. Daveletova, S., Meszaros, T., Miskolczi, P., Oberschall, A., Torok, K., Magyar, Z., Dudits, D. and Deak, M. (2001). Auxin and heat shock activation of a novel member of the calmodulin like domain protein kinase gene family in cultured alfalfa cells. J. Exp. Bot. 52: 215–221.
  31. De Jong, A.J., Cordewener, J., Lo Schiavo, F., Terzi, M., Vandekerckhove, J., Van Kammen, A. and De Vries, S.C. (1992). A carrot somatic embryo mutant is rescued by chitinase. Plant Cell. 4: 425–433.
  32. De Jong, A.J., Schmidt, E.D.L. and De Vries, S.C. (1993). Early events in higher plant embryogenesis. Plant Mol. Biol. 22: 367-377.
  33. De Klerk, G.J., Arnholdt-Schmitt, B., Lieberei, R. and Neumann, K.H. (1997). Regeneration of roots, shoots and embryos: physiological, biochemical and molecular aspects. Biol. Plant. 39: 53–66.
  34. Debiasi, C., Fraguas, C.B. and Lima, G.P.P. (2007). Study of polyamines in the morphogenesis in vitro of Hemerocallis sp. Ciência Rural 37: 1014-1020.
  35. Dodeman, V.L., Ducreux, G. and Kreis, M. (1997). Zygotic embryogenesis versus somatic embryogenesis. J. Exp. Bot. 48: 1493-1509.
  36. Duditis, D., Gyorgyey, J., Bogre, L. and Bako, L. (1995). Molecular biology of somatic emryogenesis. In Thorpe T.A. (ed.) In vitro embryogenesis in plants. Kluwer Academic Publishers, Dordrecht, Boston, London. pp. 267-308.
  37. Dyachok, J.V., Tobin, A.E., Price, N.P.J. and Von Arnold, S. (2000). Rhizobial Nod factors stimulate somatic embryo development in Picea abies. Plant Cell Rep. 19: 290-297.
  38. Dyachok, J.V., Wiweger, M., Kenne, L. and Von Arnold, S. (2002). Endogenous Nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol. 128: 523-533.
  39. El-Meskaoui, A. and Tremblay, F.M. (2009). Effects of exogenous polyamines and inhibitors of polyamine biosynthesis on endogenous free polyamine contents and the maturation of white spruce somatic embryos. Af. J. Biotech. 8: 6807-6816.
  40. Emons, A.M.C. (1994). Somatic embryogenesis: cell biological aspects. Acta Bot. Neerl. 43: 1-14.
  41. Endress, R. (1994). Plant cell biotechnology. Springer, Berlin, p 353.
  42. Eudes, F., Acharya, S., Laroche, A., Selinger, L.B. and Cheng, K.J. (2003). A novel method to introduce direct somatic embryos, secondary embryogenesis and regeneration of fertile cereal plants. Plant Cell Tiss. Org. Cult. 73: 147-157.
  43. Eun, C.H., Ko, S., Matsubayashi, Y., Sakagami, Y. and Kamada, H. (2003). Phytosulfokine-á requires auxin to stimulate carrot non-embryogenic cell proliferation. Plant Physiol. Biochem. 41: 447-452.
  44. Farooq, M., Wahid, A. and Lee, D.J. (2009). Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol. Plant. 31: 937-945.
  45. Fikelstein, R.R., Tenbarge, K.M. and Shumway, J.E. (1985). Role of ABA in maturation of rapeseed embryos. Plant Physiol. 78: 630-636.
  46. Filonova, L., Bozhkov, P. and Von Arnold, S. (2000). Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking. J. Exp. Bot. 51: 249-264.
  47. Fletcher, L.C., Brand, U., Running, M.P., Simon, R. and Meyerowitz, E.M. (1999). Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 283: 1911-4.
  48. Fos, M., Proono, K., Alabadi, D., Nuez, F., Carbonell, J., Garcia, and Mortinez, J.L. (2003). Polyamines metabolism is ultered in unpollinated parthenocarpic pot-2 tomato ovaries. Plant Physiol. 131: 359-366.
  49. Fransz, P.F., Kieft, H. and Schel, J.H.N. (1990). Cell cycle changes during callus initiation from cultured maize embryos. An autoradiographic study. Acta. Bot. Neerl. 39: 65-73.
  50. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwartz, H., Hamman, T., Offringa, R. and Jürgens, G. (2003). Efflux- dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153.
  51. Fry, S.C. (1995). Polysaccharide-modifying enzymes in the plant cell wall. Annu. Rev. Plant Physiol. Mol. Biol. 46: 497-520.
  52. Gaj, M.D. (2004). Factors influencing somatic embryogenesis induction and plant regeneration with particular reference to Arabidopsis thaliana (L.) Heynh. Plant Growth Reg. 43: 27-47.
  53. Gaj, M.D., Zhang, S.B., Harada, J.J. and Lemaux, P.G. (2005). LEAFY COTYLEDON genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222: 977–988.
  54. Garcia, M.D., Molina, M.C. and Pesqueira, J. (2000). Genotype and embryo age affect plant regeneration from maize/ Tripsacum. Maize Gen. Coop. Newsletters. 74: 41-42.
  55. George, E.F.,Hall, M.A. and Klerk, G.D. (2008). Somatic Embryogenesis. (eds.), Plant Propagation by Tissue Culture. 3rd Edition, Springer. 335–354.
  56. Hadfi, K., Speth, V. and Neuhaus, G. (1998). Auxin-induced developmental patterns in Brassica juncea embryos. Development 125: 879-887.
  57. Hanai, H., Matsuno, T., Yamamoto, M., Matsubayashi, Y., Kobayashi, T., Kamada, H. and 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.
  58. Harmon, A.C., Putnam-Evans, C. and Cormier, M.J. (1986). A calcium-dependent but calmodulin-independent protein kinase from soybean. Plant Physiol. 83: 830–837.
  59. Harper, J.F. (2001). Dissecting calcium oscillators in plant cells. Trends Plant Sci. 6: 395–396.
  60. Hata, S., Kouchi, H., Suzuka, I. and Ishii, T. (1991). Isolation and characterization of cDNA clones for plant cyclins. EMBO J. 10: 2681–2688.
  61. Hatzopoulos, P., Fong, F. and Sung, Z.R. (1990). Abscisic Acid Regulation of DC8, A Carrot Embryonic Gene. Plant Physiol. 94: 690–695.
  62. Hays, D.B., Yeung, E.C. and Pharis, R.P. (2002) The role of gibberellins in embryo axis development. J. Expt. Bot. 53: 1747-1751.
  63. Helleboid, S., Hendriks, T., Bauw, G., Inze, D., Vasseur, J. and Hilbert, J.L. (2000). Three major somatic embryogenesis related proteins in Cichorium identified as PR proteins. J. Exp. Biol. 5: 1189–1120.
  64. Henderson, I.R. and Jacobsen, S.E. (2007). Epigenetic inheritance in plants. Nature 447: 418–424.
  65. Henderson, J.T., Li, H.C., Rider, S.D., Mordhorst, A.P., Romero-Severson, J., Cheng, J.C., Robey, J., Sung, Z.R., de Vries, S.C. and Ogas, J. (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.
  66. Higashi, K., Shiota, H. and Kamada, H. (1998). Patterns of expression of the genes for glutamine synthetase isoforms during somatic and zygotic embryogenesis in carrot. Plant Cell Physiol. 39: 418–424.
  67. Ikeda-Iwai, M., Umehara, M., Satoh, S. and Kamada, H. (2003). Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J. 34: 107-114.
  68. Ipekci, Z. and Gozukirmizi, N. (2003). Direct somatic embryogenesis and synthetic seed production from Paulownia elongate. Plant Cell Rep. 22:16-24.
  69. Jia, X.X., Zhang, J.W., Wang, H.N. and Kong, W.P. (2008). Efficient maize (Zea mays L.) regeneration derived from mature embryos in vitro. Maydica 53: 239-248.
  70. Jones, H.D. (2005). Wheat transformation: current technology and applications to grain development and composition. J. Cereal Sci. 41:137-147.
  71. Joshi, R., Shukla, A. and Kumar, P. (2009). In vitro flowering in hill maize: a novel technique for future. Ind. J. Pl. Physiol. 14: 299-302.
  72. Joshi, R., Shukla, A. and Kumar, P. (2010). Interactive effect of GA3 and polyamines on in vitro somatic embryogenesis from immature embryos in maize (Zea mays L.). Maydica 55: 111-119.
  73. Joshi, R., Shukla, A. and Sairam, R.K. (2011). In vitro screening of rice genotypes for drought tolerance using polyethylene glycol. Acta Physiol. Plant. 33: 2209-2217.
  74. Kader, J.C. (1996). Lipid-transfer proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 627–654.
  75. Kawahara, R., Sunabori, S., Fukuda, H. and Komamine, A. (1992). A gene expressed preferentially in the globular stage of somatic embryogenesis encodes elongation-factor 1á in carrot. Eur. J. Biochem. 209: 157–162.
  76. Keith, K., Kraml, M., Dengler, N.G. and McCourt, P. (1994). Fusca3: A heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6: 589-600.
  77. Kermode, A.R., Dumbroff, E.B. and Bewley, J.D. (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 sensistivity in Ricinus communis L. seeds. J. Exp. Bot. 40: 303-313.
  78. Khan, T., Singh, A.K. and Pant, R.C. (2006). Regeneration via somatic embryogenesis and organogenesis in different cultivars of cotton (Gossypium spp). In Vitro Cell. Dev. Biol. Plant 42: 498–501.
  79. Kielly, G.A. and Bowley, S.R. (1992). Genetic control of somatic embryogenesis in alfalfa. Genome 35: 474-477.
  80. Kikuchi, A., Nobuya, S., Katsumi, H., Tomokazu, K. and Hiroshi, K. (2006). Abscisic acid and stress treatment are essential for the acquisition of embryogenic competence by carrot somatic cells. Planta 223: 637-645.
  81. Kitamiya, E.,Suzuki, S., Sano, T. And 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.
  82. Kiyosue, T., Yamaguchi-Shinozaki, K., Shinozaki, K., Higashi, K., Satoh, S., Kamada, H. and Harada, H. (1992). Isolation and characterization of a cDNA that encodes ECP31, an embryogenic-cell protein from carrot. Plant Mol. Biol. 19: 239–249.
  83. Kiyosue, T., Yamaguchi-Shinozaki, K., Shinozaki, K., Kamada, H. and Harada, H. (1993). cDNA cloning of ECP40, an embryogenic-cell protein in carrot, and its expression during somatic and zygotic embryogenesis. Plant Mol. Biol. 21: 1053–1068.
  84. Kiyosue, T., Shiota, H., Higashi, K., Kamada, H. and Shinozaki, K. (1998). A chromo box gene from carrot (Daucus carota L.): Its cDNA structure and expression during somatic and zygotic embryogenesis. Biochem. Biophys. Acta. 1398: 41–46.
  85. Kobayashi, T., Higashi, K., Sasaki, K., Asami, T., Yoshida, S. and Kamada, H. (2000a). Purification from conditioned medium and chemical identification of a factor that inhibits somatic embryogenesis in carrot. Plant Cell Physiol. 41: 268-273.
  86. Kobayashi, T., Higashi, K. and Kamada, H. (2000b). Inhibitory effects of p-hydroxybenzyl alcohol on somatic embryogenesis in carrot cell culture. Plant Biotech. 17: 87-92
  87. Kobayashi, T., Higashi, K. and Kamada, H. (2001). 4-Hydroxybenzyl alcohol accumulates in suspension-cell cultures and inhibits somatic embryogenesis in carrot. Physiol. Plant. 112: 280-284.
  88. Koltunow, A.M., Hidaka, T. and Robinson, S.P. (1996). Polyembryony in citrus (accumulation of seed storage proteins in seeds and in embryos cultured in vitro. Plant Physiol. 110: 599–609.
  89. Komamine, A., Matsumoto, M., Tsukahara, M., Fujiwara, A., Kawahara, R., Ito, M., Smith, J., Nomura, K. and Fujimura, T. (1990). Mechanisms of somatic embryogenesis in cell cultures - physiology, biochemistry and molecular biology. In Nijkamp H.J.J., Van der Plas L.H.W. & Van Aartrijk J. (eds.) Progress in Plant Cellular and Molecular Biology. Kluwer Academic Publishers, The Netherlands. pp 307-313.
  90. Kreuger, M. and Van Holst, G.J. (1995). Arabinogalactan-protein epitopes in somatic embryogenesis of Daucus carota L. Planta 197: 135–141.
  91. Kreuger, M. and Van Holst, G.J. (1996). Arabinogalactan proteins and plant differentiation. Plant Mol. Biol. 30: 1077-1086.
  92. Kumar, V., Giridhar, P., Chandrashekhar, A. and Ravishankar, G.A. (2008). Polyamines influence morphogenesis and caffeine biosynthesis in in vitro cultures of Coffea canephora P. ex Fr. Acta Physiol. Plant 30: 217-223.
  93. Lara, P., Onate-Sanchez, L., Abraham, Z., Ferrandiz, C., Diaz, I., Carbonero, P. and 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.
  94. Lee, K.W., Choi, G.J., Kim, K.Y., Ji, H.C., Park, H.S., Yoon, S.H. and Lee, S.H. (2009). High frequency plant regeneration from mature seed derived callus of Italian ryegrass (Lolium multiflorum) cultivars. Af. J. Biotech. 8: 6828–6833.
  95. Leyser, O. and Day, S. (2003). Mechanisms in plant development Blackwell publishing.
  96. Li, R., Bruneau, A.H. and Qu R. (2006). Improved plant regeneration and in vitro somatic embryogenesis of St Augustinegrass [Stenotaphrum secundatum (Walt.) Kuntze]. Plant Breed. 125: 52-56.
  97. Litz, R.E. and Gray, D.J. (1995). Somatic embryogenesis for agricultural improvement. World J. Microbiol. Biotechnol. 11: 416-425.
  98. Liu, C.M., Xu, Z.H. and Chua, N.H. (1993). Auxin polar transport is essential for the establishment of bilateral symmetry during plant embryogenesis. Plant Cell 5: 621–630.
  99. Liu, W., Hildebrand, D.F., Grayburn, W.S., Philips, G.C. and Collins, G.B. (1991). Effects of exogenous auxins on expression of lipoxygenases in cultured soybean embryos. Plant Physiol. 97: 969–976.
  100. Liu, W., Hildebrand, D.F., Moore, P.J. and Collins, G.B. (1994). Expression of desiccation-induced and lipoxygenase genes during the transition from the maturation to the germination phases in soybean somatic embryos. Planta 194: 69–74.
  101. Lo Schiavo, F. (1995). Early events in embryogenesis. In Bajaj Y.P.S. (ed.) Biotechnology in Agriculture and Forestry vol 30. Somatic embryogenesis and synthetic seeds, Springer Verlag Berlin, Heidelberg.
  102. Lo Schiavo, F.,Pitto, L., Giuliano, G., Torti, G., Nuti-Ronchi, V., Marazziti, D., Vergara, R., Orselli, S. and Terzi, M. (1989). DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiation, hormones and hypomethylating drugs. Theor. Appl. Genet. 77: 325-331.
  103. Loiseau, J., Michaux-Ferriere, N. and Le Deunff, Y. (1998). Histology of somatic embryogenesis in pea. Plant Physiol. Biochem. 36: 683–687.
  104. Lotan, T., Ohto, M., Yee, K.M., West, M.A., Lo, R., Kwong, R.W., Yamagishi, K., Fischer, R.L., Goldberg, R.B. and Harada, J.J. (1998). Arabidopsis LEAFY COTYLEDON1 is sufficent to induce embryo development in vegetative cells. Cell 93: 1195-1205.
  105. Lowe, K., Abbit, S., Glassman, K., Gregory, C., Hoerster, G., Rasco-Gaunt, S., Sun, X., Lazzeri, P. and Gordon- Kamm, W. (2000). Use of maize Lec1 to improve transformation. In Vitro Cell. Dev. Biol. 36: W15.
  106. Maës, O.C., Chibbar, R.N., Caswell, K., Leung, N. and Kartha, K.K. (1996). Somatic embryogenesis from isolated scutella of wheat: effects of physical, physiological and genetic factors. Plant Sci. 121: 75-84.
  107. Majewska-Sawka, A. and Nothnagel, E.A. (2000). The multiple roles of arabinogalactan proteins in plant development. Plant Physiol. 122: 3-9.
  108. Mathew, M.M. and Philip, V.J. (2003). Somatic embryogenesis versus zygotic embryogenesis in Ensete superbum. Plant Cell Tiss. Org. Cult. 72: 267-275.
  109. Matsubayashi, Y. and 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.
  110. McKersie, B.D. and Brown, D.C.W. (1996). Somatic embryogenesis and artificial seeds in forage legumes. Seed Sci. Res. 6: 109-126.
  111. Meijer, A.H., Scarpella, E., van Dijk, E.L., Qin, L., Taal, A.J.C., Rueb, S., Harrington, S.E., McCouch, S.R., Schilperoort, R.A. and Hoge, J.H.C. (1997). Transcriptional repression by OsHOX-1, a novel homeodomain leucine zipper protein from rice. Plant J. 11: 263–276.
  112. Meneses, A., Flores, D., Muñoz, M., Arrieta, G. and Espinoza, A.M. (2005). Effect of 2,4-D, hydric stress and light on indica rice (Oryza sativa) somatic embryogenesis. Rev. Biol. Trop. 53: 361-368.
  113. Mitsuhashi, W., Toyomasu, T., Masui, H., Katho, T., Nakaminami, K., Kashiwagi, Y., Akutsu, M., Kenmoku, H., Sassa, T., Yamaguchi, S., Kamiya, Y. and Kamada, H. (2003). Gibberellin is essentially required for carrot (Daucus carota L.) somatic embryogenesis: Dynamic regulation of gibberellin 3-oxidase gene expressions. Biosci. Biotech. Biochem. 67: 2438-2447.
  114. Mo´gor, G., Lima, G.P.P. and Mogor, A.F. (2007). Espermidina e espermina exogena na micropropagação de Aloe vera (L.) Burm. Rev. Cubana de Plantas Med. 12: 2.
  115. Mönke, G., Altschmied, L., Tewes, A., Reidt, W., Mock, H.P., Baumlein, H. and Conrad, U. (2004). Seed-specific transcription factors ABI3 and FUS3: molecular interaction with DNA. Planta 219: 158-166.
  116. Nasim, S.A., Mujib, A., Kapoor, R., Fatima, S., Aslam, J. and Mahmooduzzafar (2010). Somatic embryogenesis in Allium sativum L. (cv. Yamuna Safed 3): Improving embryo maturation and germination with PGRs and carbohydrates. Anales de Biol. 32: 1-9.
  117. Nhut, D.T., Hanh, N.T.M., Tuan, P.Q., Nguyet, L.T.M., Tram, N.T.H., Chinh, N.C., Nguyen, N.H. and Vinh, D.N. (2006). Liquid culture as a positive condition of induce and enhance quality and quantity of somatic embryogenesis of Lilium longiflorum. Sci. Hort. 110: 93-97.
  118. Nishiwaki, M., Fujino, K., Koda, Y., Masuda, K. and 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.
  119. Nothnagel, E.A. (1997). Proteoglycans and related components in plant cells. Int. Rev. Cytol. 174: 195–291.
  120. Ogas, J.,Cheng, J.C., Sung, Z.R. and Somerville, C. (1997). Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science. 277: 91-94.
  121. Ogata, Y., Iizuka, M., Nakayama, D., Ikeda, M., Kamada, H. and Koshiba, T. (2005). Possible involvement of abscisic acid in the induction of secondary somatic embryogenesis on seed coat-derived carrot somatic embryos. Planta 221: 417-423.
  122. Okada, K., Ueda, J., Koraaki, M.K., Bell, C.J. and Shimura, Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell. 3: 677-84.
  123. Overvoorde, P.J. and Grimes, H.D. (1994). The role of calcium and calmodulin in carrot somatic embryogenesis. Plant Cell Physiol. 35: 135–144.
  124. Padmanabhan, K., Cantliffe, D.J., Koch, K.E. (2001). Auxin-regulated gene expression and embryogenic competence in callus cultures of sweet potato, Ipomoea batatas (L.) Plant Cell Rep. 20: 187–192.
  125. Paponov, I.A., Teale, W.D., Trebar, M., Blilou, K. and Palme, K. (2005). The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci. 10: 170-7.
  126. Parcy, F., Valon, C., Raynal, M., Gaubier-Comella, P., Delseny, M. and 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.
  127. Paul, A., Mitter, K. and Raychaudhuri, S.S. (2009). Effect of polyamines on in vitro somatic embryogenesis in Momordica charantia L. Plant Cell Tiss. Org. Cult. 97: 303-311.
  128. Pedrosa, L.F. and Vasil, I.K. (1996). Optimisation of somatic embryogenesis and long term regeneration in callus cultures of Diploperennial teosinte (Zea diploperennis Iltis, Doebley and Guzman). Maydica 41: 333-348.
  129. Popelka, J.C., Xu, J. and Altpeter, F. (2003). Generation of rye (Secale cereale L.) plants with low transgene copy number after biolistic gene transfer and production of instantly marker free transgenic rye. Transgen. Res. 12: 587-596.
  130. Raghavan, V. (1997). Somatic embryogenesis. In: Raghavan, V. (ed.): Molecular embryology of flowering plants. Cambridge University Press, Cambridge-New York. Pp. 467–499.
  131. Raghavan, V. (2000). Developmental Biology of Flowering Plants, Springer-Verlag, New York, pp. 309–322.
  132. Rajam, M.V. (1989). Restriction of pollen germination and tube growth in lily pollen by inhibitors of polyamine metabolism. Plant Sci. 59: 53.
  133. Rajam, M.V. (1997). Polyamines. In: M.N.V. Prasad (Ed.), Plant Ecophysiology. John Wiley and Sons, New York. pp. 343-374.
  134. Rao, K.V., Suprasanna, P. and Reddy, G.M. (1990). Biochemical changes in embryogenic and non-embryogenic calli of Zea mays L. Plant Sci. 66: 127-130.
  135. Reid, J.B., Murfet, I.C. and Potts, W.C. (1983). Internode length in Pisum. II. Additional information on the relationship and action of the loci Le, La Cry, Na and Lm. J. Exp. Bot. 34: 349-364.
  136. Rikiishi, K., Matsuura, T., Maekawa, M. and Takeda, K. (2008). Light control of shoot regeneration in callus cultures derived from Barley (Hordeum vulgare L.) immature embryos. Breed. Sci. 58: 129-135.
  137. Roberts, D.M. and Harmon, A.C. (1992). Calcium-modulated proteins: Targets of intracellular calcium signals in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 375–414.
  138. Rose, R.J., Mantiri, F.R., Kurdyukov, S., Chen, S.K., Wang, X.D., Nolan, K.E. and Sheahan, M.B. (2010). Developmental biology of somatic embryogenesis. E C. Pua and M.R. Davey (eds.), Plant developmental biology–biotechnological perspectives: Volume 2, Springer-Verlag Berlin Heidelberg. Pp 3-26.
  139. Rout, G.R., Mohapatra, A. and Jain, S.M. (2006). Tissue culture of ornamental pot plants: a critical review on present scenario and future prospects. Biotech. Adv. 24: 531-560.
  140. Sagare, A.P., Suhasini, K. and Krishnamurthy, K.V. (1995). Histology of somatic embryo initiation and development in chickpea (Cicer arietinum L.). Plant Sci 109: 87-93.
  141. Sahrawat, A.K., Becker, D., Lütticke, S. and Lörz (2003). Genetic improvement of wheat via alien gene transfer, an assessment. Plant Sci. 165: 1147-1168.
  142. Sakhanokho, H.F., Ozias-Akins, P., May, O.I. and Chee, P.W. (2005). Putrescine enhances somatic embryogenesis and plant regeneration in upland cotton. Plant Cell Tiss. Org. Cult. 81: 91-95.
  143. Sato, S.,Toya, T., Kawahara, R., Whittier, R.F., Fukuda, H. and Komamine A. (1995). Isolation of a carrot gene expressed specifically during early-stage somatic embryogenesis. Plant Mol. Biol. 28: 39–42.
  144. Schmidt, E.D.L., Guzzo, F., Toonen, M.A.J. and de Vries, S.C. (1997). A leucine rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Devel. 124: 2049-2062.
  145. Scott, M.P., Tamkun, J.W. and Hartzell, G.W. (1989). The structure and function of the homeodomain. Biochim. Biophys. Acta 989: 25–48.
  146. Shah, K., Schmidt, E.D.L., Vlak, J.M. and de Vries, S.C. (2001). Expression of the Daucus carota somatic embryogenesis receptor kinase (DcSERK) protein in insect cells. Biochemie 83: 415–421.
  147. Sharma, S.K. and Millam, S. (2004). Somatic embryogenesis in Solanum tuberosum: A histological examination of key developmental stages. Plant Cell Rep. 23: 115-119.
  148. Sharma, V.K., Ha¨nsch, R., Mendel, R.R. and Schulze, J. (2005). Mature embryo axis-based high frequency somatic embryogenesis and plant regeneration from multiple cultivars of barley (Hordeum vulgare L.). J. Exp. Bot. 56: 1913–1922.
  149. Shiota, H., Satoh, R., Watabe, K., Harada, H. and 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.
  150. Sinha, N.R., Williams, R.E. and Hake, S. (1993). Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Gene Dev. l7: 787–795.
  151. Smith, D.L. and Kirkorian, A.D. (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.
  152. Somleva, M.N., Schmidt, E.D.L. and De Vries, S.C. (2000). Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression. Plant Cell Rep. 19: 718-726.
  153. Sopory, S.K. and Munshi, M. (1998). Protein kinases and phosphatases and their role in cellular signaling in plants. Crit Rev Plant Sci 17: 245-318.
  154. Stacey, N.J., Roberts, K. and Knox, J.P. (1990). Patterns of expression of the JIM4 arabinogalactan-protein epitope in cell cultures and during somatic embryogenesis in Daucus carota. Planta 180: 285–292.
  155. Steiner, N., Santa-Catarina, C., Silveira, V., Floh, E.I.S. and Guerra, M.P. (2007). Polyamine effects on growth and endogenous hormones levels in Araucaria angustifolia embryogenic cultures. Plant Cell Tiss. Org. Cult. 89: 55-62.
  156. Sterk, P., Booij, H., Schellekens, G.A., van Kammen, A. and de Vries, S.C. (1991). Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3:907–921.
  157. Steward, F.C., Mapes, M.O. and Hears, K. (1958). Growth and organized development of cultured cells. II. Growth and division of freely suspended cells. Am. J. Bot. 45: 705-708.
  158. Steward, F.C., Mapes, M.O., Kent, A.E. and Holsten, R.D. (1964). Growth and development of cultured plant cells. Science 143: 20-27.
  159. Swain, S.M., Reid, J.B. and Kamiya, Y. (1997). Gibberellins are required for embryo growth and seed development in pea. Plant J. 12: 1329-1338.
  160. Tabaeizadeh, Z. (1998). Drought-induced responses in plant cells. Int. Rev. Cytol. 182: 193–247.
  161. Takeda, T., Hayakawa, F., Oe, K. and Matsuoka, H. (2002). Effects of exogenous polyamine on embryogenic carrot cells. Biochem. Eng. J. 12: 21-28.
  162. Takumi, S. and Shimada, T. (1997). Variation in transformation frequencies among six common wheat cultivars through particle bombardment of scutellar tissues. Genes Genet. Sys. 72: 63-69.
  163. Teixeira-da Silva, J.A. (2006) Floriculture, ornamental and plant biotechnology: Advances and topical issues (1st Edn, Vol II), Global Science Books, London, Pp. 571.
  164. Thakur, J., Tyagi, A.K. and Khurana, J.P. (2001). OsIAA1, an Aux/IAA cDNA from rice, and changes in its expression as influenced by auxin and light. DNA Res. 8: 193–203.
  165. Theologis, A. (1986). Rapid gene regulation by auxin. Annu. Rev. Plant Physiol. 37: 407–438.
  166. Thomas, T.L. (1993). Gene expression during plant embryogenesis and germination: An overview. Plant Cell 5: 1401-1410.
  167. Thomas, W., Hoffmann, F., Potrykus, I. and Wenzel, G. (1976). Protoplast regeneration and stem embryogenesis of haploid androgenic rape. Mol. Gen. Genet. 145: 245-247.
  168. Thompson, H.J.M. and Knox, J.P. (1998). Stage-specific responses of embryogenic carrot cell suspension cultures to arabinogalactan protein-binding â–glucosyl Yariv reagent. Planta. 205: 32–38.
  169. To, A., Valon, C., Savino, G., Guilleminot, J., Devic, M., Giraudat, J. and Parcy, F. (2006). A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18: 1642-1651.
  170. Tokuji, Y. and Kuriyama, K. (2003). Involvement of gibberellin and cytokinin in the formation of embryogenic cell clumps in carrot (Daucus carota). J. Plant Physiol. 160: 133-141.
  171. Toonen, M.A.J., Hendriks, T., Schmidt, E.D.L., Verhoeven, H.A., Van Kammen, A. and De Vries, S.C. (1994). Description of somatic-embryo-forming single cells in carrot suspension cultures employing video cell tracking. Planta 194: 565-572.
  172. Toonen, M.A.J., Schmidt, E.D.L., van Kammen, A. and Devries, S.C. (1997). Promotive and inhibitory effects of diverse arabinogalactan proteins on Daucus carota L. somatic embryogenesis. Planta. 203: 188–195.
  173. Umehara, M. and Kamada, H. (2004). Plant growth substances regulating embryogenesis and its physiological properties in seed plants. Reg. Plant Growth Dev. 39: 42-49.
  174. Umehara, M., Ogita, S., Sasamoto, H., Koshino, H., Asami, T., Fujioka, S., Yoshida, S. and Kamada, H. (2005a). Identification of a novel factor, vanillyl benzyl ether, which inhibits somatic embryogenesis of Japanese larch (Larix leptolepis Gordon). Plant Cell Physiol. 46: 445-453.
  175. Umehara, M., Ogita, S., Sasamoto, H., Koshino, H., Nakamura, T., Asami, T., Yoshida, S. and Kamada, H. (2007). Identification of a factor that complementarily inhibits somatic embryogenesis with vanillyl benzyl ether in Japanese larch. In Vitro Cell. Dev. Biol.-Plant. 43: 203-208.
  176. Van Engelen, F.A., De Jong, A.J., Meijer, E.A., Kuil, C.W., Meyboom, K., Dirkse, W.G., Booij, H., Hartog, M.V., Vandekerckhove, J. and De Vries, S.C. (1995). Purification, immunological characterization and cDNA cloning of a 47kDa glycoprotein secreted by carrot suspension cells. Plant Mol. Biol. 27: 901–910.
  177. Vasil, I.K. (1987). Developing cell and tissue culture systems for the improvement of cereal and grass crops. J. Plant Physiol. 128: 193-218.
  178. Viu, A.F.M., Viu, M.A.O., Tavares, A.R., Vianello, F. and Lima, G.P.P. (2009). Endogenous and exogenous polyamines in the organogenesis in Curcuma longa L. Sci. Hort. 121: 501-504.
  179. Walker, J.C. and Key, J.L. (1982). Isolation of cloned cDNAs to auxin-responsive poly(A)+RNAs of elongating soybean hypocotyls. Proc. Natl. Acad. Sci. USA 79: 7185–7189.
  180. Wang, H., Caruso, L.V., Downie, A.B. and Perry, S.E. (2004). The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding and enzyme involved in gibberellin metabolism. Plant Cell 16: 1206-1219.
  181. West, M.A.L.W., Yee, K.M., Danao, J., Zimmerman, J.L., Fischer, R.L., Goldberg, R.B. and Harada, J.J. (1994). LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6: 1731-1745.
  182. Williats, W.G.T. and Knox, J.P. (1996). A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of ß-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J. 9: 919–925.
  183. Wurtele, E.S., Wang, H., Durgerian, S., Nikolau, B.J. and Ulrich, T.J. (1993). Characterization of a Gene Expressed Early in Somatic Embryogenesis of Daucus carota. Plant Physiol. 102: 303–312.
  184. Yadav, J.S. and Rajam, M.V. (1998). Temporal regulation of somatic embryogenesis by adjusting cellular polyamine content in eggplant. Plant Physiol. 116: 617-625.
  185. Yamamoto, N., Kobayashi, H., Togashi, T., Mori, Y., Kikuchi, K., Kuriyama, K. and Tokuji, Y. (2005). Formation of embryogenic cell clumps from carrot epidermal cells is suppressed by 5-azacytidine, a DNA methylation inhibitor. J. Plant Physiol. 162: 47–54.
  186. Yazawa, K., Takahata, K. and Kamada, H. (2004). Isolation of the gene encoding carrot leafy cotyledon 1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol. Biochem. 42: 215–223.
  187. Yeung, E.C. (1995). Structural and developmental patterns in somatic embryogenesis. In Thorpe T.A. (ed.) In vitro embryogenesis in plants. Kluwer Academic Publishers Dordrecht, Boston, London. pp. 205-247.
  188. Zhao, C.H., Zhang, L.J., Chao, G.E. and Kai, H.U. (2008). Establishment and optimization of the regeneration system of mature embryos of maize (Zea mays L.). Agric. Sci. China 7: 1046-1051.
  189. Zhu, C., Kamada, H., Harada, H., He, M. and Hao, S. (1997). Isolation and characterization of a cDNA encoded an embryogenic cell protein-63 related to embryogenesis from carrot. Acta Bot. Sin. 39: 1091–1098.
  190. Zimmerman, J.L. (1993). Somatic embryogenesis: A model for early development in higher plants. Plant Cell 5: 1411-1423.

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