Induction of somatic embryogenesis in woody plants

  • Tasiu IsahEmail author


Somatic embryogenesis, the in vitro developmental program by which somatic cells are reprogrammed to undergo cellular and molecular changes that make them competent to produce somatic embryos, has been achieved with many woody plants. The program involves the stages of competence acquisition, induction and expression of the morphogenic pathway by the cultured cells and tissues. The ability to express the program in cultured cells/tissues is regulated by many factors, including genotype, explant type and age and culture conditions. In many woody plants, somatic embryogenesis was achieved with mature, immature explants or both. Juvenile tissues as immature and mature zygotic embryos are regarded best explants to establish embryogenic cultures in woody plants and potential to obtain the cultures decline with increasing maturity of the explant.


Woody plants Trees Explant Zygotic embryo Embryogenic tissue Somatic embryogenesis 



Somatic embryogenesis


Plant growth regulators




Arabino galactan proteins


Primary embryo mass



This work was supported by the agreed financial terms between Department of Biotechnology, Government of India New Delhi and The World Academy of Sciences for the Advancement of Science in Developing Countries (TWAS) Trieste Italy, through DBT—TWAS Postgraduate Research Fellowship. I am highly grateful to Hamdard University New Delhi, India, for providing me the research facilities. Sincere appreciations are also extended to the reviews editor Anderz K. Kononowicz and an anonymous reviewer for the critical reading, valuable suggestions, observations and relevant comments on the manuscript. I also express my sincere apologies to those whose relevant literature contribution is not cited in the manuscript due to the wide scope of the topic and limited space available for a manuscript.


  1. Abrahamsson M, Valladares S, Larsson E et al (2012) Patterning during somatic embryogenesis in Scots pine in relation to polar auxin transport and programmed cell death. Plant Cell Tissue Organ Cult 109(3):391–400CrossRefGoogle Scholar
  2. Ahuja MR (1993) Regeneration and germplasm preservation in aspen-Populus. In: Ahuja MR (ed) Micropropagation of woody plants. Kluwer, Dordrecht, pp 187–194CrossRefGoogle Scholar
  3. Akhtar N (1997) Studies on induction of SE and production of artificial seeds for micropropagation of a tropical fruit tree guava (Psidium guajava L.). Unpublished Ph.D. Thesis. Banaras Hindu University, VaranasiGoogle Scholar
  4. Akhtar N (2013) Somatic embryogenesis for efficient micropropagation of guava (Psidium guajava L.). Methods Mol Biol 11013:161–177. doi: 10.1007/978-1-62703-074-8_12 PubMedGoogle Scholar
  5. Altamura MM, Della Rovere F, Fattorini L et al (2015) Recent advances on genetic and physiological bases of in vitro somatic embryo formation. Vitro embryogenesis in higher plants. Springer Science Media, New York, pp 47–85Google Scholar
  6. Amoo SO, Erhinmeyoma AB (2005) Induction of callus and somatic embryogenesis from cotyledon explants of Parkia biglobosa (Jacq.) Benth. Afri. J Biotechnol 4(1):68–71Google Scholar
  7. Anil VS, Rao KS (2000) Calcium-mediated signaling during sandalwood SE: role for exogenous calcium as the second messenger. Plant Physiol 123:1301–1311PubMedPubMedCentralCrossRefGoogle Scholar
  8. Arrillaga I, Tobolski SA, Merkle SA (1994) Advances in SE and plant production of black locust. Plant Cell Rep 13:171–175. doi: 10.1007/BF00239886 PubMedGoogle Scholar
  9. Arroyo-Herrera A, Gonzalez AK, Moo RC et al (2008) Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases SE. Plant Cell Tissue Organ Cult 94:171–180. doi: 10.1007/s11240-008-9401-1 CrossRefGoogle Scholar
  10. Astarita LV, Guerra MP (1998) Early somatic embryogenesis in Araucaria angustifolia–induction and maintenance of embryonal-suspensor mass cultures. Braz J Plant Physiol 10:113–118Google Scholar
  11. Attree SM, Fowke LC (1993) Embryogeny of gymnosperms: advances in synthetic seed technology of conifers. Plant Cell Tissue Organ Cult 35:1–35. doi: 10.1007/BF00043936 CrossRefGoogle Scholar
  12. Attree SM, Budimir S, Fowke LC (1990) SE and plantlet regeneration from cultured shoots and cotyledons of seedlings from stored seeds of black and white spruce (Picea mariana and P. glauca). Can J Bot 68:30–34. doi: 10.1139/b90-005 CrossRefGoogle Scholar
  13. Barra-Jimenez A, Blasco M, Ruiz-Galea M et al (2014) Cloning mature holm oak trees by somatic embryogenesis. Trees 28:657–667. doi: 10.1007/s00468-014-0979-0 CrossRefGoogle Scholar
  14. Becwar MR, Wann SR, Johnson MA et al (1988) Development and characterization of in vitro embryogenic systems in conifers. In: Ahuja MR (ed) Somatic cell genetics of woody plants. Kluwer, Dordrecht, pp 1–18. doi: 10.1007/978-94-009-2811-4_1 CrossRefGoogle Scholar
  15. Becwar MR, Nagmani R, Wann SR (1990) Initiation of embryogenic cultures and somatic embryo development in loblolly pine (Pinus taeda). Can J Forest Res 20:810–817. doi: 10.1139/x90-107 CrossRefGoogle Scholar
  16. Bonga JM (1987) Clonal propagation of mature trees. Problem and possible solution. In: Bonga JM, Durzan DJ (eds) Cell and tissue culture in forestry, forestry science. Springer, Netherlands, pp 249–271. doi: 10.1007/978-94-017-0994-1_15 CrossRefGoogle Scholar
  17. Bonga JM (1996) Frozen storage stimulates formation of embryo-like structures and elongating shoots in explants from mature Larix decidua and L. × eurolepis trees. Plant Cell Tissue Organ Cult 46:91–101. doi: 10.1007/BF00034841 CrossRefGoogle Scholar
  18. Bonga JM (2004) The effect of various culture media on the formation of embryo-like structures in cultures derived from explants taken from mature Larix decidua. Plant Cell Tissue Organ Cult 77:43–48CrossRefGoogle Scholar
  19. Bonga JM, von Aderkas P (1992) In vitro culture of trees. Kluwer Academic Publishers, Dordrecht, pp 236CrossRefGoogle Scholar
  20. Bonga JM, Klimaszewska K, Lelu MA, von Aderkas P (1995) Somatic embryogenesis in Larix. In: Somatic embryogenesis in woody plants, Springer, Netherlands, pp 315–339CrossRefGoogle Scholar
  21. Bonga JM, Klimaszewska K, von Aderkas P (2010) Recalcitrance in clonal propagation, in particular of conifers. Plant Cell Tissue Organ Cult 100:241–254. doi: 10.1007/s11240-009-9647-2 CrossRefGoogle Scholar
  22. Borchert R (1976) The concept of juvenility in woody plants. Acta Hortic 56:21–36CrossRefGoogle Scholar
  23. Boulay M (1987) Conifer micropropagation: applied research and commercial aspects. In: Bonga JM, Durzan DJ (eds) Cell and tissue culture in forestry, case histories: gymnosperms, angiosperms and palms, vol 3. Martinus Nijhoff Publishers, Dordrecht, pp 185–206CrossRefGoogle Scholar
  24. Boutilier K, Offringa R, Sharma VK et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749PubMedPubMedCentralCrossRefGoogle Scholar
  25. Bozhkov PV, Filonova LH, von Arnold S (2002) A key developmental switch during Norway spruce somatic embryogenesis is induced by withdrawal of growth regulators and is associated with cell death and extracellular acidification. Biotechnol Bioeng 77:658–667PubMedCrossRefGoogle Scholar
  26. Breton D, Harvengt L, Trontin J-F et al (2006) Long-term subculture randomly affects morphology and subsequent maturation of early somatic embryos in maritime pine. Plant Cell Tissue Organ Cult 87:95–108. doi: 10.1007/s11240-006-9144-9 CrossRefGoogle Scholar
  27. Cairney J, Pullman GS (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 176:511–536. doi: 10.1111/j.1469-8137.2007.02239.x PubMedCrossRefGoogle Scholar
  28. Canhoto JM, Lopes ML, Cruz GS (2005) Protocol of SE: Tamarillo (Cyphomandra betacea (Cav.) Sendtn.). In: Jain SM, Gupta PK (eds) Protocol for SE in woody plants, forestry sciences, vol 77. Springer, Netherlands, pp 379–389. doi: 10.1007/1-4020-2985-3_30 Google Scholar
  29. Carneros E, Celestino C, Klimaszewska K et al (2009) Plant regeneration in Stone pine (Pinus pinea L.) by somatic embryogenesis. Plant Cell Tissue Organ Cult 98:165–178CrossRefGoogle Scholar
  30. Carron MP, Etienne H, Lardet L et al (1995) SE in rubber (Hevea brasiliensis Miill. Arg.). In: Jain S et al (eds) SE in woody plants, vol 2. Kluwer, Dordrecht, pp 117–136. doi: 10.1007/978-3-662-03091-2_23 Google Scholar
  31. Causevic A, Delaunay A, Ounnar S et al (2005) DNA methylating and demethylating treatments modify phenotype and cell wall differentiation state in sugar beet cell lines. Plant Physiol Biochem 43:681–691. doi: 10.1016/j.plaphy.2005.05.011 PubMedCrossRefGoogle Scholar
  32. Celestino C, Carneros E, Alegre J et al (2014) Formation of embryogenic-like tissues from mature zygotic embryos of stone pine. In: Proceedings of the third international conference of the IUFRO unit 2.09.02 on “Woody plant production integrating genetic and vegetative propagation technologies”, Vitoria-Gasteiz, pp 11–21Google Scholar
  33. Chakrabarty D, Yu KW, Paek KY (2003) Detection of DNA methylation changes during somatic embryogenesis of Siberian ginseng (Eleutherococcus senticosus). Plant Sci 165:61–68. doi: 10.1016/S0168-9452(03)00127-4 CrossRefGoogle Scholar
  34. Chalupa V (1990) Plant regeneration by somatic embryogenesis from cultured immature embryos of oak (Quercus robur L.) and linden (Tilia cordata Mill.). Plant Cell Rep 9:398–401PubMedCrossRefGoogle Scholar
  35. Chalupa V (1995a) SE in oak (Quercus spp.). In: Jain S et al (eds) SE in woody plants, vol 2. Kluwer, Netherlands, pp 67–87. doi: 10.1007/978-94-011-0491-3_5 Google Scholar
  36. Chalupa V (1995b) SE in (Betula pendula Roth.). In: Jain S et al (eds) SE in woody plants, vol 2. Kluwer, Netherlands, pp 137–151. doi: 10.1007/978-94-011-0491-3_9 Google Scholar
  37. Chalupa V (2005) Protocol of SE: pedunculate oak (Quercus robur) and sessile oak (Q. petraea). In: Jain SM, Gupta PK (eds) Protocol for SE in woody plants, forestry sciences, vol 77. Springer, Netherlands, pp 369–378. doi: 10.1007/1-4020-2985-3_29 Google Scholar
  38. Chang WC (1995) SE of Bambusa oldhamii, Bambusa beecheyana, and Sinocalamus latiflora. In: Jain S et al (eds) SE in woody plants, vol 2. Kluwer, Dordrecht, pp 53–65. doi: 10.1007/978-94-011-0491-3_4 Google Scholar
  39. Chavez VM, Litz RE, Norstog K (1992) In vitro morphogenesis of Ceratozamia hildae and C. mexicana from megagametophytes and zygotic embryos. Plant Cell Tissue Organ Cult 30:93–98. doi: 10.1007/BF00034301 CrossRefGoogle Scholar
  40. Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19(8):2430–2439PubMedPubMedCentralCrossRefGoogle Scholar
  41. Chupeau MC, Granier F, Pichon O et al (2013) Characterization of the early events leading to totipotency in an Arabidopsis protoplast liquid culture by temporal transcript profiling. Plant Cell 25:2444–2463PubMedPubMedCentralCrossRefGoogle Scholar
  42. Corredoira E, Ballester A, Ibarra M, Vieitez AM (2015) Induction of somatic embryogenesis in explants of shoot cultures established from adult Eucalyptus globulus and E. saligna × E. maidenii trees. Tree Physiol 35(6):678–690. doi: 10.1093/treephys/tpv028 Epub 2015 Apr 15 PubMedCrossRefGoogle Scholar
  43. Correia SI, Lopes ML, Canhoto JM (2009) SE in Tamarillo (Cyphomandra betacea): recent advances. Acta Hortic (ISHS) 839:157–164CrossRefGoogle Scholar
  44. Cortizo M, de Diego N, Moncalean P, Ordas RJ (2009) Micropropagation of adult Stone pine (Pinus pinea L.). Trees Struct Funct 23:835–842CrossRefGoogle Scholar
  45. Das DK, Rahman A (2013) Induction of somatic embryogenesis and long-term maintenance of embryogenic lines of Litchi. Curr Trends Biotechnol Pharm 7(2):625–634Google Scholar
  46. Datta MM, Majumder A, Jha S (2006) Organogenesis and plant regeneration in Taxus wallichiana (Zucc.). Plant Cell Rep 25:11–18PubMedCrossRefGoogle Scholar
  47. De Diego N, Montalban IA, Moncalean P (2010) In vitro regeneration of adult Pinus sylvestris trees. South Afr J Bot 76:158–162CrossRefGoogle Scholar
  48. De Jong AJ, Schmidt EDL, DeVries SC (1993) Early events in higher plant embryogenesis. Plant Mol Biol 22:367–377. doi: 10.1007/BF00014943 PubMedCrossRefGoogle Scholar
  49. De Vries SC, Booij H, Meyerink P et al (1988) Acquisition of embryogenic potential in carrot cell suspension cultures. Planta 176:196–204. doi: 10.1007/BF00392445 PubMedCrossRefGoogle Scholar
  50. De-la-Pena C, Nic-Can GI, Galaz-Avalos RM et al (2015) The role of chromatin modifications in somatic embryogenesis in plants. Front Plant Sci 6:635. doi: 10.3389/fpls.2015.00635 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Dodeman VL, Ducreux G, Kreis M (1997) Zygotic embryogenesis versus SE. J Exp Bot 48:1493–1509Google Scholar
  52. Domon J, Meyer Y, Faye L et al (1994) Extracellular (glyco) proteins in embryogenic and non-embryogenic cell lines of Caribbean pine. Comparison between phenotypes of stage one somatic embryos. Plant Physiol Biochem 32:137–147Google Scholar
  53. Dong JZ, Dustan DI (2000) Molecular biology of SE in conifers. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants, vol I. Kluwer, Dordrecht, pp 53–54. doi: 10.1007/978-94-017-2311-4_3 Google Scholar
  54. Dubois T, Guedira M, Dubois J, Vasseur J (1990) Direct SE in roots of Cichorium-is callose an early marker. Ann Bot 65(5):539–545. doi: 10.1093/aob/mcr033 Google Scholar
  55. Duhem K, Le Mercier N, Boxus P (1989) Donnes nouvelles sur l’induction et Ie developpement d’embryons somatiques chez Theobroma cacao L. Cafe Cacao The 33:9–14Google Scholar
  56. Dyachok JV, Wiweger M, Kenne L, von Arnold S (2002) Endogenous Nod-factor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol 128:523–533. doi: 10.1104/pp.010547 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Elhiti M, Stasolla C (2011) The use of zygotic embryos as explants for in vitro propagation: an overview. In: Thorpe TA, Yeung EC (eds) Plant embryo culture: methods and protocols, methods in molecular biology, vol 710, pp 229–255. doi: 10.1007/978-1-61737-988-8_17
  58. Elhiti M, Stasolla C (2012) In vitro propagation methods of ornamental conifers with emphasis on spruce SE. Propag Ornam Plants 12(1):3–10Google Scholar
  59. Elhiti M, Stasolla C, Wang A (2013) Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev Biol Plant 49:631–642CrossRefGoogle Scholar
  60. Evans DA, Sharp WR, Flick CE (1981) Growth and behavior of cell cultures—embryogenesis and organogenesis. In: Thorpe TA (ed) Plant tissue culture: methods and applications in agriculture. Academic Press, New York, pp 45–113Google Scholar
  61. Ewald D, Zaspel I, Naujoks G et al (2000) Endogenous bacteria in tissue cultures of conifers—appearance and action. In: Cassells AC, Doyle BM, Curry RF (eds) Proceedings of the international symposium on methods and markers for quality assurance in micropropagation. Acta Hort, vol 530, pp 137–145Google Scholar
  62. Feher A (2005) Why somatic plant cells start to form embryos? Plant Cell Monogr 2:85–101CrossRefGoogle Scholar
  63. Feher A (2008) The initiation phase of SE: what we know and what we don’t. Acta Biol Szeged 52(1):53–56Google Scholar
  64. Feher A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta 1849(4):385–402PubMedCrossRefGoogle Scholar
  65. Feher A, Pasternak T, Otvos K et al (2002) Induction of embryogenic competence in somatic plant cells: a review. Biologia 57:5–12Google Scholar
  66. Feher A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228. doi: 10.1023/a:1024033216561 CrossRefGoogle Scholar
  67. Fernandez-Guijarro B, Celistino C, Toribio M (1995) Influence of externa1 factors on secondary embryogenesis and germination in somatic embryo from leaves of Quercus suber. Plant Cell Tiss Organ Cult 41:99–106CrossRefGoogle Scholar
  68. Filonova LH, von Arnold S, Daniel G, Bozhkov PV (2002) Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ 9(10):1057–1062. doi: 10.1038/sj.cdd.4401068 PubMedCrossRefGoogle Scholar
  69. Fraser LG, Harvey CF (1986) SE from anther-derived callus in two Actinidia species. Sci Hortic 29:335–346. doi: 10.1016/0304-4238(86)90017-8 CrossRefGoogle Scholar
  70. Fulzele DP, Satdive RK (2003) Somatic embryogenesis, plant regeneration, and the evaluation of camptothecin content in Nothapodytes foetida. In Vitro Cell Dev Biol Plant 45:212–216CrossRefGoogle Scholar
  71. Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of SE of Arabidopsis. Planta 222(6):977–988. doi: 10.1007/s00425-005-0041-y PubMedCrossRefGoogle Scholar
  72. Gomez-Garay A, Lopez JA, Camafeitab E et al (2013) Proteomic perspective of Quercus suber SE. J Proteomics 93:314–325. doi: 10.1016/j.jprot.2013.06.006 PubMedCrossRefGoogle Scholar
  73. Gomez-Garay A, Manzanera JA, Pintos B (2014) Embryogenesis in Oak species. A review. Forest Syst 23(2):191–198CrossRefGoogle Scholar
  74. Gosal SS, Gill MIS, Grewal HS (1995) SE in Citrus species. In: Jain SM et al (eds) SE in woody plants, vol 2. Kluwer, Dordrecht, pp 1–21. doi: 10.1007/978-94-011-0491-3_1 Google Scholar
  75. Grosset J, Marty I, Chartier Y, Meyer Y (1990) mRNAs newly synthesized by tobacco mesophyll protoplasts are wound-inducible. Plant Mol Biol 15(3):485–496PubMedCrossRefGoogle Scholar
  76. Guerra MP, Silviera V, Santos ALW et al (2000) Somatic embryogenesis in A. augustifolia (Bert) O. Ktze. In: Jain S, Gupta P, Newton R (eds) Somatic Embryogenesis in Woody Plants, vol VI. Kluwer Academic Publishers, Dordrecht, Netherlands, pp 457–478Google Scholar
  77. Gupta PK, Durzan DJ (1987) Biotechnology of somatic poly-embryogenesis and plantlet regeneration in loblolly pine. Nat Biotechnol 5:147–151. doi: 10.1038/nbt0287-147 CrossRefGoogle Scholar
  78. Hackett WP (1985) Juvenility, maturation, and rejuvenation in woody plants. In: Janick J (ed) Horticultural reviews, vol 7. Wiley, Hoboken, p 23. doi: 10.1002/9781118060735.ch3 Google Scholar
  79. Hakman I, von Arnold S (1985) Plantlet regeneration through somatic embryogenesis in Picea abies. J Plant Physiol 121:149–158CrossRefGoogle Scholar
  80. Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J Plant Physiol 158:405–409CrossRefGoogle Scholar
  81. Harvengt L, Trontin JF, Reymont I et al (2001) Molecular evidence of true-to-type propagation of 3-year-old Norway spruce through somatic embryogenesis. Planta 213:823–832CrossRefGoogle Scholar
  82. Heringer AS, Steinmacher DA, Fraga HP et al (2013) Global DNA methylation profiles of somatic embryos of peach palm are influenced by cryoprotectants and droplet-vitrification cryopreservation. Plant Cell Tissue Organ Cult 114:365–372. doi: 10.1007/s11240-013-0331-1 CrossRefGoogle Scholar
  83. Jain SM, Newton RJ, Soltes EJ (1988) Enhancement of somatic embryogenesis in Norway spruce (Picea abies). Theor Appl Genet 76:501–506PubMedCrossRefGoogle Scholar
  84. Jain SM, Dong N, Newton RJ (1989) Somatic embryogenesis in slash pine (Pinus elliottii) from immature embryos cultured in vitro. Plant Sci 65:233–241CrossRefGoogle Scholar
  85. Jain S, Gupta PK, Newton RJ (1995a) SE in woody plants (3)—gymnosperms, forestry sciences, vol 44. Kluwer, Dordrecht, pp 1–388. doi: 10.1007/978-94-011-0960-4 Google Scholar
  86. Jain S, Gupta PK, Newton RJ (1995b) SE in woody plants (2)—angiosperms, forestry sciences, vol 46. Kluwer, Dordrecht, pp 1–509. doi: 10.1007/978-94-011-0491-3 Google Scholar
  87. Jain SM, Gupta PK, Newton RJ (1999a) SE in woody plants (4), forestry sciences, vol 55. Kluwer, Dordrecht, pp 1–547. doi: 10.1007/978-94-017-3032-7 Google Scholar
  88. Jain SM, Gupta PK, Newton RJ (1999b) SE in woody plants (5), forestry sciences, vol 59. Kluwer, Dordrecht, pp 1–336. doi: 10.1007/978-94-011-4774-3 Google Scholar
  89. Jain SM, Gupta PK, Newton RJ (2000) SE in woody plants (6), forestry sciences, vol 67. Kluwer, Dordrecht, pp 1–746. doi: 10.1007/978-94-017-3030-3 Google Scholar
  90. Jain S, Gupta PK, Newton RJ (2005) Protocols for SE in woody plants, forestry sciences, vol 77. Kluwer, Dordrecht, pp 1–385. doi: 10.1007/1-4020-2985-3 Google Scholar
  91. Jayasankar S, Bondada BR, Li Z, Gray DJ (2003) Comparative anatomy and morphology of Vitis vinifera (Vitaceae) somatic embryos from solid and liquid culture systems. Am J Bot 90:973–979PubMedCrossRefGoogle Scholar
  92. Jimenez VM (2001) Regulation of in vitro SE with emphasis on to the role of endogenous hormones. Rev Brasi de Fisio Vegl 13:196–223. doi: 10.1590/S0103-31312001000200008 CrossRefGoogle Scholar
  93. Jimenez VM (2005) Involvement of plant hormones and plant growth regulators on in vitro SE. Plant Growth Regul 47(2–3):91–110. doi: 10.1007/s10725-005-3478-x CrossRefGoogle Scholar
  94. Jimenez VM, Thomas C (2005) Participation of plant hormones in determination and progression of SE. In: Mujib A, Samaj J (eds) SE, plant cell monographs (2). Springer, Berlin, pp 103–118. doi: 10.1007/7089_034 Google Scholar
  95. Joy IVRW, Yeung EC, Kong L, Thorpe TA (1991) Development of white spruce somatic embryos: I. Storage product deposition. In Vitro Cell Dev Biol Plant 27:32–41. doi: 10.1007/BF02632059 CrossRefGoogle Scholar
  96. Kamada H, Kobayashi K, Kiyosue T, Harada H (1989) Stress-induced SE in carrot and its application to synthetic seed production. In Vitro Cell Dev Biol 25:1163–1169. doi: 10.1007/BF02621268 CrossRefGoogle Scholar
  97. Kamada H, Ishikawa K, Saga H, Harada H (1993) Induction of SE in carrot by osmotic stress. Plant Tissue Cult Lett 10:38–44CrossRefGoogle Scholar
  98. Kaplan DR, Cooke TJ (1997) Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9:1903–1919. doi: 10.1105/tpc.9.11.1903 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Karami O, Aghavaisi B, Pour AM (2009) Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol 2:177–190. doi: 10.1007/s12154-009-0028-4 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Kendurkar SV, Nadgauda RS, Phadke CH et al (1995) SE in some woody angiosperms. In: Jain SM, Gupta PK, Newton RJ (eds) SE in woody plants, vol 5. Kluwer, Dordrecht, pp 49–79. doi: 10.1007/978-94-011-0491-3 Google Scholar
  101. Klimaszewska K, Trontin JF, Becwar MR et al (2007) Recent progress in somatic embryogenesis of four Pinus spp. Tree Forest Sci Biotechnol 1(1):11–25Google Scholar
  102. Klimaszewska K, Noceda C, Pelletier G et al (2009) Biological characterization of young and aged embryogenic cultures of Pinus pinaster (Ait.). In Vitro Cell Dev Biol Plant 45:20–33. doi: 10.1007/s11627-008-9158-6 CrossRefGoogle Scholar
  103. Klimaszewska K, Overton C, Steward D, Rutledge RG (2011) Initiation of somatic embryos and regeneration of plants from primordial shoots of 10-year-old white spruce and expression profile of 11 genes followed during the tissue culture process. Planta 233(3):635–647. doi: 10.1007/s00425-010-1325-4 PubMedCrossRefGoogle Scholar
  104. Klimaszewska K, Hargreaves C, Lelu-Walter MA, Trontin JF (2015) Advances in conifer somatic embryogenesis since year 2000. In vitro embryogenesis in higher plants. Springer Science Media, New York, pp 131–166Google Scholar
  105. Kochba J, Button J (1974) The stimulation of embryogenesis and embryoid development in habituated ovular callus from the ‘Shamouti’ orange (Citrus sinensis) as affected by tissue age and sucrose concentration. Z Pflanzenphysiol 73:415–421CrossRefGoogle Scholar
  106. Kouakou TH, Waffo-Teguo P, Kouadio YJ et al (2007) Phenolic compounds and somatic embryogenesis in cotton (Gossypium hirsutum L.). Plant Cell Tissue Org Cult 90:25–29. doi: 10.1007/s11240-007-9243-2 CrossRefGoogle Scholar
  107. Krogstrup P (1986) Embryo-like structures from cotyledons and ripe embryos of Norway spruce (Picea abies). Can J Forest Res 16:664–668. doi: 10.1139/x86-116I CrossRefGoogle Scholar
  108. Krogstrup P, Eriksen EN, Moller JD, Roulund H (1988) SE in Sitka spruce (Picea sitchensis (Bong.) Carr.). Plant Cell Rep 7:594–597. doi: 10.1007/978-94-011-0960-4_9 PubMedCrossRefGoogle Scholar
  109. Kurten U, Nuutila AM, Kauppinen V, Rousi M (1990) SE in cell cultures of birch (Betula pendula Roth). Plant Cell Tissue Organ Cult 23:101–105. doi: 10.1007/BF00035829 CrossRefGoogle Scholar
  110. Kwaaitaal MA, de Vries SC, Russinova E (2005) Arabidopsis thaliana SE receptor kinase 1 protein is present in sporophytic and gametophytic cells and undergoes endocytosis. Protoplasma 226:55–65PubMedCrossRefGoogle Scholar
  111. Landey RB, Cenci A, Guyot R (2015) Assessment of genetic and epigenetic changes during cell culture ageing and relations with somaclonal variation in Coffea arabica. Plant Cell Tissue Organ Cult 122:517–531. doi: 10.1007/s11240-015-0772-9 CrossRefGoogle Scholar
  112. Lecourieux D, Mazars C, Pauly N et al (2002) Analysis and effects of cytosolic-free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14(10):2627–2641PubMedPubMedCentralCrossRefGoogle Scholar
  113. Leljak-Levanic D, Bauer N, Mihaljevic S, Jelaska S (2004) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23:120–127. doi: 10.1007/s00299-004-0819-6 PubMedCrossRefGoogle Scholar
  114. Lelu MA, Bornman CH (1990) Induction of SE in excised cotyledons of Picea abies and P. mariana. Plant Physiol Biochem 28:785–791Google Scholar
  115. Lelu-Walter MA, Bernier-Cardou M, Klimaszewska K (2006) Simplified and improved somatic embryogenesis for clonal propagation of Pinus pinaster. Plant Cell Rep 25:767–776PubMedCrossRefGoogle Scholar
  116. Levanic DL, Mihaljevic S, Jelaska S (2009) Variations in DNA methylation in Picea omorika (Panc) Purk. Embryogenic tissue and the ability for embryo maturation. Prop Orn Plants 9:3–9Google Scholar
  117. Lippert D, Zhuang J, Ralph S et al (2005) Proteome analysis of early SE in Picea glauca. Proteomics 5:461–473. doi: 10.1002/pmic.200400986 PubMedCrossRefGoogle Scholar
  118. Litz RE, Hendrix RC, Moon PA, Chavez VM (1998) Induction of embryogenic mango cultures as affected by genotype, explanting 2,4-D and embryogenic nurse culture. Plant Cell Tissue Organ Cult 53:13–18CrossRefGoogle Scholar
  119. Loidli P (2004) A plant dialect of the histone language. Trends Plant Sci 9:84–90. doi: 10.1016/j.tplants.2003.12.007 CrossRefGoogle Scholar
  120. Malabadi RB, van Staden J (2003) Somatic embryos can be induced from shoot apical domes of mature Pinus patula trees. South Afr J Bot 69:450–451CrossRefGoogle Scholar
  121. Malabadi RB, van Staden J (2005) SE from vegetative shoot apices of mature trees of Pinus patula. Tree Physiol 25:11–16PubMedCrossRefGoogle Scholar
  122. Malabadi RB, van Staden J (2006) Cold-enhanced SE in Pinus patula is mediated by calcium. South Afr J Bot 72:613–618CrossRefGoogle Scholar
  123. Malabadi RB, Teixeira da Silva JA, Nataraja K (2008a) A new approach involving salicylic acid and thin cell layers for cloning mature trees of Pinus roxburghii (Chir Pine). Am J Plant Sci Biotechnol 2(2):56–59Google Scholar
  124. Malabadi RB, Teixeira da Silva JA, Nataraja K (2008b) Salicylic acid induces SE from mature trees of Pinus roxburghii (Chir pine) using TCL technology. Tree Forest Sci Biotechnol 2(1):34–39Google Scholar
  125. Marsoni M, Bracale M, Espen L et al (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Rep 27(2):347–356PubMedCrossRefGoogle Scholar
  126. Martinez MT, Ballester A, Vieitez A, Corredoira E (2014) Induction of somatic embryogenesis in leaf and shoot apex explants derived from red oak trees: effects of explant type, silver thiosulphate and activated charcoal on the embryogenic system. In: Proceedings of the third international conference of the IUFRO unit 2.09.02 on “Woody plant production integrating genetic and vegetative propagation technologies”, Vitoria-GasteizGoogle Scholar
  127. Merckie SA, Parrott WA, Flinn BS (1995) Morphogenic aspects of SE. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer, Dordrecht, pp 155–203. doi: 10.1007/978-94-011-0485-2_5 Google Scholar
  128. Michler CH, Bauer EO (1991) High frequency somatic embryogenesis from leaf tissue of Populus spp. Plant Sci 77(1):111–118. doi: 10.1016/0168-9452(91)90186-C CrossRefGoogle Scholar
  129. Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62:3713–3725. doi: 10.1093/jxb/err155 PubMedCrossRefGoogle Scholar
  130. Mihaljevic S, Radic S, Bauer N et al (2011) Ammonium-related metabolic changes affect SE in pumpkin (Cucurbita pepo L.). J Plant Physiol 168(16):1943–1951. doi: 10.1016/j.jplph.2011.05.025 PubMedCrossRefGoogle Scholar
  131. Minocha SC, Minocha R (1995) Historical aspects of SE in woody plants. In: Jain S, Gupta P, Newtorz R (eds) SE in woody plants, vol 1. Kluwer, Dordrech, pp 9–22Google Scholar
  132. Mo LH, von Arnold S (1991) Origin and development of embryogenic cultures from seedlings of Norway spruce (Picea abies). J Plant Physiol 138:223–230CrossRefGoogle Scholar
  133. Monk M, Boubelik M, Lehnert S (1987) Temporal and regional changes in DNA methylation in the embryonic, extra embryonic and germ cell lineages during mouse embryo development. Development 99:371–382PubMedGoogle Scholar
  134. Montalban IA, De Diego N, Igartua EA (2011) A combined pathway of somatic embryogenesis and organogenesis to regenerate radiate pine plants. Plant Biotechnol Rep 5(2):177–186CrossRefGoogle Scholar
  135. Moon HK, Park SY, Kim YW, Kim SH (2008) Somatic embryogenesis and plantlet production using rejuvenated tissues from serial grafting of a mature Kalopanax septemlobus tree. In Vitro Cell Dev Biol Plant 44(2):119–127. doi: 10.1007/s11627-008-9122-5 CrossRefGoogle Scholar
  136. Moon HK, Kim YW, Hong YP, Park SY (2013) Improvement of somatic embryogenesis and plantlet conversion in Oplopanax elatus, an endangered medicinal woody plant. Springer Plus 2:421–428CrossRefGoogle Scholar
  137. Moore GA (1985) Factors affecting in vitro embryogenesis from undeveloped ovules of mature citrus fruits. J Am Soc Hortic Sci 110:66–70Google Scholar
  138. Mordhorst AP, Toonen MAJ, De Vries SC (1997) Plant embryogenesis. Crit Rev Plant Sci 16:535–576. doi: 10.1080/07352689709701959 CrossRefGoogle Scholar
  139. Moura-Costa PM, Viana AM, Mantell SH (1993) In vitro plantlet regeneration of Ocotea catharinensis, an endangered Brasilian hardwood forest tree. Plant Cell Tissue Organ Cult 35:279–286. doi: 10.1007/BF00037282 CrossRefGoogle Scholar
  140. Muller AJ (1963) Embryonentest zum Nachweis rezessiver Letalfaktoren bei Arabidopsis thaliana. Biol zbl 82:113–163Google Scholar
  141. Muralidharan EM, Mascarenhas AF (1995) SE in Eucalyptus. In: Jain S et al (eds) SE in woody plants, vol 2. Kluwer, Dordrecht, pp 23–40. doi: 10.1007/978-94-011-0491-3_2 Google Scholar
  142. Namasivayam P (2007) Acquisition of embryogenic competence during SE. Plant Cell Tissue Organ Cult 90:1–8. doi: 10.1007/s11240-007-9249-9 CrossRefGoogle Scholar
  143. Nawrot-Chorabik K (2008) Embryogenic callus induction and differentiation in silver fir (Abies alba Mill.) tissue cultures. Dendrobiology 59:31–40Google Scholar
  144. Nic-Can GI, De-la-Pena C (2014) Epigenetic advances on somatic embryogenesis of agronomical and important crops. In: Alvarez-Venegas A, De-la-Pena C, Casas-Mollano JA (eds) Epigenetics in plants of agronomic importance: fundamentals and applications. Springer, London, pp 91–109. doi: 10.1007/978-3-319-07971-4_6 Google Scholar
  145. Nic-Can GI, Lopez-Torres A, Barredo-Pool FA et al (2013) New insights into somatic embryogenesis: LEAFYCOTYLEDON1, BABYBOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS One 8:e72160. doi: 10.1371/journal.pone.0072160 PubMedPubMedCentralCrossRefGoogle Scholar
  146. Nic-Can GI, Galaz-Avalos RM, De-la-Pena C et al (2015) Somatic embryogenesis: identified factors that lead to embryogenic repression. A case of species of the same genus. PLoS One 10:e0126414. doi: 10.1371/journal.pone.0126414 PubMedPubMedCentralCrossRefGoogle Scholar
  147. Ning SB, Wang L, Song YC (1999) Programmed cell death in plants-a new emerging research field. Dev Reprod Biol 8:71–100Google Scholar
  148. Ogita S, Ishikawa H, Kubo T (1999) Somatic embryogenesis from immature and mature zygotic embryos of Cryptomeria japonica I: Embryogenic cell induction and its morphological characteristics. J Wood Sci 45:87–91CrossRefGoogle Scholar
  149. Ogita S, Sasamoto H, Yeung EC, Thorpe TA (2001) The effects of glutamine on the maintenance of embryogenic cultures of Cryptomeria japonica. In Vitro Cell Dev Biol Plant 37:268–273CrossRefGoogle Scholar
  150. Okano M, Bell DW, Haber DA, Li E (1999) DNA methyl transferases Dnmt3a and Dnmt3b are essential for denovo methylation and mammalian development. Cell 99:247–257. doi: 10.1016/S0092-8674(00)81656 PubMedCrossRefGoogle Scholar
  151. Pan Z, Guan R, Zhu S, Deng X (2009) Proteomic analysis of SE in Valencia sweet orange (Citrus sinensis Osbeck). Plant Cell Rep 28:281–289. doi: 10.1007/s00299-008-0633-7 PubMedCrossRefGoogle Scholar
  152. Pandey S (1998) Plant regeneration through SE in two tropical trees, Mangifera indica L. and Sterculia alata Roxb, unpublished Ph.D. thesis. Banaras Hindu University, VaranasiGoogle Scholar
  153. Park YS (2002) Implementation of conifer SE in clonal forestry: technical requirements and deployment considerations. Ann Forest Sci 59:651–656CrossRefGoogle Scholar
  154. Park YS (2010) Achievements in SE of conifers and its implementation in the management of future forests and plantations. Oral communication presented during the XXIII IUFRO World Congress, SeoulGoogle Scholar
  155. Park YS, Barrett JD, Bonga JM (1998) Application of SE in high-value clonal forestry: deployment, genetic control, and stability of cryopreserved clones. In Vitro Cell Dev Biol Plant 34:231–239CrossRefGoogle Scholar
  156. Park SY, Cho HM, Moon HK et al (2011) Genotypic variation and aging effects on the embryogenic capability of Kalopanax septemlobus. Plant Cell Tissue Organ Cult 105:265–270. doi: 10.1007/s11240-010-9862-x CrossRefGoogle Scholar
  157. Pasternak T, Prinsen E, Ayaydin F et al (2002) The role of auxin, pH and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa (Medicago sativa L.). Plant Physiol 129:1807–1819. doi: 10.1104/pp.000810 PubMedPubMedCentralCrossRefGoogle Scholar
  158. Pedroso MC, Pais MS (1995a) Explant region-specific embryogenic competence and plant recovery in Camellia japonica. Vitro Cell Dev Biol Plant 31(1):8–14. doi: 10.1007/BF02632219 CrossRefGoogle Scholar
  159. Pedroso MC, Pais MS (1995b) Factors controlling SE. Cell wall change as an in vivo marker of the embryogenic competence. Plant Cell Tissue Organ Cult 43:147–154. doi: 10.1007/BF00052170 CrossRefGoogle Scholar
  160. Perez M, Canal MJ, Toorop PE (2015) Expression analysis of epigenetic and abscisic acid-related genes during maturation of Quercus suber somatic embryos. Plant Cell Tissue Organ Cult 121:353–366. doi: 10.1007/s11240-014-0706-y CrossRefGoogle Scholar
  161. Pinto G, Park YS, Silva S et al (2008) Factors affecting maintenance, proliferation, and germination of secondary somatic embryos of Eucalyptus globulus Labill. Plant Cell Tissue Organ Cult 95(1):69–78CrossRefGoogle Scholar
  162. Polito VS, McGranahan G, Pinney K, Leslie C (1989) Origin of somatic embryos from repetitively embryogenic cultures of walnut (Juglans regia L.): implications for Agrobacterium mediated transformation. Plant Cell Rep 8:219–221. doi: 10.1007/BF00778537 PubMedCrossRefGoogle Scholar
  163. Poovaiah BW, Reddy ASN (1993) Calcium and signal transduction in plants. Crit Rev Plant Sci 12:185–211PubMedCrossRefGoogle Scholar
  164. Preece JE, Bates S (1995) SE in white ash (Fraxinus americana L.). In: Jain SM, Gupta PK, Newton RJ (eds) SE in woody plants, vol 5. Kluwer, Dordrecht, pp 311–325. doi: 10.1007/978-94-011-0491-3_17 Google Scholar
  165. Pullman GS, Bucalo K (2011) Pine somatic embryogenesis using zygotic embryos as explants. Methods Mol Biol 710:267–291. doi: 10.1007/978-1-61737-988-8_19 PubMedCrossRefGoogle Scholar
  166. Pullman GS, Cairney J, Xu N, Feng X (1999) Gene expression differences between zygotic and somatic embryos monitored by differential display and cDNA array: a potential tool to improve loblolly pine somatic embryo quality. In: Altman A, Ziv M, Izhar S (eds) Plant biotechnology and in vitro biology in the 21st century. Kluwer, Dordrecht, pp 81–84. doi: 10.1007/978-94-011-4661-6_18 CrossRefGoogle Scholar
  167. Quiroz-Figueroa F, Rojas-Herrera R, Galaz-Avalos RM, Loyola-Vargas VM (2006) Embryo production through SE can be used to study cell differentiation in plants. Plant Cell Tissue Organ Cult 86:285–301. doi: 10.1007/s11240-006-9139-6 CrossRefGoogle Scholar
  168. Raghavan V (2004) Role of 2,4-D in SE on cultured zygotic embryos of Arabidopsis: cell expansion, cell cycling, and morphogenesis during continuous exposure of embryos to 2,4-D. Am J Bot 91:1743–1756. doi: 10.3732/ajb.91.11.1743 PubMedCrossRefGoogle Scholar
  169. Rao PS (1965) In vitro induction of embryonal proliferation in Santalum album L. Phytomorphol 15:175–179Google Scholar
  170. Reinert J (1958) Untersuchungen über die Morphogenese an Gewebekulturen. Ber Dtsch Bot Ges 71:15. doi: 10.1007/BF01881795 Google Scholar
  171. Renau-Morata B, Ollero J, Arrillaga I, Segura J (2005) Factors influencing axillary shoot proliferation and adventitious budding in cedar. Tree Physiol 25:477–486PubMedCrossRefGoogle Scholar
  172. Roberts DR, Flinn BS, Webb DT et al (1989) Characterization of immature embryos of interior spruce by SDS-PAGE and microscopy in relation to their competence for SE. Plant Cell Rep 8:285–288. doi: 10.1007/BF00274131 PubMedCrossRefGoogle Scholar
  173. Rode C, Gallien S, Heintz D et al (2011) Enolases: storage compounds in seeds? Evidence from a proteomic comparison of zygotic and somatic embryos of Cyclamen persicum Mill. Plant Mol Biol 75(3):305–319PubMedCrossRefGoogle Scholar
  174. Rodriguez-Sanz H, Manzanera JA, Solis MT et al (2014a) Early markers are present in both embryogenesis pathways from microspores and immature zygotic embryos in cork oak, Quercus suber L. BMC Plant Biol 14:224. doi: 10.1186/s12870-014-0224-4 PubMedPubMedCentralCrossRefGoogle Scholar
  175. Rodriguez-Sanz H, Moreno-Romero J, Solís MT et al (2014b) Changes in histone methylation and acetylation during microspore reprogramming to embryogenesis occur concomitantly with BnHKMT and BnHATexpression and are associated to cell totipotency, proliferation and differentiation in Brassica napus. Cytogenet Genome Res 143:209–218. doi: 10.1159/000365261 PubMedCrossRefGoogle Scholar
  176. Roth R, Ebert I, Schmidt J (1997) Trisomy associated with loss of maturation capacity in a long-term embryogenic culture of Abies alba. Theor Appl Genet 95:353–358CrossRefGoogle Scholar
  177. Ruaud JN, Bercetche J, Paques M (1992) First evidence of SE from needles of 1-year-old Picea abies. Plant Cell Rep 11:563–566. doi: 10.1007/BF00233093 PubMedCrossRefGoogle Scholar
  178. Saad S (1975) Factors affecting the growth of lemon (Citrus limon) callus in vitro culture, M.Sc. Thesis. Hebrew University, JerusalemGoogle Scholar
  179. Salajova T, Jasik J, Kormutak A, Salaj J, Hakman I (1996) Embryogenic culture initiation and somatic embryo development in hybrid firs (Abies alba × Abies cephalonica, and Abies alba × Abies numidica). Plant Cell Rep 15:527–553PubMedGoogle Scholar
  180. Santos D, Fevereiro P (2002) Loss of DNA methylation affects somatic embryogenesis in Medicago truncatula. Plant Cell Tissue Organ Cult 70:155–161. doi: 10.1023/A:1016369921067 CrossRefGoogle Scholar
  181. Saze H, Scheid OM, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:65–69. doi: 10.1038/ng1138 PubMedCrossRefGoogle Scholar
  182. Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) Leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124(10):2049–2062PubMedGoogle Scholar
  183. Schuerman PL, Dandekar AM (1993) Transformation of temperate woody crops: progress and potentials. Sci Hortic 55:101–124. doi: 10.1016/0304-4238(93)90027-N CrossRefGoogle Scholar
  184. Sharon M, Sinha S, Sharan M (2011) Somatic embryogenesis in different root segments of Punica granatum L. Ann Biol Res 2(5):104–112Google Scholar
  185. Sharp WR, Evans DA, Soudahl MR (1982) Applications of SE to crop improvement. In: Fujiwara A (ed) Proceedings of fifth international Congo plant tissue and cell culture. Japan Assoc. for Plant Tissue Culture, Tokyo, pp 759–762Google Scholar
  186. Silva JJ, Debergh P (2001) Somatic embryogenesis from flower explants of cocoa (Theobroma cacao L.). Meded Rijksuniv Gent Fak Landbouwkd Toegep Biol Wet 66(1):31–34PubMedGoogle Scholar
  187. Silveira V, Steiner N, Santos ALW et al (2002) Biotechnology tolls in Araucaria angustifolia conservation and improvement: inductive factors affecting somatic embryogenesis. Crop Breed Appl Biotechnol 2:463–470CrossRefGoogle Scholar
  188. Sim G, Loh C, Goh G (1988) Direct SE from protoplasts of Citrus mitis Blanco. Plant Cell Rep 7:5–8. doi: 10.1007/BF00269527 CrossRefGoogle Scholar
  189. Singla B, Chugh A, Khurana JP, Khurana P (2006) An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J Exp Bot 57(15):4059–4070PubMedCrossRefGoogle Scholar
  190. Singla B, Tyagi AK, Khurana JP, Khurana P (2007) Analysis of expression profile of selected genes expressed during auxin-induced somatic embryogenesis in leaf base system of wheat (Triticum aestivum) and their possible interactions. Plant Mol Biol 65(5):677–692PubMedCrossRefGoogle Scholar
  191. Sita GL (1999) SE in rosewood and other Indian tree legumes. In: Jain SM et al (eds) SE in woody plants, vol 5. Kluwer, Dordrecht, pp 95–112. doi: 10.1007/978-94-011-4774-3 Google Scholar
  192. Smith DR (1997) The role of in vitro methods in pine plantation establishment: the lesson from New Zealand. Plant Tissue Cult Biotechnol 3:63–73CrossRefGoogle Scholar
  193. Spencer MWB, Grene R, Lindsey K (2007) Transcriptional profiling of the Arabidopsis embryo. Plant Physiol 143:924–940PubMedPubMedCentralCrossRefGoogle Scholar
  194. Srichuay W, Kalawong S, Sirisom Y, Te-chato S (2014) Callus induction and somatic embryogenesis from anther cultures of Hevea brasiliensis Muell Arg. Kasetsart J (Nat Sci) 48:364–375Google Scholar
  195. Stasolla C, Yeung EC (2003) Recent advances in conifer SE: improving somatic embryo quality. Plant Cell Tissue Organ Cult 74:15–35. doi: 10.1023/a:1023345803336 CrossRefGoogle Scholar
  196. Stasolla C, Kong L, Yeung EC, Thorpe TA (2002) Maturation of somatic embryos in conifers: morphogenesis, physiology, biochemistry, and molecular biology. In Vitro Cell Dev Biol -Plant 38:93–105CrossRefGoogle Scholar
  197. Stasolla C, van Zyl L, Egertsdotter U et al (2003) The effects of polyethylene glycol (PEG) on gene expression of developing white spruce somatic embryos. Plant Physiol 131(1):49–60. doi: 10.1104/pp.015214 PubMedPubMedCentralCrossRefGoogle Scholar
  198. Stasolla C, Bozhkov PV, Chu T-M et al (2004) Variation in transcript abundance during somatic embryogenesis in gymnosperms. Tree Physiol 24:1073–1085PubMedCrossRefGoogle Scholar
  199. 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 45:705–708CrossRefGoogle Scholar
  200. Tautorus TE, Fowke LC, Dunstan DI (1991) SE in conifers. Can J Bot 69(9):1873–1899. doi: 10.1139/b91-237 CrossRefGoogle Scholar
  201. 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. doi: 10.1007/s00425-005-0027-9 PubMedCrossRefGoogle Scholar
  202. Teixeira da Silva JA, Malabadi RB (2012) Factors affecting SE in conifers. J Forest Res 23(4):503–515. doi: 10.1007/s11676-012-0266-0 CrossRefGoogle Scholar
  203. Teyssier C, Maury S, Beaufour M et al (2014) In search of markers for somatic embryo maturation in hybrid larch (Larixx eurolepis): global DNA methylation and proteomic analyses. Physiol Plant 150:271–291. doi: 10.1111/ppl.12081 PubMedCrossRefGoogle Scholar
  204. Thakare D, Tang W, Hill K, Perry SE (2008) The MADS-domain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol 146:1663–1672PubMedPubMedCentralCrossRefGoogle Scholar
  205. Thorpe TA, Stasolla C (2001) Somatic embryogenesis. In: Bhojwani SS (ed) Current trends in the embryology of angiosperms. Kluwer, Dordrecht, pp 279–336. doi: 10.1007/978-94-017-1203-3_12 CrossRefGoogle Scholar
  206. Tisserat B, Esan EB, Murashige T (1979) Somatic embryogenesis in angiosperms. Hortic Rev 1:1–78. doi: 10.1002/9781118060742.ch1 Google Scholar
  207. Tokuji Y, Kuriyama K (2003) Involvement of gibberellin and cytokinin in the formation of embryogenic cell clumps in carrot (Daucus carota). J Plant Physiol 160(2):133–141. doi: 10.1078/0176-1617-00892 PubMedCrossRefGoogle Scholar
  208. Toonen MAJ, Hendriks T, Schmidt EDL et al (1994) Description of somatic embryo forming a single cell in the carrot suspension cultures employing video cell tracking. Planta 194:565–572CrossRefGoogle Scholar
  209. Tremblay L, Levasseur C, Tremblay FM (1999) Frequency of somaclonal variation in plants of Black spruce (Picea mariana, Pinaceae) and White spruce (P. glauca, Pinaceae) derived from somatic embryogenesis and identification of some factors involved in genetic instability. Am J Bot 86(10):1373–1381PubMedCrossRefGoogle Scholar
  210. Tretyakova I, Voroshilova E (2014) Embryo initiation from Pinus sibirica megagametophytes in in vitro culture. Russ J Dev Biol 45(2):93CrossRefGoogle Scholar
  211. Trigiano RN, Beaty RM, Graham ET (1988) Somatic embryogenesis from immature embryos of redbud (Cercis canadensis). Plant Cell Rep 7:148–150. doi: 10.1007/BF00270127 PubMedCrossRefGoogle Scholar
  212. Trontin JF, Klimaszewska K, Morel A et al (2015) Molecular aspects of conifer zygotic and somatic embryo development: a review of genome-wide approaches and recent insights. In vitro embryogenesis in higher plants. Springer Science Media, New York, pp 167–207Google Scholar
  213. Tulecke W (1987) Somatic embryogenesis in woody perennials. In: Bonga JM et al (eds) Cell and tissue culture in forestry. Martinus Nijhoff Publishers, Dordrecht, p 62. doi: 10.1007/978-94-009-4484-8_5 Google Scholar
  214. Tuteja N, Gill SS, Trivedi PK et al (2010) Plant growth regulators and their role in stress tolerance. In: Anjum NA (ed) Plant nutrition and abiotic stress tolerance I. Plant stress, vol 4, specila issue 1, pp 1–18Google Scholar
  215. van Arnold S, Hakman I (1988) Regulation of somatic embryo development in Picea abies by abscisic acid (ABA). J Plant Physiol 132:164–168CrossRefGoogle Scholar
  216. van Arnold S, Woodward S (1988) Organogenesis and embryogenesis in mature zygotic embryos of Picea sitchensis. Tree Physiol 4:291–300. doi: 10.1093/treephys/4.3.291 PubMedCrossRefGoogle Scholar
  217. van Arnold S, Clapham D, Egertsdotter U, Mo LH (1996) Somatic embryogenesis in conifers—a case study of induction and development of somatic embryos in Picea abies. Plant Growth Regul 20:3–9CrossRefGoogle Scholar
  218. van Arnold S, Sabala I, Bozhkov P et al (2002) Developmental pathways of SE. Plant Cell Tissue Organ Cult 69:233–249. doi: 10.1023/a:1015673200621 CrossRefGoogle Scholar
  219. van Hengel AJ, Tadesse Z, Immerzeel P et al (2001) N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control SE. Plant Physiol 125:1880–1890PubMedPubMedCentralCrossRefGoogle Scholar
  220. van Zyl L, von Arnold S, Bozhkov P et al (2002) Heterologous array analysis in Pinaceae: hybridization of high-density arrays of Pinus taeda cDNA with cDNA from needles and embryogenic cultures of P. taeda, P. sylvestris and Picea abies. Comp Funct Genom 3(4):306–318. doi: 10.1002/cfg.199 CrossRefGoogle Scholar
  221. van Zyl L, Bozhkov PV, Clapham DH et al (2003) Up, down and up again is a signature global gene expression pattern at the beginning of gymnosperm embryogenesis. Gene Expr Patterns 3:83–91PubMedCrossRefGoogle Scholar
  222. Varshney A, Anis M (2014) Trees: propagation and conservation, biotechnological approaches for the propagation of a multipurpose tree, Balanites aegyptica Del. Springer XVI. doi: 10.1007/978-81-322-1701-5
  223. Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent vs totipotent plant stem cells: dependence vs autonomy? Trends Plant Sci 12:245–252. doi: 10.1016/j.tplants.2007.04.002 PubMedCrossRefGoogle Scholar
  224. Verhagen SA, Wann SR (1989) Norway spruce SE: high frequency initiation from light-cultured mature embryos. Plant Cell Tissue Organ Cult 16:103–111. doi: 10.1007/BF00036518 CrossRefGoogle Scholar
  225. Vestman D, Larsson E, Uddenberg D et al (2011) Important processes during differentiation and early development of somatic embryos of Norway spruce as revealed by changes in global gene expression. Tree Genet Genomes 7:347–362CrossRefGoogle Scholar
  226. Vieitez AM, Barciel J (1990) Somatic embryogenesis and plant regeneration from embryogenic tissues of Camellia japonica L. Plant Cell Tissue Organ Cult 21:267–274. doi: 10.1007/BF00047620 CrossRefGoogle Scholar
  227. Viejo M, Rodriguez R, Valledor L et al (2010) DNA methylation during sexual embryogenesis and implications on the induction of somatic embryogenesis in Castanea sativa Miller. Sex Plant Reprod 23:315–323. doi: 10.1007/s00497-010-0145-9 PubMedCrossRefGoogle Scholar
  228. von Aderkas P, Bonga JM (2000) Influencing micropropagation and SE in mature trees by manipulation of phase change, stress and culture environment. Tree Physiol 20:921–928. doi: 10.1093/treephys/20.14.921 CrossRefGoogle Scholar
  229. von Arnold S (1987) Improved efficiency of somatic embryogenesis in mature embryos of Picea abies. J Plant Physiol 128:233–244CrossRefGoogle Scholar
  230. Walter C, Find JI, Grace LJ (2005) Somatic embryogenesis and genetic transformation in Pinus radiata. In: Jain SM, Gupta PK (eds) Protocol for SE in woody plants, forestry sciences, vol 77. Springer, Dordrecht, pp 11–13. doi: 10.1007/1-4020-2985-3_2 Google Scholar
  231. Wang L, Wang Y, Zhang M, Lu Y (2001) Pollination induced apoptosis in tobacco related to expression of calcium/calmodulin- dependent protein kinase T1. Dev Reprod Biol 10:53–60Google Scholar
  232. Wann SR (1988) Somatic embryogenesis in woody species. Hortic Rev 10:153–181. doi: 10.1002/9781118060834.ch5 Google Scholar
  233. Wickramasuriya AM, Dunwell JM (2015) Global scale transcriptome analysis of Arabidopsis embryogenesis in vitro. BMC Genom 16:301. doi: 10.1186/s12864-015-1504-6 CrossRefGoogle Scholar
  234. Winkelmann T (2013) Recent advances in the propagation of woody plants. Acta Hortic (ISHS) 990:375–381CrossRefGoogle Scholar
  235. Wiweger M (2003) Signal molecules in embryogenesis of Norway spruce. Doctoral thesis, Swedish University of Agricultural Sciences, Uppsala, pp 1–53. ISSN 1401-6230; ISBN 91-576-6527-3Google Scholar
  236. Wu JH, Cheng JS, Zhang WE, Wan SY (1990) Studies on the ovule culture and SE of Citrus. J Fruit Sci 7:19–24Google Scholar
  237. Xu M, Li X, Korban S (2004) DNA-methylation alterations and exchanges during in vitro cellular differentiation in rose (Rosa hybrid L.). Theor Appl Genet 109:899–910. doi: 10.1007/s00122-004-1717-6 PubMedCrossRefGoogle Scholar
  238. Yamamoto N, Kobayashi H, Togashi T et al (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. doi: 10.1016/j.jplph.2004.05.013 PubMedCrossRefGoogle Scholar
  239. Yang XY, Zhang XL (2010) Regulation of SE in higher plants. Critic Rev Plant Sci 29(1):36–57. doi: 10.1080/07352680903436291 CrossRefGoogle Scholar
  240. Yang X, Zhang X (2011) Developmental and molecular aspects of non-zygotic (somatic) embryogenesis. In: Trigiano RN, Gray DJ (eds) Plant tissue culture, development and biotechnology. CRC Press, Boca raton, pp 307–326Google Scholar
  241. Yeung EC (1995) Structural and developmental patterns in SE. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer, Dordrecht, pp 205–248. doi: 10.1007/978-94-011-0485-2_6 CrossRefGoogle Scholar
  242. You XL, Yi JS, Choi YE (2006) Cellular change and callose accumulation in zygotic embryos of Eleutherococcus senticosus caused by plasmolysing pretreatment result in a high frequency of single-cell-derived SE. Protoplasma 227(2–4):105–112Google Scholar
  243. Yu TA, Yeh SD, Yang JS (2001) Effects of carbenicillin and cefotaxime on callus growth and somatic embryogenesis from adventitious roots of papaya. Bot Bull Acad Sin 42Google Scholar
  244. Zavattieri M, Frederico A, Lima M et al (2010) Induction of somatic embryogenesis as an example of stress-related plant reactions. Electron J Biotechnol North Am 13(1):15Google Scholar
  245. Zhang H, Horgan KJ, Reynolds PHS, Jameson PE (2010) 6-Benzyladenine metabolism during reinvigoration of mature Pinus radiata buds in vitro. Trees Physiol 30:514–526CrossRefGoogle Scholar
  246. Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promote a vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359PubMedCrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2016

Authors and Affiliations

  1. 1.Cellular Differentiation and Molecular Genetics Section, Department of BotanyHamdard UniversityNew DelhiIndia

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