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Volume: 6, Issue: 5, Sep-Oct, 2018
DOI: 10.7324/JABB.2018.60508

Review Article

Progress in understanding the regulation and expression of genes during plant somatic embryogenesis: A review

Vikrant, Prajisha Janardhanan

  Author Affiliations


Based on the previous available documents involving molecular events during plant somatic embryogenesis, this report aims to review the advances that have been made for the past several years in the area of molecular mechanism of plant somatic embryogenesis. To begin with, studies suggest that the induction and differentiation of embryos from somatic tissue directly or through callusing involves the interaction of various cellular and molecular factors. Several intra- and extra-cellular proteins such as germins and germins-like proteins, lipid transfer proteins, heat-shock proteins, and late embryogenesis abundant proteins are known to regulate the induction of somatic embryos from the somatic cell. Simultaneously, regulation and expression of specific genes such as housekeeping genes OsIAA in rice; hormone-responsive genes Dcarg-1, Dchsp-1, DcECP31, DcEMB1 in carrot; and AtECP63, Mt somatic embryo-related factor 1 in arabidopsis have been identified to play key roles during the process of somatic embryogenesis. These genes are known to express differentially for synthesis of new proteins during induction and development of somatic embryo. In addition, several transcription factors such as leafy cotyledon genes, agamous-like15 (AGL15) gene, ethylene-responsive element-binding protein (EREBPs), knotted1-like homeobox proteins, and RWP-RK group of plant-specific transcription factors are equally known that efficiently control the molecular events of somatic embryogenesis. Further, it is also now established that epigenetic factors such asDNA methylation, histone deacetylation/methylation, and microRNAs also influence the molecular mechanism of plant somatic embryogenesis.


Somatic embryo, Regulatory protein, Regulatory gene, Gene expression, MicroRNAs.

Citation: Vikrant, Janardhanan P. Progress in understanding the regulation and expression of genes during plant somatic embryogenesis: A review. J App
Biol Biotech. 2018;6(05):49-56. DOI: 10.7324/JABB.2018.60508

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited.


1. Steward FC, Mapes MO, Smith J. Growth and organized development of cultured cells. I. Growth and division of freely suspended cells. Am J Bot 1958;45:693-703. https://doi.org/10.1002/j.1537-2197.1958.tb12224.x

2. Reinert J. Uber die kontrolle der morphogenese und die induktion von adventivembryonen an gew-ebekulturen aus karotten. Planta 1959;53:318-33. https://doi.org/10.1007/BF01881795

3. Feh\ér A. Somatic embryogenesis - stress-induced remodeling of plant cell fate. Biochim Biophys Acta 2015;1849:385-402. https://doi.org/10.1016/j.bbagrm.2014.07.005

4. Ikeda-Iwai M, Umehara M, Satoh S, Kamada H. Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J 2003;34:107-14. https://doi.org/10.1046/j.1365-313X.2003.01702.x

5. Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K. Plant regeneration: Cellular origins and molecular mechanisms. Development 2016;143:1442-51. https://doi.org/10.1242/dev.134668

6. Malik MR, Wang F, Dirpaul JM, Zhou N, Polowick PL, Ferrie AM, et al. Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiol 2007;144:134-54. https://doi.org/10.1104/pp.106.092932

7. Elhiti MA. Molecular Characterizations of Several Brassica Shoot Apical Meristem Genes and the Effect of their Altered Expression During in vitro Morphogenesis. Ph.D. Thesis, Faculty of Graduate Studies, University of Manitoba; 2010.

8. Elhiti M, Claudio S, Wang A. Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev Biol Plant 2013. DOI: 10.1007/ s11627-013-9547-3.

9. Chugh A, Khurana P. Gene expression during somatic embryogenesis– recent advances. Curr Sci 2002;86:715-30.

10. Feher A, Pasternak TP, Dudits D. Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 2003;74:201-28. https://doi.org/10.1023/A:1024033216561

11. Zeng F, Zhang X, Jin S, Cheng L, Liang S, Hu L, et al. Chromatin reorganization and endogenous auxin/cytokinin dynamic activity during somatic embryogenesis of cultured cotton cell. Plant Cell Tissue Organ Cult 2007;90:63-70. https://doi.org/10.1007/s11240-007-9253-0

12. Zhang CX, Li Q, Kong L. Induction, development and maturation of somatic embryos in Bunge's pine (Pinus bungeana Zucc. ex Endl.). Plant Cell Tissue Organ Cult 2007;91:273-80. https://doi.org/10.1007/s11240-007-9294-4

13. Karami O, Aghavaisi B, Pour AM. Molecular aspects of somaticto-embryogenic transition in plants. J Chem Biol 2009;2:177-90. https://doi.org/10.1007/s12154-009-0028-4

14. Abid G, Jacquemin JM, Sassi K, Muhovski Y, Toussaint A, Baudoin JP. Gene expression and genetic analysis during higher plants embryogenesis. Biotechnol Agron Soc Environ 2010;14:667-80.

15. Joshi R, Kumar P. Regulation of somatic embryogenesis in crops: A review. Agric Rev 2013;34:1-20.

16. Rocha DI, Dornelas MC. Molecular overview on plant somatic embryogenesis. CAB Rev 2013;8:1-17. Available from: http://www. cabi.org/cabreviews. [Last accessed on 2013 Feb].

17. Smertenko A, Bozhkov PV. Somatic embryogenesis: Life and death processes during apical–basal patterning. J Exp Bot 2014;12:1-18. https://doi.org/10.1093/jxb/eru005

18. Toonen MA, Verhees JA, Schmidt ED, van Kammen A, de Vries SC. AtLTP1 luciferase expression during carrot somatic embryogenesis. Plant J 1997;12:1213-21. https://doi.org/10.1046/j.1365-313X.1997.12051213.x

19. Domon JM, Neutelings G, Roger D, David A, David H. A basic chitinase-like protein secreted by embryogenic tissues of Pinus caribaea acts on arabinogalactan proteins extracted from the same cell line. J Plant Physiol 2000;156:33-9. https://doi.org/10.1016/S0176-1617(00)80269-2

20. Gavish H, Vardi A, Fluhr R. Suppression of somatic embryogenesis in citrus cell cultures by extracellular proteins. Planta 1992;186:511-7. https://doi.org/10.1007/BF00198030

21. Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC. Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 1993;268:12239-42.

22. Neutelings G, Domon JM, Membre N, Bernier F, Meyer Y, David A, et al. Characterization of a germin-like protein gene expressed in somatic and zygotic embryos of pine (Pinus caribaea Morelet). Plant Mol Biol 1998;38:1179-90. https://doi.org/10.1023/A:1006033622928

23. Wojtaszek P, Pislewska M, Bolwell GP, Stobiecki M. Secretion of stress-related proteins by suspension-cultured Lupinus albus cells. Acta Biochim Pol 1998;45:281-5.

24. Çaliskan M, Turet M, Cuming AC. Formation of wheat (Triticum aestivum L.) embryogenic callus involves peroxide-generating germin-likeoxalate oxidase. Planta 2004;219:132-40. https://doi.org/10.1007/s00425-003-1199-9

25. Sterk P, Booij H, Schellekens G, Van Kammen A, De Vries S. Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 1991;3:907-21. https://doi.org/10.1105/tpc.3.9.907

26. Dodeman VL, Ducreux G, Kreis M. Zygotic embryogenesis versus somatic embryogenesis. J Exp Bot 1997;48:1493-509.

27. Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y, et al. Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Mol Biol 2006;60:167-83. https://doi.org/10.1007/s11103-005-3381-x

28. Du H, Clarke AE, Bacic A. Arabinogalactan-proteins: A class of extracellular proteoglycans involved in plant growth and development. Trends Cell Biol 1996;6:411-4. https://doi.org/10.1016/S0962-8924(96)20036-4

29. Showalter AM. Arabinogalactan-proteins: Structure, expression and function. Cell Mol Life Sci 2001;58:1399-417. https://doi.org/10.1007/PL00000784

30. Stacey N, Roberts K, Knox JP. Patterns of expression of the JIM4 arabinogalactan-protein epitope in cell cultures and during somatic embryogenesis in Daucus carota L. Planta 1990;180:285-92. https://doi.org/10.1007/BF00194009

31. van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, de Vries SC, et al. N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol 2001;125:1880-90. https://doi.org/10.1104/pp.125.4.1880

32. Saare-Surminskia K, Preilb W, Knoxc JP, Liebereia R. Arabinogalactan proteins in embryogenic and non-embryogenic callus cultures of Euphorbia pulcherrima. Physiol Plant 2000;108:180-7. https://doi.org/10.1034/j.1399-3054.2000.108002180.x

33. Letarte J, Simion E, Miner M, Kasha KJ. Arabinogalactans and arabinogalactan-proteins induce embryogenesis in wheat (Triticum aestivum L.) microspore culture. Plant Cell Rep 2006;24:691-8. https://doi.org/10.1007/s00299-005-0013-5

34. Legrand S, Hendriks T, Hilbert JL, Quillet MC. Characterization of expressed sequence tags obtained by SSH during somatic embryogenesis in Cichorium intybus L. BMC Plant Biol 2007;7:27. https://doi.org/10.1186/1471-2229-7-27

35. Filonova LH, Bozhkov PV, von Arnold S. Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking. J Exp Bot 2000;51:249-64. https://doi.org/10.1093/jexbot/51.343.249

36. Kreuger M, van Holst GJ. Arabinogalactan proteins are essential in somatic embryogenesis of Daucus carota L. Planta 1993;189:243-8. https://doi.org/10.1007/BF00195083

37. Egertsdotter U, von Arnold S. Importance of arabinogalactan proteins for development of somatic embryos of Norway spruce (Picea abies). Physiol Plant 1995;93:334-45. https://doi.org/10.1111/j.1399-3054.1995.tb02237.x

38. Coca MA, Almoguera C, Jordano J. Expression of sunflower low-molecular-weight heat-shock proteins during embryogenesis and persistence after germination: Localization and possible functional implications. Plant Mol Biol 1994;25:479-92. https://doi.org/10.1007/BF00043876

39. Kitamiya E, Suzuki S, Sano T, Nagata T. 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 Reports 2000;19:551-7. https://doi.org/10.1007/s002990050772

40. Pitto J, Schiavo FL, Guiliano G, Terzi M. Analysis of the heat-shock protein pattern during somatic embryogenesis of carrot. Plant Mol Biol 1983;2:231-7. https://doi.org/10.1007/BF01578641

41. Kanabus J, Pikaard CS, Cherry JH. Heat shock proteins in tobacco cell suspension during growth cycle. Plant Physiol 1984;75:639-44. https://doi.org/10.1104/pp.75.3.639

42. Zimmerman JL, Apuya N, Darwish K, O'Carroll C. Novel regulation of heat shock genes during carrot somatic embryo development. Plant Cell 1989;1:1137-46. https://doi.org/10.1105/tpc.1.12.1137

43. Györgyey J, Gartner A, N\émeth K, Magyar Z, Hirt H, Heberle-Bors E, et al. Alfalfa heat shock genes are differentially expressed during somatic embryogenesis. Plant Mol Biol 1991;16:999-1007. https://doi.org/10.1007/BF00016072

44. Hatzopoulos P, Fong F, Sung ZR. Abscisic acid regulation of DC8, a carrot embryonic gene. Plant Physiol 1990;94:690-5. https://doi.org/10.1104/pp.94.2.690

45. Cheng JC, Seeley KA, Goupil P, Sung ZR. Expression of DC8 is associated with, but not dependent on embryogenesis. Plant Mol Biol 1996;31:127-41. https://doi.org/10.1007/BF00020612

46. Wurtele ES, Wang H, Durgerian S, Nikolau BJ, Ulrich TJ. Characterization of a gene expressed early in somatic embryogenesis of Daucus carota. Plant Physiol 1993;102:303-12. https://doi.org/10.1104/pp.102.1.303

47. Sharon N, Goldstein IJ. Lectins: More than insecticides. Science 1998;282:1049. https://doi.org/10.1126/science.282.5391.1047e

48. Koltunow AM, Hidaka T, Robinson SP. Polyembryony in citrus. Accumulation of seed storage proteins in seeds and in embryos cultured in vitro. Plant Physiol 1996;110:599-609. https://doi.org/10.1104/pp.110.2.599

49. Aleith F, Richter G. Gene expression during induction of somatic embryogenesis in carrot cell suspensions. Planta 1990;183:17-24.

50. Kawahara R, Sunabori S, Fukuda H, Komamine A. A gene expressed preferentially in the globular stage of somatic embryogenesis encodes elongation-factor 1 alpha in carrot. Eur J Biochem 1992;209:157-62. https://doi.org/10.1111/j.1432-1033.1992.tb17272.x

51. Sato S, Toya T, Kawahara R, Whittier RF, Fukuda H, Komamine A, et al. Isolation of a carrot gene expressed specifically during early-stage somatic embryogenesis. Plant Mol Biol 1995;28:39-46. https://doi.org/10.1007/BF00042036

52. Dudits D, Bogre L, Gyorgyey J. Molecular and cellular approaches to the analysis of plant embryo development from somatic cells in vitro. J Cell Sci 1991;99:475-84.

53. De Klerk GJ, Arnholdt-Schmitt B, Lieberei R, Neumann KH. Regeneration of roots, shoots and embryos: Physiological, biochemical and molecular aspects. Biol Plant 1997;39:53-66. https://doi.org/10.1023/A:1000304922507

54. Vikrant, Rashid A. Somatic embryogenesis or shoot formation following high 2,4-D pulse-treatment of mature embryos of Paspalum scrobiculatum L. Biol Plant 2003;46:297-300. https://doi.org/10.1023/A:1022875332607

55. Yang X, Zhang X. Regulation of somatic embryogenesis in higher plants. Crit Rev Plant Sci 2010;29:36-57. https://doi.org/10.1080/07352680903436291

56. Thakur J, Tyagi AK, Khurana JP. OsIAA1, an Aux/IAA cDNA from rice and changes in its expression as influenced by auxin and light. DNA Res 2001;8:193-203. https://doi.org/10.1093/dnares/8.5.193

57. Higashi K, Shiota H, Kamada H. Patterns of expression of the genes for glutamine synthetase isoforms during somatic and zygotic embryogenesis in carrot. Plant Cell Physiol 1998;39:418-24. https://doi.org/10.1093/oxfordjournals.pcp.a029385

58. Charriere F, Hahne G. Induction of embryogenesis versus caulogenesis on in vitro cultured sunflower (Helianthus annuus L.) immature zygotic embryos: Role of plant growth regulators. Plant Sci 1998;137:63-71. https://doi.org/10.1016/S0168-9452(98)00128-9

59. Rai MK, Shekhawat NS, Gupta AK, Phulwaria M, Ram K, Jaiswal U. The role of abscisic acid in plant tissue culture: A review of recent progress. Plant Cell Tissue Organ Cult 2011;106:179-90. https://doi.org/10.1007/s11240-011-9923-9

60. Shiota H, Satoh R, Watabe K, Harada H, Kamada H. C-ABI3, the carrot homolog 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 1998;39:1184-93. https://doi.org/10.1093/oxfordjournals.pcp.a029319

61. Shiota H, Kamada H. Acquisition of desiccation tolerance by cultured carrot cells upon ectopic expression of C-ABI3, a carrot homolog of ABI3. J Plant Physiol 2000;156:510-5. https://doi.org/10.1016/S0176-1617(00)80166-2

62. Ikeda-Iwai M, Umehara M, Kamada H. Embryogenesis related genes: its expression and roles during somatic and zygotic embryogenesis in carrot and Arabidopsis. Plant Biotechnol 2006;23:153-61. https://doi.org/10.5511/plantbiotechnology.23.153

63. Hatanaka T, Sawabe E, Azuma T, Uchida N, Yasuda T. The role of ethylene in somatic embryogenesis from leaf discs of Coffea canephora. Plant Sci 1995;107:199-204. https://doi.org/10.1016/0168-9452(95)04103-2

64. Chen JT, Chang WC. 1-aminocyclopropane-1-carboxylic acid enhanced direct somatic embryogenesis from Oncidium leaf cultures. Biol Plant 2003;46:455-8. https://doi.org/10.1023/A:1024307025893

65. Kepczynska E, Rudus I, Kepczynski J. Endogenous ethylene in indirect somatic embryogenesis of Medicago sativa L. Plant Growth Regul 2009;59:63-73. https://doi.org/10.1007/s10725-009-9388-6

66. Lu J, Vahala J, Pappinen A. Involvement of ethylene in somatic embryogenesis in scots pine (Pinus sylvestris L.). Plant Cell Tissue Organ Cult 2011;107:25-33. https://doi.org/10.1007/s11240-011-9952-4

67. Mauri PV, Manzanera JA. Somatic embryogenesis of holm oak (Quercus ilex L.): ethylene production and polyamine content. Acta Physiol Plant 2011;33:717-23. https://doi.org/10.1007/s11738-010-0596-5

68. El Meskaoui A, Tremblay FM. Involvement of ethylene in the maturation of black spruce embryogenic cell lines with different maturation capacities. J Exp Bot 2001;52:761-9. https://doi.org/10.1093/jexbot/52.357.761

69. Ptak A, El Tahchy A, Wyzgolik A, Henry M, Laurain-Mattar D. Effects of ethylene on somatic embryogenesis and galanthamine content in Leucojum aestivum L. cultures. Plant Cell Tissue Organ Cult 2010;102:61-7. https://doi.org/10.1007/s11240-010-9706-8

70. Mantiri FR, Kurdyukov S, Chen SK, Rose RJ. The transcription factor mtSERF1 may function as a nexus between stress and development in somatic embryogenesis in Medicago truncatula. Plant Signal Behav 2008;3:498-500. https://doi.org/10.4161/psb.3.7.6049

71. Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang XD, et al. The transcription factor mtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiol 2008;146:1622-36. https://doi.org/10.1104/pp.107.110379

72. Liu W, Hildebrand DF, Moore PJ, Collins GB. Expression of desiccation-induced and lipoxygenase genes during the transition from the maturation to the germination phases in soybean somatic embryos. Planta 1994;194:69-76. https://doi.org/10.1007/BF00201036

73. Liu W, Hildebrand DF, Grayburn WS, Philips GC, Collins GB. Effects of exogenous auxins on expression of lipoxygenases in cultured soybean embryos. Plant Physiol 1991;97:969-76. https://doi.org/10.1104/pp.97.3.969

74. Duncan DR, Kriz AL, Paiva R, Widholm JM. Globulin-1 gene expression in regenerable Zea mays (maize) callus. Plant Cell Reports 2003;21:684-9.

75. Brill LM, Evans CJ, Hirsch AM. Expression of MsLEC1- and MsLEC2-antisense genes in alfalfa plant lines causes severe developmental and reproductive abnormalities. Plant J 2001;25:453-61. https://doi.org/10.1046/j.1365-313x.2001.00979.x

76. Braybrook SA, Harada JJ. LECs go crazy in embryo development. Trends Plant Sci 2008;13:624-30. https://doi.org/10.1016/j.tplants.2008.09.008

77. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, et al. LEAFY COTYLEDON2 Encodes a B3 Domain Transcription Factor that Induces Embryo Development. Vol. 98. USA: Proceedings of the National Academy of Sciences; 2001. p. 11806-11. https://doi.org/10.1073/pnas.201413498

78. Ledwon A, Gaj MD. LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Reports 2009;28:1677-88. https://doi.org/10.1007/s00299-009-0767-2

79. Rashid SZ, Yamaji N, Kyo M. Shoot formation from root tip region: A developmental alteration by WUS in transgenic tobacco. Plant Cell Rep 2007;26:1449-55. https://doi.org/10.1007/s00299-007-0342-7

80. Harada JJ. Role of Arabidopsis leafy cotyledon genes in seed development. J Plant Physiol 2001;158:405-9. https://doi.org/10.1078/0176-1617-00351

81. Ledwon A, Gaj MD. LEAFY COTYLEDON1, FUSCA3 expression and auxin treatment in relation to somatic embryogenesis induction in Arabidopsis. Plant Growth Regul 2011;65:157-67. https://doi.org/10.1007/s10725-011-9585-y

82. Wang H, Caruso LV, Downie AB, Perry SE. The embryo MADS domain protein AGAMOUS-like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 2004;16:1206-19. https://doi.org/10.1105/tpc.021261

83. Thakare D, Tang W, Hill K, Perry SE. The MADS-domain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol 2008;146:1663-72. https://doi.org/10.1104/pp.108.115832

84. Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE. Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-like 15. Plant Physiol 2003;133:653-63. https://doi.org/10.1104/pp.103.023499

85. Dietz KJ, Vogel MO, Viehhauser A. AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 2010;245:3-14. https://doi.org/10.1007/s00709-010-0142-8

86. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box mediated gene expression. Plant Cell 2000;12:393-404. https://doi.org/10.1105/tpc.12.3.393

87. Tsuwamoto R, Yokoi S, Takahata Y. Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 2010;73:481-92. https://doi.org/10.1007/s11103-010-9634-3

88. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 2002;14:1737-49. https://doi.org/10.1105/tpc.001941

89. El Ouakfaoui S, Schnell J, Abdeen A, Colville A, Labb\é H, Han S, et al. Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 2010;74:313-26. https://doi.org/10.1007/s11103-010-9674-8

90. Srinivasan C, Liu Z, Heidmann I, Supena ED, Fukuoka H, Joosen R, et al. Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta 2007;225:341-51. https://doi.org/10.1007/s00425-006-0358-1

91. Deng W, Luo KM, Li ZG, Yang YW. A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci 2009;177:43-8. https://doi.org/10.1016/j.plantsci.2009.03.009

92. Heidmann I, de Lange B, Lambalk J, Angenent GC, Boutilier K. Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep 2011;30:1107-15. https://doi.org/10.1007/s00299-011-1018-x

93. Scott MP, Tamkun JW, Hartzell GW 3rd. The structure and function of the homeodomain. Biochim Biophys Acta 1989;989:25-48. https://doi.org/10.1016/0304-419X(89)90033-4

94. Meijer AH, Scarpella E, van Dijk EL, Qin L, Taal AJ, Rueb S, et al. Transcriptional repression by oshox1, a novel homeodomain leucine zipper protein from rice. Plant J 1997;11:263-76. https://doi.org/10.1046/j.1365-313X.1997.11020263.x

95. Kiyosue T, Shiota H, Higashi K, Kamada H, Shinozaki K. A chromo box gene from carrot (Daucus carota l.): Its cDNA structure and expression during somatic and zygotic embryogenesis. Biochim Biophys Acta 1998;1398:42-6. https://doi.org/10.1016/S0167-4781(98)00052-9

96. Hay A, Tsiantis M. KNOX genes: Versatile regulators of plant development and diversity. Development 2010;137:3153-65. https://doi.org/10.1242/dev.030049

97. Ma H, McMullen MD, Finer JJ. Identification of a homeobox-containing gene with enhanced expression during soybean (Glycine max L.) somatic embryo development. Plant Mol Biol 1994;24:465-73. https://doi.org/10.1007/BF00024114

98. Hjortswang HI, Larsson AS, Bharathan G, Bozhkov PV, von Arnold S, Vahala T. KNOTTED1-like homeobox genes of a gymnosperm, Norway spruce, expressed during somatic embryogenesis. Plant Physiol Biochem 2002;40:837-43. https://doi.org/10.1016/S0981-9428(02)01445-6

99. Larsson E, Sitbon F, von Arnold S. Differential regulation of knotted1- like genes during establishment of the shoot apical meristem in Norway spruce (Picea abies). Plant Cell Rep 2012;31:1053-60. https://doi.org/10.1007/s00299-011-1224-6

100. Belmonte MF, Tahir M, Schroeder D, Stasolla C. Overexpression of HBK3, a class I KNOX homeobox gene, improves the development of Norway spruce (Picea abies) somatic embryos. J Exp Bot 2007;58:2851-61. https://doi.org/10.1093/jxb/erm099

101. Arroyo-Herrera A, Gonzalez AK, Moo RC, Quiroz-Figueroa FR, Loyola-Vargas VM, Rodriguez-Zapata LC, et al. Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell Tissue Organ Cult 2008;94:171-80. https://doi.org/10.1007/s11240-008-9401-1

102. Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 2011;21:1277-81. https://doi.org/10.1016/j.cub.2011.07.001

103. Shibukawa T, Yazawa K, Kikuchi A, Kamada H. Possible involvement of DNA methylation on expression regulation of carrot LEC1 gene in its 5'-upstream region. Gene 2009;437:22-31. https://doi.org/10.1016/j.gene.2009.02.011

104. Yamamoto N, Kobayashi H, Togashi T, Mori Y, Kikuchi K, Kuriyama K, et al. Formation of embryogenic cell clumps from carrot epidermal cells is suppressed by 5-azacytidine, a DNA methylation inhibitor. J Plant Physiol 2005;162:47-54. https://doi.org/10.1016/j.jplph.2004.05.013

105. Tanaka M, Kikuchi A, Kamada H. The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 2008;146:149-61. https://doi.org/10.1104/pp.107.111674

106. Li H, Soriano M, Cordewener J, Mui-o JM, Riksen T, Fukuoka H, et al. The histone deacetylase inhibitor trichostatin A promotes totipotency in the male gametophyte. Plant Cell 2014;26:195-209. https://doi.org/10.1105/tpc.113.116491

107. Jones PL, Wolffe AP. Relationships between chromatic organization and DNA methylation in determining gene expression. Semin Cancer Biol 1999;9:339-47. https://doi.org/10.1006/scbi.1999.0134

108. Zhu HG, Tu LL, Jin SX, Xu L, Tan JF, Deng FL, et al. Analysis of genes differentially expressed during initial cellular dedifferentiation in cotton. Chin Sci Bull 2008;23:3666-76. https://doi.org/10.1007/s11434-008-0468-1

109. van Zyl L, Bozhkov PV, Clapham DH, Sederoff RR, von Arnold S. Up, down and up again is a signature global gene expression pattern at the beginning of gymnosperm embryogenesis. Gene Expr Patterns 2003;3:83-91. https://doi.org/10.1016/S1567-133X(02)00068-6

110. Willmann MR, Poethig RS. Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 2007;10:503-11. https://doi.org/10.1016/j.pbi.2007.07.004

111. Willmann MR, Mehalick AJ, Packer RL, Jenik PD. MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 2011;155:1871-84. https://doi.org/10.1104/pp.110.171355

112. Wu XM, Liu MY, Ge XX, Xu Q, Guo WW. Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 2011;233:495-505. https://doi.org/10.1007/s00425-010-1312-9

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