Somatic and zygotic embryos share common developmental features at the onset of plant embryogenesis

Acta Physiologiae Plantarum

Volumn 37, Issue 7, 2015, Pages

  Leljak Levanić, Dunja ^a   Mihaljević, Snježana ^b   Bauer, Nataša ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b RUDER BO KOVI INSTITUTE   (Croatia)

Author keywords

Cell wall; DNA methylation; Plant growth regulators; Somatic embryogenesis; Stress; Zygotic embryogenesis

Indexed keywords

TRACHEOPHYTA;

EID: 84930943194     PISSN: 01375881     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11738-015-1875-y     Document Type: Review

References (179)

1. Abrahamsson M, Valladares S, Larsson E, Clapham D, von Arnold S (2012) Patterning during somatic embryogenesis in Scots pine in relation to polar auxin transport and programmed cell death. Plant Cell Tiss Org Cult 109:391–400. doi:10.1007/s11240-011-0103-8
2. Achard P, Renou JP, Berthomé R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18:656–660
3. Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc’h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D (2009) Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. Plant J 57:626–644
4. Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, Grob S, Steimer A, Barann M, Klostermeier UC, Leblanc O, Vielle-Calzada JP, Rosenstiel P, Grimanelli D, Grossniklaus U (2011) Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145(5):707–719
5. Berger F, Grini PE, Schnittger A (2006) Endosperm: an integrator of seed growth and development. Curr Opin Plant Biol 9:664–670
6. Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16:S228–S245
7. Bobák M, Šamaj J, Hlinkovà E, Hlavačka A, Ovečka M (2004) Extracellular matrix in early stages of direct somatic embryogenesis in leaves of Drosera spathulata. Biol Plant 47:161–166
8. Borderies G, le Bechec M, Rossignol M, Lafitte C, Le Deunff E, Beckert M, Dumas C, Matthys-Rochon E (2004) Characterization of proteins secreted during maize microspore culture: arabinogalactan proteins (AGPs) stimulate embryo development. Eur J Cell Biol 83(5):205–212
9. Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang LM, Hattori J, Liu CM, van Lammeren AAM, Miki BLA, Custers JBM, Campagne MMV (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749
10. Braybrook SA, Stone SL, Park S, Bui AQ, Le BH et al (2006) Genes directly regulated by LEAFY COTYLEDONE2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci USA 103:3468–3473
11. Cao X (2003) Role of the DRM and CMT3 methyltransferases in RNAdirected DNA methylation. Curr Biol 13:2212–2217
12. Cao X, Jacobsen SE (2002a) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99:16491–16498
13. Cao X, Jacobsen SE (2002b) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144
14. Casson S, Spencer M, Walker K, Lindsey K (2005) Laser capture microdissection for the analysis of gene expression during embryogenesis of Arabidopsis. Plant J 42:111–123
15. Chandler JW, Cole M, Flier A, Grewe B, Werr W (2007) The AP2 transcription factors DORNROSCHEN and DORNROSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 134:1653–1662. doi:10.1242/dev.001016
16. Chapman A, Blervacq AS, Hendrix T, Slomianny C, Vasseur J, Hilbert JL (2000a) Cell wall differentiation during early somatic embryogenesis in plants. II. Ultrastructural study and pectin immunolocalisation on chicory embryos. Can J Bot 78:824–831. doi:10.1139/b00-060
17. Chapman A, Helleboid S, Blervacq AS, Vasseur J, Hilbert JL (2000b) Removal of the fibrillar network surrounding Cichorium somatic embryos using cytoskeleton inhibitors: analysis of proteic components. Plant Sci 150:103–114. doi:10.1016/S0168-9452(99)00185-5
18. Chapman A, Blervacq AS, Vasseur J, Hilbert JL (2000c) Arabinogalactan proteins in Chichorium somatic embryogenesis: effect of β-glucosyl Yariv reagent and epitope localisation during embryo development. Planta 211:305–314
19. Clark JK, Sheridan WF (1991) Isolation and characterization of 51 embryo-specific mutations of Maize. Plant Cell 3:935–995
20. Coutos-Thevenot P, Maes O, Jouenne T, Mauro MC, Boulay M, Deloire A, Guern J (1992) Extracellular protein patterns of grapevine cell suspensions in embryogenic and non-embryogenic situations. Plant Sci 86(2):137–145
21. Curaba J, Moritz T, Blervaque R, Parcy F, Raz V, Herzog M, Vachon G (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol 136:3660–3669
22. De Jong AJ, Cordewener J, LoSchiavo F, Terzi M, Vandekerckhove J, VanKammen A, De Vries SC (1992) A carrot somatic embryo mutant is rescued by chitinase. Plant Cell 4(4):425–433
23. Decout E, Dubois T, Guedira M, Dubois J, Audran JC, Vasseur J (1994) Role of temperature as a triggering signal for organogenesis or somatic embryogenesis in wounded leaves of chicory cultured in vitro. J Exp Bot 45(281):1859–1865
24. De Jong AJ, Schmidt EDL, DeVries SC (1993) Early events in higher-plant embryogenesis. Plant Mol Biol 22:367–377
25. DeVries SC, Booij H, Janssen R, Vogels R, Saris L, LoSchiavo F, Terzi M, VanKammen A (1998) Carrot somatic embryogenesis depends on the phytohormone-controlled presence of correctly glicosylated proteins. Gene Develop 2:462–476
26. Dickinson H, Scott R (2002) DEMETER, goddess of the harvest, activates maternal MEDEA to produce the perfect seed. Mol Cell 10:5–7
27. Dodeman VL, Ducreux G, Kreis M (1997) Zygotic embryogenesis versus somatic embryogenesis. J Exp Bot 48(313):1493–1509. doi:10.1093/jxb/48.8.1493
28. Dubois T, Guedira M, Dubois J, Vasseur J (1990) Direct somatic embryogenesis in roots of Cichorium—is callose an early marker. Ann Bot 65(5):539–545
29. Dubois T, Guedira M, Dubois J, Vasseur J (1991) Direct somatic embryogenesis in leaves of Cichorium—a histological and SEM study of early stages. Protoplasma 162(2–3):120–127
30. Dyachock 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(2):523–533. doi:10.1104/pp.128.2.523
31. Eckardt NA (2001) Auxin and the power of the proteasome in plants. Plant Cell 13:2161–2163
32. Fehér A (2005) Why somatic plant cells start to form embryos? In: Mujib A, Samaj J (eds) Somatic embryogenesis, plant cell monographs (2). Springer-Verlag, Berlin, pp 85–101. doi:10.1007/7089_019
33. Fehér A, Taras P, Pasternak T, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tiss Org Cult 74(3):201–228. doi:10.1023/A:1024033216561
34. Finnegan EJ, Kovac KA (2000) Plant DNA methyltransferases. Plant Mol Biol 43:189–201
35. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis results in abnormal plant development. Proc Natl Acad Sci USA 93:8449–8454
36. Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12
37. Gaj MD, Zhang SB, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988
38. Gaj MD, Trojanowska A, Ujczak A, Mędrek M, Kozioł A, Garbaciak B (2006) Hormone—response mutants of Arabidopsis thaliana (L.) Heynh. impaired in somatic embryogenesis. Plant Growth Regul 49(2–3):183–197
39. Gavish H, Vardi A, Fluhr R (1991) Extracellular proteins and early embryo development in Citrus nucellar cell cultures. Physiol Plant 82(4):606–616. doi:10.1111/j.1399-3054.1991.tb02954.x
40. Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7:373–385
41. Gleeson PA, Mcnamara M, Wettenhall REH, Stone BA, Fincher GB (1989) Characterization of the hydroxyproline-rich protein core of an arabinogalactan-protein secreted from suspension-cultured Lolium multiflorum (Italian ryegrass) endosperm cells. Biochem J 264(3):857–862
42. Gliwicka M, Nowak K, Balazadeh S, Mueller-Roeber B, Gaj MD (2013) Extensive modulation of the transcription factor transcriptome during somatic embryogenesis in Arabidopsis thaliana. PLoS One 8(7):e69261. doi:10.1371/journal.pone.0069261
43. Gomez LD, Baud S, Gilday A, Li Y, Graham IA (2006) Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J 46:69–84
44. Goralski G, Lafitte C, Bouazza L, Matthys-Rochon E, Przywara L (2002) Influence of sugars on isolated microspore development in maize (Zea mays L.). Acta Biol Crac Ser Bot 44:203–212
45. Grant-Downton RT, Dickinson HG (2005) Epigenetics and its implications for plant biology. The epigenetic network in plants. Ann Bot 96(7):1143–1164
46. Gray-Mitsumune M, O’Brien M, Bertrand C, Tebbji F, Nantel A, Matton DP (2006) Loss of ovule identity induced by overexpression of the fertilization-related kinase 2 (ScFRK2), a MAPKKK from Solanum chacoense. J Exp Bot 57:4171–4187
47. Griffith ME, Mayer U, Capron A, Ngo QA, Surendrarao A, McClinton R, Jurgens G, Sundaresan V (2007) The TORMOZ gene encodes a nucleolar protein required for regulated division planes and embryo development in Arabidopsis. Plant Cell 19:2246–2263
48. Grosset J, Marty I, Chartier Y, Meyer Y (1990) mRNAs newly synthetized by tobacco mesophyll protoplasts are wound-inducible. Plant Mol Biol 15:485–496
49. Hadfi K, Speth V, Neuhaus G (1998) Auxin-induced developmental patterns in Brassica juncea embryos. Development 125:879–887
50. Harada H, Kiyosue T, Kamada H, Kobayashi K (1990) Stress induced carrot somatic embryogenesis and their application to synthetic seeds. In: Sangwan RS, Sangwan-Norreel BS (eds) The impact of biotechnology in agriculture. Kluwer Academic, Dordrecht, pp 129–157
51. Harmon AC, Gribskov M, Gubrium E, Harper JF (2001) The CDPK superfamily of protein kinases. New Phytol 151:175–183. doi:10.1046/j.1469-8137.2001.00171.x
52. Helleboid S, Bauw G, Belingheri L, Vasseur J, Hilbert JL (1998) Extracellular beta-1,3-glucanases are induced during early somatic embryogenesis in Cichorium. Planta 205(1):56–63
53. Helleboid S, Chapman A, Hendriks T, Inze D, Vasseur J, Hilbert JL (2000) Cloning of beta-1,3-glucanases expressed during Cichorium somatic embryogenesis. Plant Mol Biol 42(2):377–386
54. Hilbert JL, Dubois T, Vasseur J (1992) Detection of embryogenesis-related proteins during somatic embryo formation in Cichorium. Plant Physiol Bioch 30(6):733–741
55. Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 97:2405–2407
56. Holm PB, Knudsen S, Mouritzen P, Negri D, Olsen FL, Roue C (1994) Regeneration of fertile barley plants from mechanically isolated protoplasts of the fertilized egg cell. Plant Cell 6(4):531–543
57. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, Zilberman D (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451–1454
58. Ikeda-Iwai M, Umehara M, Satoh S, Kamada H (2003) Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J 34(1):107–113
59. Ingouff M, Jullien PE, Berger F (2006) The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18(12):3491–3501
60. Ingouff M, Rademacher S, Holec S, Soljic L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20(23):2137–2143
61. Inui H, Yamaguchi Y, Ishigami Y, Kawaguchi S, Yamada T, Ihara H, Hirano S (1996) Three extracellular chitinases in suspension-cultured rice cells elicited by N-acetylchito-oligosaccharides. Biosci Biotech Bioch 60(12):1956–1961
62. Ivanova A, Velcheva M, Denchev P, Atanassov A, Van Onckelen H (1994) Endogenous hormone levels during direct somatic embryogenesis in Medicago falcata. Physiol Plant 92:85–89. doi:10.1111/j.1399-3054.1994.tb06658.x
63. Jensen WA (1968) Cotton embryogenesis—Zygote. Planta 79(4):346–366
64. Jiménez VM (2005) Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis. Plant Growth Regul 47(2–3):91–110. doi:10.1007/s10725-005-3478-x
65. Jiménez VM, Thomas C (2005) Participation of plant hormones in determination and progression of somatic embryogenesis. In: Mujib A, Samaj J (eds) Somatic embryogenesis, plant cell monographs (2). Springer-Verlag, Berlin, pp 103–118. doi:10.1007/7089_034
66. Jin FY, Hu LS, Yuan DJ, Xu J, Gao WH, He LR, Yang XY, Zhang XL (2013) Comparative transcriptome analysis between somatic embryos (SEs) and zygotic embryos in cotton: evidence for stress response functions in SE development. Plant Biotech J 12:161–173
67. Kakutani T, Kato M, Kinoshita T, Miura A (2004) Control of development and transposon movement by DNA methylation in Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol 69:139–143
68. Kamada H, Kobayashi K, Kiyosue T, Harada H (1989) Stress-induced somatic embryogenesis in carrot and its application to synthetic seed production. Vitro Cell Dev Biol Plant 25(12):1163–1166
69. Kamada H, Ishikawa K, Saga H, Harada H (1993) Induction of somatic embryogenesis in carrot by osmotic stress. Plant Tissue Cult Lett 10(1):38–44
70. Kamada H, Tachikawa Y, Saitou T, Harada H (1994) Heat stresses induction of carrot somatic embryogenesis. Plant Tissue Cult Lett 11(3):229–232
71. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122
72. Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell 18(10):2733–2748
73. Karami O, Saidi A (2010) The molecular basis for stress-induced acquisition of somatic embryogenesis. Mol Biol Rep 37:2493–2507
74. Kieffer M, Neve J, Kępiński S (2010) Defining auxin response contexts in plant development. Curr Opin Plant Biol 13:12–20. doi:10.1016/j.pbi.2009.10.006
75. Kikuchi A, Sanuki N, Higashi K, Koshiba T, Kamada H (2006) Abscisic acid and stress treatment are essential for the acquisition of embryogenic competence by carrot somatic cells. Planta 223(4):637–645
76. Kitamiya E, Suzuki S, Sano T, 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
77. Kiyosue T, Satoh S, Kamada H, Harada H (1993) Somatic embryogenesis in higher plants. J Plant Res 3:75–82 (special issue)
78. Ko S, Thitamadee S, Yang H, Eun C-H, Sage-ono K, Higashi K, Satoh S, Kamada H (2001) Comparison and characterization of cis-regulatory regions in some embryo-specific and ABA-responsive carrot genes. DcECPs. Plant Biotech 18(1):45–54
79. Koltunow AM, Bicknell RA, Chaudhury AM (1995) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiol 108:1345–1352
80. Konieczny R, Bohdanowicz J, Czaplicki AZ, Przywara L (2005) Extracellular matrix surface network during plant regeneration in wheat anther culture. Plant Cell Tiss Org Cult 83:201–208. doi:10.1007/s11240-005-5771-9
81. Kragh KM, Jacobsen S, Mikkelsen JD, Nielsen KA (1991) Purification and characterization of 3 chitinases and one beta-1,3-glucanase accumulating in the medium of cell-suspension cultures of barley (Hordeum vulgare L). Plant Sci 76(1):65–77. doi:10.1016/0168-9452(91)90219-X
82. Kranz E, Bautor J, Lorz H (1991) In vitro fertilization of single, isolated gametes of maize mediated by electrofusion. Sex Plant Reprod 4(1):12–16. doi:10.1007/BF00194565
83. Kreuger MV, Van Holst G-J (1996) Arabinogalactan proteins and plant differentiation. Plant Mol Biol 30:1077–1086
84. Kumlehn J, Lorz H, Kranz E (1998) Differentiation of isolated wheat zygotes into embryos and normal plants. Planta 205(3):327–333
85. Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18
86. Lahmy S, Guilleminot J, Schmit AC, Pelletier G, Chaboute ME, Devic M (2007) QQT proteins colocalize with microtubules and are essential for early embryo development in Arabidopsis. Plant J 50:615–626
87. Lau S, Slane D, Herud O, Kong J, Jurgens G (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Annu Rev Plant Biol 63:483–506
88. Lee EK, Cho DY, Soh WY (2001) Enhanced production and germination of somatic embryos by temporary starvation in tissue cultures of Daucus carota. Plant Cell Rep 20:408–415. doi:10.1007/s002990100338
89. Legrand S, Hendriks T, Hilbert JL, Quillet MC (2007) Characterisation of expressed sequence tags obtained by SSH during somatic embryogenesis in Cichorium intybus L. BMC Plant Biol 7:27–33
90. Leljak D, Jelaska S (1995) Callus formation and somatic embryo production in pumpkin Cucurbita pepo L. explants on hormone-free medium. Period Biol 97(4):327–332
91. Leljak-Levanić D, Bauer N, Mihaljević S, Jelaska S (2004a) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23(3):120–127
92. Leljak-Levanić D, Bauer N, Mihaljević S, Jelaska S (2004b) Somatic embryogenesis in pumpkin (Cucurbita pepo L.): control of somatic embryo development by nitrogen compounds. J Plant Physiol 161(2):229–236
93. Leyser O (2002) Molecular genetics of auxin signaling. Ann Rev Plant Biol 53:377–398
94. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080
95. Liu C-M, Xu Z, Chua N-H (1993) Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5(6):621–630
96. Liu NY, Zhang ZF, Yang WC (2008) Isolation of embryo-specific mutants in Arabidopsis: genetic and phenotypic analysis. Methods Mol Biol (Clifton NJ) 427:101–109
97. Lo Schiavo F, Pitto L, Giuliano G, Torti G, Nutironchi V, Marazziti D, Vergara R, Orselli S, 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(3):325–331. doi:10.1007/BF00305823
98. Long TA, Benfey PN (2006) Transcription factors and hormones: new insights into plant cell differentiation. Curr Opin Cell Biol 18:710–714. doi:10.1016/j.ceb.2006.09.004
99. Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205
100. Luerssen K, Kirik V, Herrmann P, Misera S (1998) FUSCA3 encodes a protein with a conserved VP1/ABI3-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764
101. Lukowitz W, Mayer U, Jurgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84:61–71
102. Ma H, Sundaresan V (2010) Development of flowering plant gametophytes. Curr Top Dev Biol 91:379–412
103. Maheswaran G, Williams EG (1985) Origin and development of somatic embryoids formed directly on immature embryos of Trifolium repens in vitro. Ann Bot 56(5):619–630
104. Malinowski R, Filipecki M (2002) The role of cell wall in plant embryogenesis. Cell Mol Biol Lett 7(4):1137–1151
105. Massonneau A, Coronado MJ, Audran A, Bagniewska A, Mol R, Testillano PS, Goralski G, Dumas C, Risueno MC, Matthys-Rochon E (2005) Multicellular structures developing during maize microspore culture express endosperm and embryo-specific genes and show different embryogenic potentialities. Eur J Cell Biol 84(7):663–675
106. Matthys-Rochon E (2005) Secreted molecules and their role in embryo formation in plants: a mini-review. Acta Biol Cracov Ser Bot 47(1):23–29
107. McCabe PF, Valentine TA, Forsberg LS, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9(12):2225–2241
108. McElver J, Tzafrir I, Aux G, Rogers R, Ashby C, Smith K, Thomas C, Schetter A, Zhou Q, Cushman MA, Tossberg J, Nickle T, Levin JZ, Law M, Meinke D, Patton D (2001) Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics 159:1751–1763
109. Meinke DW (1985) Embryo-lethal mutants of Arabidopsis thaliana: analysis of mutants with a wide range of lethal phases. Theor Appl Genet 69:543–552
110. Meinke DW, Sussex IM (1979) Embryo-lethal mutants of Arabidopsis thaliana: a model system for genetic analysis of plant embryo development. Dev Biol 72:50–61
111. Meinke D, Muralla R, Sweeney C, Dickerman A (2008) Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci 13(9):483–491
112. Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62(11):3713–3725
113. Mihaljević S, Radić S, Bauer N, Garic R, Horvat G, Leljak-Levanić D, Jelaska S (2011) Ammonium-related metabolic changes affect somatic embryogenesis in pumpkin (Cucurbita pepo L.). J Plant Physiol 168(16):1943–1951
114. Muralla R, Lloyd J, Meinke D (2011) Molecular foundations of reproductive lethality in Arabidopsis thaliana. PLoS One 6(12):e28398. doi:10.1371/journal.pone.0028398
115. Nakagawa H, Saijyo T, Yamauchi N, Shigyo M, Kako S, Ito A (2001) Effects of sugars and abscisic acid on somatic embryogenesis from melon (Cucumis melo L.) expanded cotyledon. Sci Hort 90:85–92. doi:10.1016/S0304-4238(00)00259-4
116. Neuhaus J-M (1999) Plant chitinases. In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 77–105
117. Nielsen KA, Hansen IB (1992) Appearance of extracellular proteins associated with somatic embryogenesis in suspension cultures of barley (Hordeum vulgare L.). J Plant Physiol 139(4):489–497. doi:10.1016/S0176-1617(11)80500-6
118. Nishiwaki M, Fujino K, Koda Y, Masuda K, 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. Nodine MD, Bartel DP (2012) Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482(7383):94–120
120. Nolan KE, Saeed NA, Rose RJ (2006) The stress kinase gene MtSK1 in Medicago truncatula with particular reference to somatic embryogenesis. Plant Cell Rep 25:711–722
121. Paire A, Devaux P, Lafitte C, Dumas C, Matthys-Rochon E (2003) Proteins produced by barley microspores and their derived androgenic structures promote in vitro zygotic maize embryo formation. Plant Cell Tiss Org Cult 73(2):167–176. doi:10.1023/A:1022805623167
122. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6:1567–1582
123. Pasternak T, Potters G, Caubergs G, Jansen MAK (2005) Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level. J Exp Bot 56(418):1991–2001. doi:10.1093/jxb/eri196
124. Patnaik D, Mahalakshmi A, Khurana P (2005) Effect of water stress and heavy metals on induction of somatic embryogenesis in wheat leaf base cultures. Indian J Exp Biol 43(8):740–745
125. Phillips RL, Kaeppler SM, Peschke WM (1990) Do we understand somaclonal variation? In: Nijkamp HJJ, Van Der Plas LHW, Van Aartrijk J (eds) Progress in plant cellular and molecular biology. Kluwer, Dordrecht, pp 131–141. doi:10.1007/978-94-009-2103-0_19
126. Pillot M, Baroux C, Vazquez MA, Autran D, Leblanc O, Vielle-Calzada JP, Grossniklaus U, Grimanelli D (2010) Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22(2):307–320
127. Piyatrakul P, Putranto RA, Martin F, Rio M, Dessailly F et al (2012) Some ethylene biosynthesis and AP2/ERF genes reveal a specific pattern of expression during somatic embryogenesis in Hevea brasiliensis. BMC Plant Biol 12:244. doi:10.1186/1471-2229-12-244
128. Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12(3):98–105. doi:10.1016/j.tplants.2007.01.004
129. Puigderrajols P, Jofre A, Mir G, Pla M, Verdaguer D, Huguet G, Molinas M (2002) Developmentally and stress-induced small heat shock proteins in cork oak somatic embryos. J Exp Bot 53:1445–1452
130. Rademacher EH, Möller B, Lokerse AS, Llavata-Peris CI, van den Berg W et al (2011) A cellular expression map of the ArabidopsisAUXIN RESPONSE FACTOR gene family. Plant J 68:597–606. doi:10.1111/j.1365-313x.2011.04710.x
131. Raghavan V (2004) Role of 2,4-dichlorophenoxyacetic acid (2,4-D) in somatic embryogenesis 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
132. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646
133. Rumyantseva NI, Samaj J, Ensikat HJ, Salnikov VV, Kostyukova YA, Baluska F, Volkman D (2003) Changes in the extracellular matrix surface network during cyclic reproduction of proembryogenic cell complex in the Fagopyrum tataricum (L.) Gaertn callus. Dokl Biol Sci 391:375–378
134. Sabeli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26
135. Šamaj J, Bobák M, Blehová A, Krištin J, Auxtová-Šamajová O (1995) Developmental SEM observations on an extracellular matrix in embryogenic calli of Drosera rotundifolia and Zea mays. Protoplasma 186:45–49. doi:10.1007/BF01276934
136. Šamaj J, Baluška F, Bobák M, Volkmann D (1999) Extracellular matrix surface network of embryogenic units of friable maize callus contains arabinogalactan-proteins recognized by monoclonal antibody JIM4. Plant Cell Rep 18:369–374
137. Satoh S, Kamada H, Harada H, Fujii T (1986) Auxin-controlled glycoprotein release into medium of embryogenic carrot cells. Plant Physiol 81:931–933
138. Scanlon MJ, Stinard PS, James MG, Myers AM, Robertson DS (1994) Genetic analysis of 63 mutations affecting maize kernel development isolated from Mutator stocks. Genetics 136:281–294
139. Schmidt EDL, De Jong AJ, De Vries SC (1994) Signal molecules involved in plant embryogenesis. Plant Mol Biol 26:1305–1313
140. Schoft VK, Chumak N, Choi Y et al (2011) Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc Natl Acad Sci USA 108:8042–8047
141. Sharma VK, Ramirez J, Fletcher JC (2003) The Arabidopsis CLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Mol Biol 51(3):415–425
142. Sharma SK, Millam S, Hedley PE, McNicol J, Bryan GJ (2008) Molecular regulation of somatic embryogenesis in potato: an auxin led perspective. Plant Mol Biol 68:185–201
143. Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2(5):410–418
144. Shiota H, Satoh R, K-i Watabe, Harada H, Kamada H (1998) C-ABI3, the carrot homologue of the Arabidopsis ABI3, is expressed during both zygotic and somatic embryogenesis and functions in the regulation of embryo-specific ABA-inducible genes. Plant Cell Physiol 39(11):1184–1193
145. Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436. doi:10.1016/s1369-5266(02)00289-3
146. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L et al (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811. doi:10.1073/pnas.201413498
147. Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J et al (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci USA 105:3151–3156
148. Strauss E (1998) When walls can talk, plant biologists listen. Science 282(5386):28–29. doi:10.1126/science.282.5386.28
149. Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59:448–460. doi:10.1111/j.1365-313X.2009.03880.x
150. Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471
151. Svetek J, Yadav MP, Nothnagel EA (1999) Presence of a glycosylphosphatidylinositol lipid anchor on rose arabinogalactan proteins. J Biol Chem 274(21):14724–14733
152. Tao L, Yang Y, Wang Q, You X (2012) Callose deposition is required for somatic embryogenesis in plasmolyzed Eleutherococcus senticosus zygotic embryos. Int J Mol Sci 13:14115–14126
153. Thibaud-Nissen F, Shealy RT, Khanna A, Vodkin LO (2003) Clustering of microarray data reveals transcript patterns associated with somatic embryogenesis in soybean. Plant Physiol 132:118–136. doi:10.1104/pp.103.019968
154. Thomas C, Bronner R, Molinier J, Prinsen E, van Onckelen H, Hahne G (2002) Immuno-cytochemical localization of indole-3-acetic acid during induction of somatic embryogenesis in cultured sunflower embryos. Planta 215:577–583
155. To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18:1642–1651
156. Trigiano RN, Gray DJ, Conger BV, McDaniel JK (1989) Origin of direct somatic embryos from cultured leaf segments of Dactylis glomerata. Bot Gaz 150:72–77
157. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, Sweeney TC, McElver J, Aux G, Patton D, Meinke D (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135:1206–1220
158. Vaillant I, Paszkowski J (2007) Role of histone and DNA methylation in gene regulation. Curr Opin Plant Biol 10(5):528–533
159. Van Hengel AJ, van Kammen A, de Vries SC (2002) A relationship between seed development, arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiol Plant 114(4):637–644
160. Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252
161. Vidaurre DP, Ploense S, Krogan NT, Berleth T (2007) AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134:2561–2567
162. Vögeli-Lange R, Fründt C, Hart CM, Beffa R, Nagy F, Meins F Jr (1994) Evidence for a role of β-1,3-glucanase in dicot seed germination. Plant J 5:273–278
163. Weijers D, Jurgens G (2005) Auxin and embryo axis formation: the ends in sight? Curr Opin Plant Biol 8:32–37
164. Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614
165. Williams EG, Knox RB, Kaul V, Rouse JL (1984) Post-pollination callose development in ovules of rhododendron and ledum (Ericaceae)—zygote special wall. J Cell Sci 69:127–135
166. Wiweger M, Farbos I, Ingouff M, Lagercrantz U, von Arnold S (2003) Expression of Chia4- Pa chitinase genes during somatic and zygotic embryo development in Norway spruce (Picea abies): similarities and differences between gymnosperm and angiosperm class IV chitinases. J Exp Bot 54(393):2691–2699
167. Wójcikowska B, Jaskóła K, Gąsiorek P, Meus M, Nowak K, Gaj MD (2013) LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta 238(3):425–440
168. Wu C-T, Leubner-Metzger G, Meins F Jr, Bradford KJ (2001) Class I β-1,3-glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiol 1261:1299–1313. doi:10.1104/pp.126.3.1299
169. Xiang DQ, Venglat P, Tibiche C, Yang H, Risseeuw E, Cao YG, Babic V, Cloutier M, Keller W, Wang E, Selvaraj G, Datla R (2011) Genome-wide analysis reveals gene expression and metabolic network dynamics during embryo development in Arabidopsis. Plant Physiol 156(1):346–356
170. Xiao WY, Custard KD, Brown RC, Lemmon BE, Harada JJ, Goldberg RB, Fischer RL (2006) DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18(4):805–814
171. Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell 16(1):133–141
172. Yamamoto N, Kobayashi H, Togashi T, Mori Y, Kikuchi K, Kuriyama K, 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
173. Yang XY, Zhang XL (2010) Regulation of somatic embryogenesis in higher plants. Critic Rev Plant Sci 29(1):36–57
174. Yang WC, Shi DQ, Chen YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108
175. Yang X, Zhang X, Yuan D, Jin F, Zhang Y, Xu J (2012) Transcript profiling reveals complex auxin signalling pathway and transcription regulation involved in dedifferentiation and redifferentiation during somatic embryogenesis in cotton. BMC Plant Biol 12:110. doi:10.1186/1471-2229-12-110
176. You XL, Yi JS, Choi YE (2006) Cellular change and callose accumulation in zygotic embryos of Eleutherococcus senticosus caused by plasmolyzing pretreatment result in high frequency of single-cell-derived somatic embryogenesis. Protoplasma 227(2–4):105–112
177. Zeng F, Zhang X, Cheng L, Hu L, Zhu L, Cao J, Guo X (2007) A draft gene regulatory network for cellular totipotency reprogramming during plant somatic embryogenesis. Genomics 90(5):620–628
178. Zimmerman JL (1993) Somatic embryogenesis - a model for early development in higher-plants. Plant Cell 5:1411–1423
179. Zuo JR, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359