Abstract
It is widely believed that all cells of a plant are totipotent and can regenerate the whole organism. This view is supported by uncountable experimental observations demonstrating the regrowth of whole plants from various explants, even from single cells. However, recent investigations have demonstrated that plant regeneration may proceed via transdifferentiation of meristems or root meristem-like callus tissues due to adult stem cells present all over the plants. These pathways do not start from single totipotent cells. There is a strong argument for plant cell totipotency, however, and that is somatic embryogenesis. During this process, differentiated somatic cells change their fate to develop into an embryo. Animal embryos can develop only from the totipotent zygote and its direct descendants (this cell state can also be artificially produced by injecting a somatic cell nucleus into an egg cell cytoplasm during cloning). Plant cells have to be induced to start somatic embryogenesis and not all of them are competent to respond properly to the induction. In conclusion, plant cells cannot be considered as totipotent per se, but some of them can regain totipotency under appropriate conditions. In addition, accumulating evidence supports the view that even somatic embryo development can follow various initial steps not necessarily requiring cellular totipotency. Although, there are experimental observations to support the progression of somatic embryogenesis through a zygote-like state in certain experimental systems, in other instances the reorganization of several cells into an embryo was described. The direct release/induction of the embryo development program in vegetative plant cells may represent a third pathway of somatic embryo development. In this chapter, a brief literature review is provided to support the above view on plant cell totipotency as well as on the various ways to start somatic embryogenesis.
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References
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. doi:10.1111/j.1365-313X.2008.03715.x
Bai B, Su YH, Yuan J, Zhang XS (2013) Induction of somatic embryos in Arabidopsis requires local YUCCA expression mediated by the down-regulation of ethylene biosynthesis. Mol Plant 6:1247–1260. doi:10.1093/mp/sss154
Cinalli RM, Rangan P, Lehmann R (2008) Germ cells are forever. Cell 132:559–562. doi:10.1016/j.cell.2008.02.003
de Almeida M, de Almeida CV, Mendes Graner E et al (2012) Pre-procambial cells are niches for pluripotent and totipotent stem-like cells for organogenesis and somatic embryogenesis in the peach palm: a histological study. Plant Cell Rep 31:1495–1515. doi:10.1007/s00299-012-1264-6
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
Elhiti M, Tahir M, Gulden RH et al (2010) Modulation of embryo-forming capacity in culture through the expression of Brassica genes involved in the regulation of the shoot apical meristem. J Exp Bot 61:4069–4085. doi:10.1093/jxb/erq222
Fehér A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta-Gene Regul Mech 1849:385–402. doi:10.1016/j.bbagrm.2014.07.005
Fehér A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tiss Org 74:201–228. doi:10.1023/A:1024033216561
Feng X, Zilberman D, Dickinson H (2013) A conversation across generations: soma-germ cell crosstalk in plants. Dev Cell 24:215–225. doi:10.1016/j.devcel.2013.01.014
Gaj MD (2001) Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana. Plant Cell Tiss Org 64:39–46. doi:10.1023/A:1010679614721
Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988. doi:10.1007/s00425-005-0041-y
Gambino G, Minuto M, Boccacci P et al (2011) Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot 62:1089–1101. doi:10.1093/jxb/erq349
Garcês HMP, Champagne CEM, Townsley BT et al (2007) Evolution of asexual reproduction in leaves of the genus Kalanchoë. Proc Natl Acad Sci (USA) 104:15578–15583. doi:10.1073/pnas.0704105104
Grafi G (2004) How cells dedifferentiate: a lesson from plants. Dev Biol 268:1–6. doi:10.1016/j.ydbio.2003.12.027
Grafi G, Chalifa-Caspi V, Nagar T et al (2011a) Plant response to stress meets dedifferentiation. Planta 233:433–438. doi:10.1007/s00425-011-1366-3
Grafi G, Florentin A, Ransbotyn V, Morgenstern Y (2011b) The stem cell state in plant development and in response to stress. Front Plant Sci 2:53. doi:10.3389/fpls.2011.00053
Guzzo F, Baldan B, Mariani P et al (1994) Studies on the origin of totipotent cells in explants of Daucus carota L. J Exp Bot 45:1427–1432. doi:10.1093/jxb/45.10.1427
Haecker A, Gross-Hardt R, Geiges B et al (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668. doi:10.1242/dev.00963
Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J Plant Physiol 158:405–409. doi:10.1078/0176-1617-00351
Henderson JT, Li H-C, Rider SD et al (2004) PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134:995–1005. doi:10.1104/pp.103.030148
Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54. doi:10.1111/j.1469-8137.2008.02437.x
Ikeda M, Umehara M, Kamada H (2006) Embryogenesis-related genes; its expression and roles during somatic and zygotic embryogenesis in carrot and Arabidopsis. Plant Biotechnol 23:153–161. doi:10.5511/plantbiotechnology.23.153
Ikeda-Iwai M (2002) Establishment of a reproducible tissue culture system for the induction of Arabidopsis somatic embryos. J Exp Bot 53:1575–1580. doi:10.1093/jxb/erf006
Ikeda-Iwai M, Umehara M, Satoh S, Kamada H (2003) Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J 34:107–114. doi:10.1046/j.1365-313X.2003.01702.x
Ikeuchi M, Iwase A, Rymen B et al (2015) PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis. Nat Plants 1:15089. doi:10.1038/nplants.2015.89
Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. doi:10.1105/tpc.113.116053
Iwase A, Mitsuda N, Koyama T et al (2011a) The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol 21:508–514. doi:10.1016/j.cub.2011.02.020
Iwase A, Ohme-Takagi M, Sugimoto K (2011b) WIND1: a key molecular switch for plant cell dedifferentiation. Plant Signal Behav 6:1943–1945. doi:10.4161/psb.6.12.18266
Koltunow A (2012) Apomixis. In: Encyclopedia of Life Sciences, eLS. John Wiley & Sons, Ltd, Chichester. doi:10.1002/9780470015902.a0002035.pub2
Kőszegi D, Johnston AJ, Rutten T et al (2011) Members of the RKD transcription factor family induce an egg cell-like gene expression program. Plant J 67:280–291. doi:10.1111/j.1365-313X.2011.04592.x
Laux T (2003) The stem cell concept in plants. Cell 113:281–283. doi:10.1016/S0092-8674(03)00312-X
Liu Y, Li X, Zhao J et al (2015) Direct evidence that suspensor cells have embryogenic potential that is suppressed by the embryo proper during normal embryogenesis. Proc Natl Acad Sci USA. 112:12432–12437. doi:10.1073/pnas.1508651112
Lotan T, Ohto M, Yee KM et al (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205. doi:10.1016/S0092-8674(00)81463-4
Mordhorst AP, Hartog MV, El Tamer MK et al (2002) Somatic embryogenesis from Arabidopsis shoot apical meristem mutants. Planta 214:829–836. doi:10.1007/s00425-001-0700-6
Mordhorst AP, Voerman KJ, Hartog MV et al (1998) Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. Genetics 149:549–563
Nishiwaki M, Fujino K, Koda Y et al (2000) Somatic embryogenesis induced by the simple application of abscisic acid to carrot (Daucus carota L.) seedlings in culture. Planta 211:756–759. doi:10.1007/s004250000387
Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–1689. doi:10.1126/science.1167324
Palovaara J, Hakman I (2008) Conifer WOX-related homeodomain transcription factors, developmental consideration and expression dynamic of WOX2 during Picea abies somatic embryogenesis. Plant Mol Biol 66:533–549. doi:10.1007/s11103-008-9289-5
Palovaara J, Hallberg H, Stasolla C, Hakman I (2010) Comparative expression pattern analysis of WUSCHEL-related homeobox 2 (WOX2) and WOX8/9 in developing seeds and somatic embryos of the gymnosperm Picea abies. New Phytol 188:122–135. doi:10.1111/j.1469-8137.2010.03336.x
Pennell RI, Janniche L, Kjellbom P et al (1991) Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3:1317–1326. doi:10.1105/tpc.3.12.1317
Radoeva T, Weijers D (2014) A roadmap to embryo identity in plants. Trends Plant Sci 1–8. doi:10.1016/j.tplants.2014.06.009
Rider SD, Henderson JTJ, Dean Rider S et al (2003) Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J 35:33–43. doi:10.1046/j.1365-313X.2003.01783.x
Rose RJ, Mantiri FR, Kurdyukov S, et al (2010) Developmental biology of somatic embryogenesis. In: Pua EC, Davey MR (eds) Plant developmental biology-biotechnological perspectives. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 3–26. doi:10.1007/978-3-642-04670-4_1
Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062
Seydoux G, Braun RE (2006) Pathway to totipotency: lessons from germ cells. Cell 127:891–904. doi:10.1016/j.cell.2006.11.016
Smertenko A, Bozhkov PV (2014) Somatic embryogenesis: life and death processes during apical-basal patterning. J Exp Bot 65:1343–1360. doi:10.1093/jxb/eru005
Soriano M, Li H, Boutilier K (2013) Microspore embryogenesis: establishment of embryo identity and pattern in culture. Plant Reprod 26:181–196. doi:10.1007/s00497-013-0226-7
Souter M, Lindsey K (2000) Polarity and signalling in plant embryogenesis. J Exp Bot 51:971–983. doi:10.1093/jexbot/51.347.971
Stone SL, Braybrook SA, Paula SL et al (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis. Proc Natl Acad Sci (USA) 105:3151–3156. doi:10.1073/pnas.0712364105
Stone SL, Kwong LW, Yee KM 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
Su YH, Liu YB, Bai B, Zhang XS (2015) Establishment of embryonic shoot-root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front Plant Sci 5:1–9. doi:10.3389/fpls.2014.00792
Su YH, Zhang XS (2014) The hormonal control of regeneration in plants. Curr Top Dev Biol 108:35–69. doi:10.1016/B978-0-12-391498-9.00010-3
Su YH, Zhao XY, Liu YB et al (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
Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol 21:212–218. doi:10.1016/j.tcb.2010.12.004
Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471. doi:10.1016/j.devcel.2010.02.004
Sundaresan V, Alandete-Saez M (2010) Pattern formation in miniature: the female gametophyte of flowering plants. Development 137:179–189. doi:10.1242/dev.030346
Tanaka M, Kikuchi A, Kamada H (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146:149–161. doi:10.1104/pp.107.111674
Tang X, Lim M-H, Pelletier J et al (2012) Synergistic repression of the embryonic programme by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis seedlings. J Exp Bot 63:1391–1404. doi:10.1093/jxb/err383
Twell D (2011) Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24:149–160. doi:10.1007/s00497-010-0157-5
Ueda M, Laux T (2012) The origin of the plant body axis. Curr Opin Plant Biol 15:578–584. doi:10.1016/j.pbi.2012.08.001
Verdeil J-L, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252. doi:10.1016/j.tplants.2007.04.002
Waki T, Hiki T, Watanabe R et al (2011) The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 21:1277–1281. doi:10.1016/j.cub.2011.07.001
Wang Q, Kohlen W, Rossmann S et al (2014a) Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. Plant Cell 26:2068–2079. doi:10.1105/tpc.114.123059
Wang X-DX-D, Nolan KE, Irwanto RR et al (2011) Ontogeny of embryogenic callus in Medicago truncatula: the fate of the pluripotent and totipotent stem cells. Ann Bot 107:599–609. doi:10.1093/aob/mcq269
Wang Y, Wang J, Shi B et al (2014b) The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. Plant Cell 26:2055–2067. doi:10.1105/tpc.114.123083
Wuest SE, Vijverberg K, Schmidt A et al (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20:506–512. doi:10.1016/j.cub.2010.01.051
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
Yang W-C, Shi D-Q, Chen Y-H (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108. doi:10.1146/annurev-arplant-042809-112203
Zuo J, Niu Q-W, Frugis G, Chua N-H (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359. doi:10.1046/j.1365-313X.2002.01289.x
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The authors acknowledge the support of the Hungarian Scientific Research Fund (OTKA K108802).
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Fehér, A., Bernula, D., Gémes, K. (2016). The Many Ways of Somatic Embryo Initiation. In: Loyola-Vargas, V., Ochoa-Alejo, N. (eds) Somatic Embryogenesis: Fundamental Aspects and Applications. Springer, Cham. https://doi.org/10.1007/978-3-319-33705-0_3
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