Abstract
Somatic embryogenesis (SE) is a model system for understanding the physiological, biochemical, and molecular biological events occurring during plant embryo development. Plant somatic cells have the ability to undergo sustained divisions and give rise to an entire organism. This remarkable feature is called plant cell totipotency. SE is a notable illustration of plant totipotency and involves reprogramming of development in somatic cells toward the embryogenic pathway. Plant growth regularities, especially auxins, are key components as their exogenous application recapitulates the embryogenic potential of the mitotically quiescent somatic cells. It has been observed that there are genetic and also physiological factors that trigger in vitro embryogenesis in various types of plant somatic cells. Analysis of the proteome and transcriptome has led to the identification and characterization of certain genes involved in SE. Most of these genes, however, are upregulated only in the late developmental stages, suggesting that they do not play a direct role in the vegetative-to-embryogenic transition. However, the molecular bases of those triggering factors and the genetic and biochemical mechanisms leading to in vitro embryogenesis are still unknown. Here, we describe the plant factors that participate in the vegetative-to-embryogenic transition and discuss their possible roles in this process.
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Aker J, de Vries SC (2008) Plant Physiol 147:1560
Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) Plant Cell 17:3337
Alemanno L, Devic M, Niemenak N, Sanier C (2008) Planta 227:853
Banno H, Ikeda Y, Niu Q-W, Chua N-H (2001) Plant Cell 13:2609
Baudino S, Hansen S, Brettschneider R, Hecht VRG, Dresselhaus T, Lorz H, Dumas C, Rogowsky PM (2001) Planta 213:1
Becker D, Hedrich R (2002) Plant Mol Biol 49:349
Ben C, Hewezi T, Jardinaud MF, Bena F, Ladouce N, Moretti S, Tamborindeguy C, Liboz T, Petitprez M, Gentzbittel L (2005) Plant Molecular Biology 57:255
Bender J (2004) Annul Review Plant Biology 55:41
Bhalla PL, Singh MB (2006) Plant Cell Rep 25:249
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J (2005) Nature 433:39
Boutilier K, OVringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002) Plant Cell 14:1737
Braybrook SA, Stone SL, Park S, Bui AQ, Lee BH, Fischer RL, Goldberg RB, Harada JJ (2006) Proc Natl Acad Sci USA 103:3468
Caliskan M, Cuming AC (1998) Plant J 15:165
Caliskan M, Turet M, Cuming AC (2004) Planta 219:132
Campbell MA, Lara MH, Jennifer C (1998) Plant Physiol 118:711
Cao X (2003) Curr Biol 13:2212
Casson S, Spencer M, Walker K, Lindsey K (2005) Plant J 42:111
Chang C (2003) Trends Plant Sci 8:365
Chapman A, Blervacq AS, Vasseur J, Hilbert JL (2000) Planta 211:305
Charriere F, Hahne G (1998) Plant Sci 137:63
Che P, Lall S, Nettleton D, Howell SH (2006) Plant Physiol 141:620
Che P, Love TM, Frame BR, Wang K, Carriquiry AL, Howell SH (2006) Plant Mol Biol 62:1
Chen JG, Ullah H, Young JC, Sussman MR, Jones AM (2001) Genes Dev 15:902
Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Plant Physiology 129:661
Chuck G, Meeley RB, Hake S (1998) Genes Dev 12:1145
Chugh A, Khurana PJ (2002) Curr Sci 83:715
Davletova S, Meszaros T, Miskolczi P, Oberschall A, Torok K, Magyar Z, Dudits D, Deak M (2001) J Exp Bot 52:215
de Vries SC, Booij H, Meyerink P, Huisman G, Wilde HD, Thomas TL (1988) Planta 176:196
Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jürgens G, Estelle M (2005) Dev Cell 9:109
Domon JM, Dumas B, Laine E, Meyer Y, David A, David H (1995) Plant Physiology 108:141
Domon JM, Neutelings G, Roger D, David A, David H (2000) J Plant Physiol 156:33
Du L, Chen Z (2000) Plant J 24:837–47
Dumas B, Freyssinet G, Pallett KE (1995) Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol 107:1091
Dunwell JM (1998) Biotechnol Genet Eng Rev 15:1
Dunwell JM, Purvis A, Khuri S (2004) Phytochemistry 65:7
Edwards R, Dixon DP, Walbot V (2000) Trends Plant Sci 5:193
Egertsdotter U, von Arnold S (1995) Physiology Plant 93:334
Elliot RC, Betzner AS, Huttner E, Oakes M, Tucker WQJ, Gerentes D, Parez P, Smith DR (1996) Plant Cell 8:155
Eshed Y, Baum SF, Bowman JL (1999) Cell 99:199
Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L, Michelotti V, Salvini M, Pugliesi C (2006) Development Genes Evaluation 1216:253
Fedina IS, Tsonev TD, Guleva EI (1994) J Plant Physiol 143:245
Feher A, Pasternak TP, Dudits D (2003) Plant Cell Tissue Organ Cult 74:201
Fernandez DE, Heck GR, Perry SE, Patterson SE, Bleecker AB, Fang SC (2000) Plant Cell 12:183
Finnegan EJ, Peacock WJ, Dennis ES (1996) Development 93:8449
Francis D, Sorrell DA (2001) Plant Growth Regul 33:1
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T (2003) Nature 426:147
Fujimura T, Komamine A (1980) Plant Physiol 64:162
Gaj MD (2001) Plant Cell Tissue Organ Cult 64:39
Gaj MD (2004) Plant Growth Regul 43:27
Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Planta 222:977
Galland R, Randoux B, Vasseur J, Hilbert JL (2001) Biochemistry Biophysics Acta 1522:212
Gampala S, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron J (2007) Dev Cell 13:177
Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) Dev Cell 7:373
Gehring M, Henikoff S (2007) Biochemistry Biophysics Acta 1769:276
Geisler M, Murphy A (2006) FEBS Lett 580:1094
Gelhaye E, Rouhier N, Jacquot JP (2004) Plant Physiol Biochem 42:265
Giroux RW, Pauls KP (1997) Plant Mol Biol 33:393
Gray WM, Hellmann H, Dharmasiri S, Estelle M (2002) Plant Cell 14:213744
Grebe M, Friml J, Swarup R, Ljung K, Sandberg G, Terlou M (2002) Curr Biol 12:329
Guilfoyle TJ (1999) Auxin-regulated genes and promotors. In: Hooykaas PJJ, Hall MA, Libbenga KR (eds) Biochemistry and molecular biology of plant hormones. Elsevier, Amsterdam, p 423
Guo H, Ecker JR (2003) Cell 115:667
Guzzo F, Baldan B, Levi M, Sparvoli E, Schiavo FL, Terzi M, Mariani P (1995) Protoplasma 185:1
Harada JJ (2001) J Plant Physiol 158:405
Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Plant Physiol 133:653
He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J (2007) Curr Biol 17:1109
Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC (2001) Plant Physiol 127:803
Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) Plant Cell 7:1271
Hellmann H, Estelle M (2002) Science 297:793
Henderson JT, Li HC, Rider SD, Mordhorst AP, Romero-Severson J, Cheng JC, Robey J, Sung ZR, De Vries SC, Ogas J (2004) Plant Physiology 134:995
Holm PB, Knudsen S, Mouritzen P, Negri D, Olsen FL, Roue C (1994) Plant Cell 6:531
Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halfordm N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu J-K, Harmon AC (2003) Plant Physiol 132:666
Hu H, Xiong L, Yang Y (2005) Planta 222:107–117
Ikeda M, Umehara M, Kamada H (2006) Plant Biotechnol 23:153
Ikeda Y, Banno H, Niu QW, Howell SH, Chua NH (2006) Plant Cell Physiology 47:1443
Ikeda-Iwai M, Satoh S, Kamada H (2002) J Exp Bot 53:1575
Imin N, De Jong F, Mathesius U, van Noorden G, Saeed NA, Wang XD, Rose RJ, Rolfe BG (2004) Proteomics 4:1883
Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Plant Physiol 137:1250
Imin N, Nizamidin M, Wu T, Rolfe BG (2006) J Exp Bot 58:439
Ito Y, Takaya K, Kurata N (2005) Biochemistry Biophysics Acta 1730:253
Jimenez VM (2005) Plant Growth Regul 47:91
Jimenez VM (2001) Revista Brasileira de Fisiologia Vegetal 13:196
Jong AJ, Hendriks T, Meijer EA, Penning M, LoSchiavo F, Terzi M, Kammen A, van de Vries SC (1995) Development Genetic 16:332
Kakutani T, Jeddeloh JA, Flowers SK, Munakata K, Richards EJ (1996) Proc Natl Acad Sci USA 93:12406
Kakutani T, Kato M, Kinoshita T, Miura A (2004) Cold Spring Herb Symptom Quant Biology 69:139
Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Genetics 163:1109
Karami O, Deljou A, Karimi Kordestani G (2008) Plant Cell Tissue Organ Cult 92:273
Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S (2006) Plant Cell 18:626
Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Curr Biol 13:421
Kidner CA, Martienssen RA (2005) Development Biology 280:504
Kikuchi A, Sanuki N, Higashi K, Koshiba T, Kamada H (2006) Planta 223:637
Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Proc Natl Acad Sci USA 103:814
Kim S, Soltis PS, Wall K, Soltis DE (2006) Mol Biol Evol 23:107
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K, Higashi K, Satoh S, Kamada H, Harada H (1992) Planta 186:337
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K, Kamada H, Harada H (1993) Plant Mol Biol 21:1053
Klose RJ, Bird AP (2006) Trends Biochem Sci 31:89
Klucher KM, Chow H, Reiser L, Fischer RL (1996) Plant Cell 8:137
Komamine A, Matsumoto M, Tsukahara M, Fujiwara A, Kawahara R, Ito M, Smith J, Nomura K, Fujimura T (1990) Mechanism of somatic embryogenesis in cell cultures-physiology, biochemistry and molecular biology. In: Nijkamp HJJ, Van der Plas LHW, Van Aartrijk J (eds) Progress in plant cellular and molecular biology, current plant science and biotechnology in agriculture, vol 9. Kluwer, Dordrecht, p 307
Koornneef M, Reuling G, Karessen CM (1984) Plant Physiol 61:377
Kreuger M, van Holst GJ (1993) Planta 189:243
Kurczynska EU, Gaj MD, Ujczak A, Mazur E (2007) Planta 226:619
Kwaaitaal MA, de Vries SC, Russinova E (2005) Protoplasma 226:55
Kwong RM, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) Plant Cell 15:5
Lee H, Fischer RL, Goldberg RB, Harada JJ (2003) Proc Natl Acad Sci USA 100:2152
Legrand S, Hendriks T, Hilbert Je-L, Quillet M-C (2007) BMC Plant Biology 7:27
Leljak-Levanic D, Naana B, Jelaska MS (2004) Plant Cell Report 23:120
Letarte J, Simion E, Miner M, Kasha-Ken J (2006) Plant Cell Report 24:691
Levine A, Tenhaken R, Dixon R, Lamb C (1994) Cell 79:583
Lin X, Hwang GJ, Zimmerman JL (1996) Plant Physiol 112:1365
Lo Schiavo F, Giuliano G, de Vries S, Genga A, Bollini R, Pitto L, Cozzani F, Nuti-Ronchi V, Terzi M (1990) Molecular Gene Genetic 223:385
Loschiavo F, Pitto L, Giuliano G, Torti G, Nuit-Ronchi V, Marazziti D, Vergara R, Orselli S, Terzi M (1989) Theory Apply Genetic 77:325
Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Tamagishi K, Fisher RL, Goldberg RB, Harada JJ (1998) Cell 93:1195
Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) Development 126:469
Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006) Science 311:94
Mahonen AP, Higuchi M, Tormakangas K, Miyawaki K, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T (2006) Curr Biol 16:1116
Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang X-D, VandenBosch KA, Rose RJ (2008) Plant Physiol 146:1622
Maraschin SF, Priester W, Spaink HP, Wang M (2005) J Exp Bot 56:1711
Suarez MF, Bozhkov PV (2008) Methods Mol Biol 427:1–14. doi:10.1007/978-1-59745-273-1
Martin KP (2004) BIOLOGIA, PLANTARUM 48:285
Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Cell 95:805
Membre N, Berna A, Neutelings G, David A, David H, Staiger D, Saez Vasquez J, Raynal M, Delseny M, Bernier F (1997) Plant Mol Biol 35:459
Michniewicz M, Brewer PB, Friml J (2007) Polar auxin transport and asymmetric auxin distribution. Somerville CR, Meyerowitz EM (eds) Arabidopsis book. American Society of Plant Biologists, Rockville, p 125
Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kalo P, Prabhu R, Marsh JF, Mitra RM, Kereszt A (2007) Plant Cell 19:1221
Mordhorst AP, Hartog MV, El Talmer MK, Laux T, de Vries SC (2002) Planta 214:829
Mordhorst AP, Toonen MAJ, de Vries SC (1997) Critical Review Plant Science 16:535
Mordhorst AP, Voerman KJ, Hartog MV, Meijer EA, VanWent J, Koornneef M, deVries SC (1998) Genetics 149:549
Nagata T, Ishida S, Hasezawa S, Takahashi Y (1994) Int J Dev Biology 38:321
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Plant Physiol 140:411
Namasivayam P (2007) Plant Cell Tissue Organ Cult 90:1
Neutelings G, Domon JM, Membre N, Bernier F, Meyer Y, David A, David H (1998) Plant Mol Biol 38:1179
Nishiwaki M, Fujino K, Koda Y, Masuda K, Kikuta Y (2000) Planta 211:756
Nolan KE, Irwanto RR, Rose RJ (2003) Plant Physiol 133:218
Nolan KE, Saeed NA, Rose RJ (2006) Plant Cell Report 25:711
Ogas J, Kaufmann S, Henderson J, Somerville C (1999) Proc Natl Acad Sci USA 96:13839
Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Science 277:91
Ogata Y, Iizuka M, Nakayama D, Ikeda M, Kamada H, Koshiba T (2005) Planta 221:417
Ohmiya A, Tanaka Y, Kadowaki K, Hayashi T (1998) Plant Cell Physiology 39:492
Okamura JK, Caster B, Villaroel R, van Montagu M, Jofuku KD (1997) Proc Natl Acad Sci USA 94:7076
Paponov IA, Teale WD, Trebar M, Blilou K, Palme K (2005) Trends Plant Sci 10:170
Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Plant Cell 6:1567
Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B (2003) Plant Cell 15:1538
Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) J Biology Chemistry 282:10036
Parry G, Marchant A, May S, Swarup R, Swarup K, James N (2001) Plant Growth Regul 20:217
Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, Boer B, van der Geest Lo, Boutilier K (2008) Plant Mol Biol 68:225
Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, Dudits D, Feher A (2002) Plant Physiol 129:1807
Pennell RI, Graham NLJ, Hilbert S, de Vries SC, Robertsw K (1992) J Cell Biol 119:1371
Pennell RI, Quentin CB, Cronk L, Scott F, Christine S, Lars S, Per K, Paul FM (1995) Biol Sci 350:87
Perry SE, Nichols KW, Fernandez DE (1996) Plant Cell 8:1977
Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S (2003) Cell 115:679
Puigderrajols P, Jofre A, Mir G, Pla M, Verdaguer D, Huguet G, Molinas M (2002) J Exp Bot 53:1445
Quint M, Gary WM (2006) Curr Opin Plant Biol 9:448
Quiroz-Figueroa FR, Rojas-Herrera R, Galaz-Avalos RM, Loyola-Vargas VM (2006) Plant Cell Tissue Org Culture 86:285
Raghavan V (2004) Am J Bot 9:1743
Raghavan V (2006) Curr Sci 90:1336
Raghavan V (1986) Somatic embryogenesis. In: Raghavan V (ed) Embryogenesis in angiosperms. Cambridge University Press, Cambridge, p 115
Rani AR, Reddy VD, Prakash Babu P, Padmaja G (2005) Biology Plant 49:347
Ray PM, Dohrmann U, Hertel R (1977) Plant Physiol 60:585
Reichheld JP, Mestres-Ortega D, Laloi C, Meyer Y (2002) Plant Physiol Biochem 40:685
Rensing SA, Daniel L, Schumann, Reski R, Hohe A (2005) Journal Plant Growth Regulators 24:102
Ribnicky DM, Ilic N, Cohen JD, Cooke TJ (1996) Plant Physiology 112:549
Rider SD, Hemm MR, Hostetler HA, Li HC, Chapple C, Ogas J (2004) Planta 219:489
Rider SD, Henderson JT, Jerome RE, Edenberg HJ, Romero-Severson J, Ogas J (2003) Plant J 35:33
Roberts AG, Oparka K (2003) Plant Cell Environmental 26:103
Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Science 273:654
Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M (1998) Genes Dev 12:198
Ryu H, Kim K, Hwang I (2008) Plant Signal Behavior 3:278
Saab IN, Sharp RE, Pritchard J (1992) Plant Physiol 99:26
Sagare AP, Lee YL, Lin TC, Chen CC, Tsay HS (2000) Plant Sci 160:139
Sakuma Y, Liu Q, Dubouzet JG, Abes H, Shinozak K, Yamaguchi- Shinozaki K (2002) Biochemical and Biophysical Research Communications 290:998
Sallandrouze A, Faurobert M, Maataoui M, Espagnac H (1999) Electrophoresis 20:1109
Santos A, Oliveira MD, Romano E, Clemente YKS, Penha TML, Andrade BB (2005) Plant Sci 168:723
Santos MM, Dubreucq B, Miquel M, Caboche M, Lepiniec L (2005) FEBS Lett 579:4666
Sauser C, Kwiatkowski J, Jung J, Grossamann K (1992) J Plant Physiol 140:747
Saze H, Scheid OM, Paszkowski J (2003) Nat Genet 34:65
Schmidt EDL, Guzzo F, Toonen MAJ, de Vries SC (1997) Development 124:2049
Schoof H, Lenhard M, Haecker A, Mayer KFX, Jurgens G, Laux T (2000) Cell 100:635
Segarra CI, Casalongue CA, Pinedo ML, Ronchi VP, Conde RD (2003) J Exp Bot 54:1335
Shah K, Schmidt EDL, Vlak JM, de Vries SC (2001) Biochimie 83:415
Sharma SK, Millam S, Hein I, Glenn BJ (2008) Planta 228:319
Shimada T, Hirabayashi T, Endo T, Fujii H, Kita M, Omura M (2005) Scientia Horticulture 103:233
Shiota H, Kamada H (2000) J Plant Physiol 156:510
Shiota H, Satoh R, Watabe K, Harada H, Kamada H (1998) Plant Cell Physiology 39:1184
Showalter AM (2001) Cell Molecular Life Science 58:1399
Singla B, Tyag AK, Khurana JP, Khurana P (2007) Plant Mol Biol 65:677
Skriver K, Mundy J (1990) Plant Cell 2:503
Somleva MN, Schmidt EDL, de Vries SC (2000) Plant Cell Report 19:718
Souter M, Lindsey K (2000) J Exp Bot 51:971
Srinivasan C, Liu ZR, Heidmann I, Supena EDJ, Fukuoka H, Joosen R, Lambalk J, Angenent G, Scorza R, Custers JBM (2007) Planta 225:341
Stasolla C, Bozhkov PV, Chu TM, van Zyl L, Egertsdotter U, Suarez MF, Craig D, Wolfinger RD, Von Arnold S, Sederoff RR (2004) Tree Physiology 24:1073
Steele-King CG, Willats WGT, Knox JP (2000) Arabinogalactan-proteins and cell development in roots and somatic embryos. In: Nothnagel EA, Bacic A, Clarke AE (eds) Cell and developmental biology of Arabinogalactan-proteins. Kluwer, New York, pp 95–107
Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S (1999) Science 286:316
Stone SL, Braybrook SA, Paula S, Kwon LW, Meuser J, Pelletier J, Hsieh T-F, Fischer RL, Goldberg B, Harada JJ (2008) Proc Natl Acad Sci USA 105:3151
Stone SL, Kwong LW, Yee KM, Pelletier J, Loic L, Fischer RL, Goldberg RB, Harada JJ (2001) Proc Natl Acad Sci USA 98:11806
Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K (2001) Genes Dev 15:2648
Tabuchi T, Kumon T, Azuma T, Nanmori T, Yasuda T (2003) Physiology Plant 118:523
Tachikawa Y, Saitou T, Kamada H, Harada H (1998) Plant Biotechnology 15:17
Tanaka H, Dhonukshe P, Brewer PB, Friml J (2006) Cell Molecular Life Science 63:2738
Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Plant J 45:1028
Thakare D, Weining T, Hill K, Perry SE (2008) Plant Physiol 146:1663
Thomas C, Meyer D, Himber C, Steinmetz A (2004) Plant Physiol Biochem 42:35
Thompson EW, Lane BG (1980) J Biology Chemistry 255:5965
Tokuji Y, Kuriyama K (2003) Journal of Plant Physiology 160:133
Toonen MAJ, Hendriks T, Schmidt Ed DL, Verhoeven HA, Kammen Ab, Van Vries SC (1994) Planta 194:565
Toonen MAJ, Schmidt EDL, Heo TH, Verhoeven HA, van Kammen A, de Vries SC (1996) Planta 200:167
Toonen MAJ, Schmidt EDL, van Kammen A, de Vries SC (1997) Planta 203:188
Torii KU (2004) Int Rev Cytol 234:1
van der Graa VE, Den Dulk-Ras A, Hooykaas PJJ, Keller B (2000) Development 127:4971
Thibaud-Nissen FO, Shealy RT, Khanna A, Vodkin LO (2003) Plant Physiology 132:118
van Hengel AJ, van Kammen A, De Vries SC (2002) Physiology Plant 114:637
van Hengel AJ, Guzzo F, van Kammen A, de Vries SC (1998) Plant Physiol 117:43
van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, De Vries SC (2001) Plant Physiol 125:1880
Vergne P, Dumas C (2000) Plant Mol Biol 44:559
Vogel G (2005) Science 300:86
Vogler H, Kuhlemeier C (2003) Curr Opin Plant Biol 6:51
von Recklinghausen IR, Iwanowska A, Kieft H, Mordhorst AP, Schel JHN, van Lammeren AAM (2000) Protoplasma 211:217
Vroemen C, deVries S, Quatrano R (1999) Cell Development Biology 10:157
Wang H, Caruso LV, Downie AB, Perry SE (2004) Plant Cell 16:1206
Wang X, Chory J (2006) Science 313:1118
Willemsen V, Scheres B (2004) Annul Review Genetic 38:587
Williams EG, Maheswaran G (1986) Annals Botany 57:443
Wilson JW, Wilson PMW (1993) J Plant Physiology 20:555
Winkelmann T, Heintz D, Van Dorsselaer A, Serek M, Braun HP (2006) Planta 224:508
Xiao W, Custard KD, Brown RC, Lemmon BE, Harada JJ, Goldberg RB, Fischer RL (2006) Plant Cell 18:805
Yamamoto N, Kobayashi H, Togashi T, Mori Y, Kikuchi K, Kuriyama K, Tokuji Y (2005) J Plant Physiol 162:47
Yazawa K, Takahata K, Kamada H (2004) Plant Physiol Biochem 42:215
Zambryski P, Crawford K (2000) Annul Review Cell Development Biology 16:393
Zdravkovic-Korac S, Neskovic M (1999) Plant Cell Tissue Organ Cult 55:109
Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y (2006) Plant Mol Biol 60:167
Zhu C, Perry SE (2005) Plant J 41:583
Zimmerman JL (1993) Plant Cell 5:1411
Zuo Jianru Q-W, Giovanna F, Nam-Hai C (2002) Plant J 30:349
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Karami, O., Aghavaisi, B. & Mahmoudi Pour, A. Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol 2, 177–190 (2009). https://doi.org/10.1007/s12154-009-0028-4
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DOI: https://doi.org/10.1007/s12154-009-0028-4