Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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RNA-Seq Analysis of the Arabidopsis Transcriptome in Pluripotent Calli

  • Lee, Kyounghee (Department of Bioactive Material Sciences and Research Center of Bioactive Materials, Chonbuk National University) ;
  • Park, Ok-Sun (Department of Chemistry and Research Institute of Physics and Chemistry, Chonbuk National University) ;
  • Seo, Pil Joon (Department of Bioactive Material Sciences and Research Center of Bioactive Materials, Chonbuk National University)
  • Received : 2016.02.23
  • Accepted : 2016.04.28
  • Published : 2016.06.30
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Abstract

Plant cells have a remarkable ability to induce pluripotent cell masses and regenerate whole plant organs under the appropriate culture conditions. Although the in vitro regeneration system is widely applied to manipulate agronomic traits, an understanding of the molecular mechanisms underlying callus formation is starting to emerge. Here, we performed genome-wide transcriptome profiling of wild-type leaves and leaf explant-derived calli for comparison and identified 10,405 differentially expressed genes (> two-fold change). In addition to the well-defined signaling pathways involved in callus formation, we uncovered additional biological processes that may contribute to robust cellular dedifferentiation. Particular emphasis is placed on molecular components involved in leaf development, circadian clock, stress and hormone signaling, carbohydrate metabolism, and chromatin organization. Genetic and pharmacological analyses further supported that homeostasis of clock activity and stress signaling is crucial for proper callus induction. In addition, gibberellic acid (GA) and brassinosteroid (BR) signaling also participates in intricate cellular reprogramming. Collectively, our findings indicate that multiple signaling pathways are intertwined to allow reversible transition of cellular differentiation and dedifferentiation.

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References

  1. Argyros, R.D., Mathews, D.E., Chiang, Y.H., Palmer, C.M., Thibault, D.M., Etheridge, N., Argyros, D.A., Mason, M.G., Kieber, J.J., and Schaller, G.E. (2008). Type B response regulators of Arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20, 2102-2116. https://doi.org/10.1105/tpc.108.059584
  2. Berckmans, B., Vassileva, V., Schmid, S.P., Maes, S., Parizot, B., Naramoto, S., Magyar, Z., Alvim Kamei, C.L., Koncz, C., Bogre, L., et al. (2011). Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell 23, 3671-3683. https://doi.org/10.1105/tpc.111.088377
  3. Berr, A., Xu, L., Gao, J., Cognat, V., Steinmetz, A., Dong, A., and Shen, W.H. (2009). SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol. 151, 1476-1485. https://doi.org/10.1104/pp.109.143941
  4. Boutilier, K., Offringa, R., Sharma, V.K., Kieft, H., Ouellet, T., Zhang, L., Hattori, J., Lium, C.M., van Lammeren, A.A., Miki, B.L., et al. (2002). Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14, 1737-1749. https://doi.org/10.1105/tpc.001941
  5. Bouyer, D., Roudier, F., Heese, M., Andersen, E.D., Gey, D., Nowack, M.K., Goodrich, J., Renou, J.P., Grini, P.E., Colot, V., et al. (2011). Polycomb repressive complex 2 controls the embryoto-seedling phase transition. PLoS Genet. 7, e1002014. https://doi.org/10.1371/journal.pgen.1002014
  6. Bratzel, F., Lopez-Torrejon, G., Koch, M., Del Pozo, J.C., and Calonje, M. (2010). Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr. Biol. 2, 1853-1859.
  7. Caverzan, A., Passaia, G., Rosa, S.B., Ribeiro, C.W., Lazzarotto, F., and Margis-Pinheiro, M. (2012). Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 35, 1011-1019. https://doi.org/10.1590/S1415-47572012000600016
  8. Chan, Z. (2012). Expression profiling of ABA pathway transcripts indicates crosstalk between abiotic and biotic stress responses in Arabidopsis. Genomics 100, 110-115. https://doi.org/10.1016/j.ygeno.2012.06.004
  9. Charon, C., Johansson, C., Kondorosi, E., Kondorosi, A., and Crespi, M. (1997). ENOD40 induces dedifferentiation and division of root cortical cells in legumes. Proc. Natl. Acad. Sci. USA 94, 8901-8906. https://doi.org/10.1073/pnas.94.16.8901
  10. Chen, D., Molitor, A., Liu, C., and Shen, W.H. (2010). The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res. 20, 1332-1344. https://doi.org/10.1038/cr.2010.151
  11. Cheon, J., Park, S.Y., Schulz, B., and Choe, S. (2010). Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction. BMC Plant Biol. 10, 270. https://doi.org/10.1186/1471-2229-10-270
  12. Cui, K., Li, J., Xing, G., Li, J., Wang, L., and Wang, Y. (2002). Effect of hydrogen peroxide on synthesis of proteins during somatic embryogenesis in Lycium barbarum. Plant Cell Tissue Organ Cult. 68, 187-193. https://doi.org/10.1023/A:1013871500575
  13. Dempsey, D.A., Vlot, A.C., Wildermuth, M.C, and Klessig, D.F. (2011). Salicylic Acid biosynthesis and metabolism. Arabidopsis Book 9, e0156. https://doi.org/10.1199/tab.0156
  14. Endler, A., and Persson, S. (2011). Cellulose synthases and synthesis in Arabidopsis. Mol. Plant 4, 199-211. https://doi.org/10.1093/mp/ssq079
  15. Eulgem, T., and Somssich, I.E. (2007). Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366-371. https://doi.org/10.1016/j.pbi.2007.04.020
  16. Fan, M., Xu, C., Xu, K., and Hu, Y. (2012). LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Res. 22, 1169-1180. https://doi.org/10.1038/cr.2012.63
  17. Florentin, A., Damri, M., and Grafi, G. (2013). Stress induces plant somatic cells to acquire some features of stem cells accompanied by selective chromatin reorganization. Dev. Dyn. 242, 1121-1133. https://doi.org/10.1002/dvdy.24003
  18. Frank, M., Guivarc'h, A., Krupkova, E., Lorenz-Meyer, I., Chriqui, D., and Schmulling, T. (2002). TUMOROUS SHOOT DEVELOPMENT (TSD) genes are required for co-ordinated plant shoot development. Plant J. 29, 73-85. https://doi.org/10.1046/j.1365-313x.2002.01197.x
  19. Fu, X., and Harberd, N.P. (2003). Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740-743. https://doi.org/10.1038/nature01387
  20. Gaj, M.D., Zhang, S., Harada, J.J., and Lemaux, P.G. (2005). Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222, 977-988. https://doi.org/10.1007/s00425-005-0041-y
  21. Garcia-Ruiz, H., Carbonell, A., Hoyer, J.S., Fahlgren, N., Gilbert, K.B., Takeda, A., Giampetruzzi, A., Garcia Ruiz, M.T., McGinn, M.G., Lowery, N., et al. (2015). Roles and programming of Arabidopsis ARGONAUTE proteins during Turnip mosaic virus infection. PLoS Pathog. 11, e1004755. https://doi.org/10.1371/journal.ppat.1004755
  22. Gasciolli, V., Mallory, A.C., Bartel, D.P., and Vaucheret, H. (2005). Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494-1500. https://doi.org/10.1016/j.cub.2005.07.024
  23. Gaspar-Maia, A., Alajem, A., Meshorer, E., and Ramalho-Santos, M. (2011). Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 12, 36-47. https://doi.org/10.1038/nrm3036
  24. Gohlke, J., and Deeken, R. (2014). Plant responses to Agrobacterium tumefaciens and crown gall development. Front. Plant Sci. 5, 155.
  25. Gonzalez-Garcia, M.P., Vilarrasa-Blasi, J., Zhiponova, M., Divol, F., Mora-Garcia, S., Russinova, E., and Cano-Delgado, A.I. (2011). Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138, 849-959. https://doi.org/10.1242/dev.057331
  26. Grafi, G. (2004). How cells dedifferentiate: a lesson from plants. Dev. Biol. 268, 1-6. https://doi.org/10.1016/j.ydbio.2003.12.027
  27. Grafi, G., and Barak, S. (2015). Stress induces cell dedifferentiation in plants. Biochim. Biophys. Acta. 1849, 378-384. https://doi.org/10.1016/j.bbagrm.2014.07.015
  28. Grafi, G., Chalifa-Caspi, V., Nagar, T., Plaschkes, I., Barak, S., and Ransbotyn, V. (2011). Plant response to stress meets dedifferentiation. Planta 233, 433-438. https://doi.org/10.1007/s00425-011-1366-3
  29. Guo, L., Yu, Y., Law, J.A., and Zhang, X. (2010). SET DOMAIN GROUP2 is the major histone H3 lysine [corrected] 4 trimethyltransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 107, 18557-18562. https://doi.org/10.1073/pnas.1010478107
  30. Guo, F., Liu, C., Xia, H., Bi, Y., Zhao, C., Zhao, S., Hou, L., Li, F., and Wang, X. (2013). Induced expression of AtLEC1 and AtLEC2 differentially promotes somatic embryogenesis in transgenic tobacco plants. PLoS One 8, e71714. https://doi.org/10.1371/journal.pone.0071714
  31. Harding, E.W., Tang, W., Nichols, K.W., Fernandez, D.E., and Perry, S.E. (2003). Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-LIKE 15. Plant Physiol. 133, 653-663. https://doi.org/10.1104/pp.103.023499
  32. He, C., Chen, X., Huang, H., and Xu, L. (2012). Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet. 8, e1002911. https://doi.org/10.1371/journal.pgen.1002911
  33. Henderson, I.R., Zhang, X., Lu, C., Johnson, L., Meyers, B.C., Green, P.J., and Jacobsen, S.E. (2006). Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38, 721-725. https://doi.org/10.1038/ng1804
  34. Holmes-Davis, R., Tanaka, C.K., Vensel, W.H., Hurkman, W.J., and McCormick, S. (2005). Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5, 4864-4884. https://doi.org/10.1002/pmic.200402011
  35. Huang, D.W., Sherman, B.T., and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protoc. 4, 44-57. https://doi.org/10.1038/nprot.2008.211
  36. Ikeda-Iwai, M., Umehara, M., Satoh, S., and Kamada, H. (2003). Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J. 34, 107-114. https://doi.org/10.1046/j.1365-313X.2003.01702.x
  37. Ikeda, Y., Banno, H., Niu, Q.W., Howell, S.H., and Chua, N.H. (2006). The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis regulates CUP-SHAPED COTYLEDON 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol. 47, 1443-1456. https://doi.org/10.1093/pcp/pcl023
  38. Ikeuchi, M., Sugimoto, K., and Iwase, A. (2013). Plant callus: mechanisms of induction and repression. Plant Cell 25, 3159-3173. https://doi.org/10.1105/tpc.113.116053
  39. Iwase, A., Mitsuda, N., Koyama, T., Hiratsu, K., Kojima, M., Arai, T., Inoue, Y., Seki, M., Sakakibara, H., Sugimoto, K., et al. (2011). The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr.Biol. 21, 508-514. https://doi.org/10.1016/j.cub.2011.02.020
  40. Keegstra, K. (2010). Plant cell walls. Plant Physiol. 154, 483-486. https://doi.org/10.1104/pp.110.161240
  41. Kim, M.G., Kim, S.Y., Kim, W.Y., Mackey, D., and Lee, S.Y. (2008). Responses of Arabidopsis thaliana to challenge by Pseudomonas syringae. Mol. Cells 25, 323-331.
  42. Kosugi, S., and Ohashi, Y. (2003). Constitutive E2F expression in tobacco plants exhibits altered cell cycle control and morphological change in a cell type-specific manner. Plant Physiol. 132, 2012-2022. https://doi.org/10.1104/pp.103.025080
  43. Kotting, O., Pusch, K., Tiessen, A., Geigenberger, P., Steup, M., and Ritte, G. (2005). Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 137, 242-252. https://doi.org/10.1104/pp.104.055954
  44. Koyama, T., Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2010). TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22, 3574-3588. https://doi.org/10.1105/tpc.110.075598
  45. Kumar, R., Kushalappa, K., Godt, D., Pidkowich, M.S., Pastorelli, S., Hepworth, S.R., and Haughn, G.W. (2007). The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19, 2719-2735. https://doi.org/10.1105/tpc.106.048769
  46. Lafos, M., Kroll, P., Hohenstatt, M.L., Thorpe, F.L., Clarenz, O., and Schubert, D. (2011). Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet. 7, e1002040. https://doi.org/10.1371/journal.pgen.1002040
  47. Lee, H.G., Mas, P., and Seo, P.J. (2016). MYB96 shapes the circadian gating of ABA signaling in Arabidopsis. Sci. Rep. 6, 17754. https://doi.org/10.1038/srep17754
  48. Mason, M.G., Mathews, D.E., Argyros, D.A., Maxwell, B.B., Kieber, J.J., Alonso, J.M., Ecker, J.R., and Schaller, G.E. (2005). Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17, 3007-3018. https://doi.org/10.1105/tpc.105.035451
  49. Nag, A., King, S., and Jack, T. (2009). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc. Natl. Acad. Sci. USA 106, 22534-22539. https://doi.org/10.1073/pnas.0908718106
  50. Nakamichi, N., Ito, S., Oyama, T., Yamashino, T., Kondo, T., and Mizuno, T. (2004). Characterization of plant circadian rhythms by employing Arabidopsis cultured cells with bioluminescence reporters. Plant Cell Physiol. 45, 57-67. https://doi.org/10.1093/pcp/pch003
  51. Narbonne, P., and Roy, R. (2006). Regulation of germline stem cell proliferation downstream of nutrient sensing. Cell Div. 1, 29. https://doi.org/10.1186/1747-1028-1-29
  52. Nicaise, V., Roux, M., and Zipfel, C. (2009). Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol. 150, 1638-1647. https://doi.org/10.1104/pp.109.139709
  53. Niederhuth, C.E., Patharkar, O.R., and Walker, J.C. (2013). Transcriptional profiling of the Arabidopsis abscission mutant hae hsl2 by RNA-Seq. BMC Genomics 14, 37. https://doi.org/10.1186/1471-2164-14-37
  54. Nuruzzaman, M., Sharoni, A.M., and Kikuchi, S. (2013). Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front. Microbiol. 4, 248.
  55. Okushima, Y., Fukaki, H., Onoda, M., Theologis, A., and Tasaka, M. (2007). ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19, 118-130. https://doi.org/10.1105/tpc.106.047761
  56. Passaia, G., Queval, G., Bai, J., Margis-Pinheiro, M., and Foyer, C.H. (2014). The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana. J. Exp. Bot. 65, 1403-1413. https://doi.org/10.1093/jxb/ert486
  57. Pumplin, N., and Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counterdefence. Nat. Rev. Microbiol. 11, 745-760. https://doi.org/10.1038/nrmicro3120
  58. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R.C., and Melton, D.A. (2002). "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600. https://doi.org/10.1126/science.1072530
  59. Rasmussen, M.W., Roux, M., Petersen, M., and Mundy, J. (2012). MAP kinase cascades in Arabidopsis innate immunity. Front. Plant Sci. 3, 169.
  60. Rodrigues, A., Adamo, M., Crozet, P., Margalha, L., Confraria, A., Martinho, C., Elias, A., Rabissi, A., Lumbreras, V., Gonzalez-Guzman, M., et al. (2013). ABI1 and PP2CA phosphatases are negative regulators of SNF1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25, 3871-3884. https://doi.org/10.1105/tpc.113.114066
  61. Sakai, H., Honma, T., Aoyama, T., Sato, S., Kato, T., Tabata, S., and Oka, A. (2001). ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294, 1519-1521. https://doi.org/10.1126/science.1065201
  62. Santelia, D., Kotting, O., Seung, D., Schubert, M., Thalmann, M., Bischof, S., Meekins, D.A., Lutz, A., Patron, N., Gentry, M.S., et al. (2011). The phosphoglucan phosphatase like sex Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant cell 23, 4096-4111. https://doi.org/10.1105/tpc.111.092155
  63. Sieberer, T., Hauser, M.T., Seifert, G.J., and Luschnig, C. (2003). PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr. Biol. 13, 837-842. https://doi.org/10.1016/S0960-9822(03)00327-0
  64. Skylar, A., Sung, F., Hong, F., Chory, J., and Wu, X. (2011). Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2. Dev. Biol. 351, 82-89. https://doi.org/10.1016/j.ydbio.2010.12.019
  65. Smith, A.M., Zeeman, S.C., and Smith, S.M. (2005). Starch degradation. Annu. Rev. Plant Biol. 56, 73-98. https://doi.org/10.1146/annurev.arplant.56.032604.144257
  66. Streb, S., Eicke, S., and Zeeman, S.C. (2012). The simultaneous abolition of three starch hydrolases blocks transient starch breakdown in Arabidopsis. J. Biol. Chem. 287, 41745-41756. https://doi.org/10.1074/jbc.M112.395244
  67. Sugimoto, K., Jiao, Y., and Meyerowitz, E.M. (2010). Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev. Cell 18, 463-471. https://doi.org/10.1016/j.devcel.2010.02.004
  68. Tao, Q., Guo, D., Wei, B., Zhang, F., Pang, C., Jiang, H., Zhang, J., Wei, T., Gu, H., Qu, L.J., et al. (2013). The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell 25, 421-437. https://doi.org/10.1105/tpc.113.109223
  69. Thakare, D., Tang, W., Hill, K., and Perry SE. (2008). The MADSdomain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiol. 146, 1663-1672. https://doi.org/10.1104/pp.108.115832
  70. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111. https://doi.org/10.1093/bioinformatics/btp120
  71. Trigueros, M., Navarrete-Gomez, M., Sato, S., Christensen, S.K., Pelaz, S., Weigel, D., Yanofsky, M.F., and Ferrandiz, C. (2009). The NGATHA genes direct style development in the Arabidopsis gynoecium. Plant Cell 21, 1394-1409. https://doi.org/10.1105/tpc.109.065508
  72. Tsukagoshi, H., Busch, W., and Benfey, P.N. (2010). Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143, 606-616. https://doi.org/10.1016/j.cell.2010.10.020
  73. Tsuwamoto, R., Yokoi, S., and Takahata, Y. (2010). Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol. Biol. 73, 481-492. https://doi.org/10.1007/s11103-010-9634-3
  74. Vanstraelen, M., and Benkova, E. (2012). Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 28, 463-487. https://doi.org/10.1146/annurev-cellbio-101011-155741
  75. Xing, Y., Jia, W., and Zhang, J. (2007). AtMEK1 mediates stressinduced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J. Exp. Bot. 58, 2969-2981. https://doi.org/10.1093/jxb/erm144
  76. Xing, Y., Cao, Q., Zhang, Q., Qin, L., Jia, W., and Zhang, J. (2013). MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis. Plant Cell Physiol. 54, 1217-1227. https://doi.org/10.1093/pcp/pct072
  77. Yakir, E., Hilman, D., Harir, Y., and Green, R.M. (2007). Regulation of output from the plant circadian clock. FEBS J. 274, 335-345. https://doi.org/10.1111/j.1742-4658.2006.05616.x
  78. Yang, H., Mo, H., Fan, D., Cao, Y., Cui, S., and Ma, L. (2012). Overexpression of a histone H3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis. Plant Cell Rep. 31, 1297-1308. https://doi.org/10.1007/s00299-012-1249-5
  79. Zuo, J., Niu, Q.W., Frugis, G., and Chua, N.H. (2002). The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J. 30, 349-359. https://doi.org/10.1046/j.1365-313X.2002.01289.x

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