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RNA-Seq Analysis of the Arabidopsis Transcriptome in Pluripotent Calli
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  • Journal title : Molecules and Cells
  • Volume 39, Issue 6,  2016, pp.484-494
  • Publisher : Korea Society for Molecular and Cellular Biology
  • DOI : 10.14348/molcells.2016.0049
 Title & Authors
RNA-Seq Analysis of the Arabidopsis Transcriptome in Pluripotent Calli
Lee, Kyounghee; Park, Ok-Sun; Seo, Pil Joon;
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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.
 Keywords
Arabidopsis;biological process;callus formation;dedifferentiation;RNA-Seq;
 Language
English
 Cited by
1.
Developmental transitions: integrating environmental cues with hormonal signaling in the chromatin landscape in plants, Genome Biology, 2017, 18, 1  crossref(new windwow)
2.
High-temperature promotion of callus formation requires the BIN2-ARF-LBD axis in Arabidopsis, Planta, 2017, 246, 4, 797  crossref(new windwow)
 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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

8.
Chan, Z. (2012). Expression profiling of ABA pathway transcripts indicates crosstalk between abiotic and biotic stress responses in Arabidopsis. Genomics 100, 110-115. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

13.
Dempsey, D.A., Vlot, A.C., Wildermuth, M.C, and Klessig, D.F. (2011). Salicylic Acid biosynthesis and metabolism. Arabidopsis Book 9, e0156. crossref(new window)

14.
Endler, A., and Persson, S. (2011). Cellulose synthases and synthesis in Arabidopsis. Mol. Plant 4, 199-211. crossref(new window)

15.
Eulgem, T., and Somssich, I.E. (2007). Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366-371. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

19.
Fu, X., and Harberd, N.P. (2003). Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740-743. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

26.
Grafi, G. (2004). How cells dedifferentiate: a lesson from plants. Dev. Biol. 268, 1-6. crossref(new window)

27.
Grafi, G., and Barak, S. (2015). Stress induces cell dedifferentiation in plants. Biochim. Biophys. Acta. 1849, 378-384. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

38.
Ikeuchi, M., Sugimoto, K., and Iwase, A. (2013). Plant callus: mechanisms of induction and repression. Plant Cell 25, 3159-3173. crossref(new window)

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. crossref(new window)

40.
Keegstra, K. (2010). Plant cell walls. Plant Physiol. 154, 483-486. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

51.
Narbonne, P., and Roy, R. (2006). Regulation of germline stem cell proliferation downstream of nutrient sensing. Cell Div. 1, 29. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

65.
Smith, A.M., Zeeman, S.C., and Smith, S.M. (2005). Starch degradation. Annu. Rev. Plant Biol. 56, 73-98. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

70.
Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

74.
Vanstraelen, M., and Benkova, E. (2012). Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 28, 463-487. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)

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. crossref(new window)