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Involvement of Pyridoxine/Pyridoxamine 5′- Phosphate Oxidase (PDX3) in Ethylene-Induced Auxin Biosynthesis in the Arabidopsis Root

  • Kim, Gyuree ;
  • Jang, Sejeong ;
  • Yoon, Eun Kyung ;
  • Lee, Shin Ae ;
  • Dhar, Souvik ;
  • Kim, Jinkwon ;
  • Lee, Myeong Min ;
  • Lim, Jun
  • Received : 2018.08.29
  • Accepted : 2018.10.10
  • Published : 2018.12.31

Abstract

As sessile organisms, plants have evolved to adjust their growth and development to environmental changes. It has been well documented that the crosstalk between different plant hormones plays important roles in the coordination of growth and development of the plant. Here, we describe a novel recessive mutant, mildly insensitive to ethylene (mine), which displayed insensitivity to the ethylene precursor, ACC (1-aminocyclopropane-1-carboxylic acid), in the root under the dark-grown conditions. By contrast, mine roots exhibited a normal growth response to exogenous IAA (indole-3-acetic acid). Thus, it appears that the growth responses of mine to ACC and IAA resemble those of weak ethylene insensitive (wei) mutants. To understand the molecular events underlying the crosstalk between ethylene and auxin in the root, we identified the MINE locus and found that the MINE gene encodes the pyridoxine 5′-phosphate (PNP)/pyridoxamine 5′-phosphate (PMP) oxidase, PDX3. Our results revealed that MINE/PDX3 likely plays a role in the conversion of the auxin precursor tryptophan to indole-3-pyruvic acid in the auxin biosynthesis pathway, in which TAA1 (TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1) and its related genes (TRYPTOPHAN AMINOTRANSFERASE RELATED 1 and 2; TAR1 and TAR2) are involved. Considering that TAA1 and TARs belong to a subgroup of PLP (pyridoxal-5′-phosphate)-dependent enzymes, we propose that PLP produced by MINE/PDX3 acts as a cofactor in TAA1/TAR-dependent auxin biosynthesis induced by ethylene, which in turn influences the crosstalk between ethylene and auxin in the Arabidopsis root.

Keywords

Arabidopsis;auxin biosynthesis;ethylene;PDX3;PLP

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Fig. 1. The mine mutant shows root-specific insensitivity to ACC.

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Fig. 2. The mine mutant exhibits normal growth responses to IAA.

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Fig. 3. The mine mutant shows aberrant expression of auxin maxima monitored by DR5 under ACC treatment.

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Fig. 4. Genetic analysis of ethylene-induced auxin biosynthesis in mine roots.

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Fig. 5. The mine mutant exhibits retarded root growth under normal growth conditions.

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Fig. 6. The MINE gene encodes the PNP/PMP oxidase, PDX3.

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Fig. 7. Ethylene-insensitive responses of mine roots are restored by IAA, but not by Trp.

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Fig. 8. A schematic model for the involvement of MINE/PDX3 in ethylene-induced auxin biosynthesis.

References

  1. Abel, S., Nguyen, M.D., Chow, W., and Theologis, A. (1995). ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin [corrected]. J. Biol. Chem. 270, 19093-19099. Erratum. J. Biol. Chem. 270, 26020. https://doi.org/10.1074/jbc.270.32.19093
  2. Achard, P., Gusti, A., Cheminant, S., Alioua, M., Dhondt, S., Coppens, F., Beemster, G.T., and Genschik, P. (2009). Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr. Biol. 19, 1188-1193. https://doi.org/10.1016/j.cub.2009.05.059
  3. Alarcon, M.V., Lloret, P.G., and Salguero, J. (2014). Synergistic action of auxin and ethylene on root elongation inhibition is caused by a reduction of epidermal cell length. Plant Signal. Behav. 9, e28361. https://doi.org/10.4161/psb.28361
  4. Alonso, J.M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J.R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148-2152. https://doi.org/10.1126/science.284.5423.2148
  5. Alonso, J.M., Stepanova, A.N., Solano, R., Wisman, E., Ferrari, S., Ausubel, F.M., and Ecker, J.R. (2003). Five components of the ethylene-response pathway identified in a screen for weak ethylene insensitive mutants in Arabidopsis. Proc. Natl. Acad. Sci. USA 100, 2992-2997. https://doi.org/10.1073/pnas.0438070100
  6. Barlier, I., Kowalczyk, M., Marchant, A., Ljung, K., Bhalerao, R., Bennett, M., Sandberg, G., and Bellini, C. (2000). The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc. Natl. Acad. Sci. USA 97, 14819-14824. https://doi.org/10.1073/pnas.260502697
  7. Beemster, G.T.S., and Baskin, T.I. (1998). Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol. 116, 1515-1526. https://doi.org/10.1104/pp.116.4.1515
  8. Bleecker, A.B., Estelle, M.A., Somerville, C., and Kende, H. (1988). Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086-1090. https://doi.org/10.1126/science.241.4869.1086
  9. Bleecker, A.B., and Kende, H. (2000). Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16, 1-18. https://doi.org/10.1146/annurev.cellbio.16.1.1
  10. Boerjan, W., Cervera, M.T., Delarue, M., Beeckman, T., Dewitte, W., Bellini, C., Caboche, M., Onckelen, H.V., Montagu, M.V., and Inze, D. (1995). superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7, 1405-1419.
  11. Boycheva, S., Dominguez, A., Rolcik, J., Boller, T., and Fitzpatrick, T.B. (2015). Consequences of a deficit in vitamin $B_6$ biosynthesis de novo for hormone homeostasis and root development in Arabidopsis. Plant Physiol. 167, 102-117. https://doi.org/10.1104/pp.114.247767
  12. Chen, H., and Xiong, L. (2005). Pyridoxine is required for postembryonic root development and tolerance to osmotic and oxidative stresses. Plant J. 44, 396-408. https://doi.org/10.1111/j.1365-313X.2005.02538.x
  13. Chen, H., and Xiong, L. (2009a). Localized auxin biosynthesis and postembryonic root development in Arabidopsis. Plant Signal. Behav. 4, 752-754. https://doi.org/10.4161/psb.4.8.9177
  14. Chen, H., and Xiong, L. (2009b). The short-rooted vitamin $B_6$-deficient mutant pdx1 has impaired local auxin biosynthesis. Planta 229, 1303-1310. https://doi.org/10.1007/s00425-009-0912-8
  15. Choe, J.E., Kim, B., Yoon, E.K., Jang, S., Kim, G., Dhar, S., Lee, S.A., and Lim, J. (2017). Characterization of the GRAS transcription factor SCARECROW-LIKE 28's role in Arabidopsis root growth. J. Plant Biol. 60, 462-471. https://doi.org/10.1007/s12374-017-0112-1
  16. Clough, S., and Bent, A. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
  17. Colinas, M., Eisenhut, M., Tohge, T., Pesquera, M., Fernie, A.R., Weber, A.P., and Fitzpatrick, T.B. (2016). Balancing of $B_6$ vitamers is essential for plant development and metabolism in Arabidopsis. Plant Cell 28, 439-453. https://doi.org/10.1105/tpc.15.01033
  18. Curtis, M., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469. https://doi.org/10.1104/pp.103.027979
  19. Delarue, M., Prinsen, E., Onckelen, H.V., Caboche, M., and Bellini, C. (1998). Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J. 14, 603-611. https://doi.org/10.1046/j.1365-313X.1998.00163.x
  20. Dello Ioio, R., Linhares, F.S., Scacchi, E., Casamitjana-Martinez, E., Heidstra, R., Costantino, P., and Sabatini, S. (2007). Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 17, 678-682. https://doi.org/10.1016/j.cub.2007.02.047
  21. Denslow, S.A., Reuschhoff, E.E., and Daub, M.E. (2007). Regulation of the Arabidopsis thaliana vitamin $B_6$ biosynthesis genes by abiotic stress. Plant Physiol. Biochem. 45, 152-161. https://doi.org/10.1016/j.plaphy.2007.01.007
  22. Depuydt, S., and Hardtke, C.S. (2011). Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 21, R365-R373. https://doi.org/10.1016/j.cub.2011.03.013
  23. Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A., and Benfey, P.N. (1996). The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423-433. https://doi.org/10.1016/S0092-8674(00)80115-4
  24. Donnelly, P.M., Bonetta, D., Tsukaya, H., Dengler, R.E., and Dengler, N.G. (1999). Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215, 407-419. https://doi.org/10.1006/dbio.1999.9443
  25. Fitzpatrick, T.B., Amrhein, N., Kappes, B., Macheroux, P., Tews, I., and Raschle, T. (2007). Two independent routes of de novo vitamin $B_6$ biosynthesis: not that different after all. Biochem. J. 407, 1-13. https://doi.org/10.1042/BJ20070765
  26. Gallagher, K.L., Paquette, A.J., Nakajima, K., and Benfey, P.N. (2004). Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14, 1847-1851. https://doi.org/10.1016/j.cub.2004.09.081
  27. Gazzarrini, S.., and McCourt, P. (2003). Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann. Bot. 91, 605-612. https://doi.org/10.1093/aob/mcg064
  28. Gonzalez, E., Danehower, D., and Daub, M.E. (2007). Vitamer levels, stress response, enzyme activity, and gene regulation of Arabidopsis lines mutant in the pyridoxine/pyridoxamine 5′-phosphate oxidase (PDX3) and the pyridoxal kinase (SOS4) genes involved in the vitamin $B_6$ salvage pathway. Plant Physiol. 145, 985-996. https://doi.org/10.1104/pp.107.105189
  29. Guzman, P., and Ecker, J.R. (1990). Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523.
  30. He, W., Brumos, J., Li, H., Ji, Y., Ke, M., Gong, X., Zeng, Q., Li, W., Zhang, X., An, F., et al. (2011). A small-molecule screen identifies Lkynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23, 3944-3960. https://doi.org/10.1105/tpc.111.089029
  31. Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T., and Benfey, P.N. (2000). The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555-567. https://doi.org/10.1016/S0092-8674(00)80865-X
  32. Heo, J.O., Chang, K.S., Kim, I.A., Lee, M.-H., Lee, S.A., Song, S.K., Lee, M.M., and Lim, J. (2011). Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proc. Natl. Acad. Sci. USA 108, 2166-2171. https://doi.org/10.1073/pnas.1012215108
  33. Hong, J.H., Chu, H., Zhang, C., Ghosh, D., Gong, X., and Xu, J. (2015). A quantitative analysis of stem cell homeostasis in the Arabidopsis columella root cap. Front. Plant Sci. 6, 206.
  34. Huai, Q., Xia, Y., Chen, Y., Callahan, B., Li, N., and Ke, H. (2001). Crystal structures of 1-aminocyclopropane-1-carboxylate (ACC) synthase in complex with aminoethoxyvinylglycine and pyridoxal-5'-phosphate provide new insight into catalytic mechanisms. J. Biol. Chem. 276, 38210-38216.
  35. Konieczny, A., and Ausubel, F.M. (1993). A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCRbased markers. Plant J. 4, 403-410. https://doi.org/10.1046/j.1365-313X.1993.04020403.x
  36. Kotogany, E., Dudits, D., Horvath, G.V., and Ayaydin, F. (2010). A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine. Plant Methods 6, 5. https://doi.org/10.1186/1746-4811-6-5
  37. Le, J., Vandenbussche, F., Van Der Straeten, D., and Verbelen, J.P. (2001). In the early response of Arabidopsis roots to ethylene, cell elongation is up and down regulated and uncoupled from differentiation. Plant Physiol. 125, 519-522. https://doi.org/10.1104/pp.125.2.519
  38. Lee, S.A., Jang, S., Yoon, E.K., Heo, J.O., Chang, K.S., Choi, J.W., Dhar, S., Kim, G., Choe, J.-e., Heo, J.B., et al. (2016). Interplay between ABA and GA modulates the timing of asymmetric cell divisions in the Arabidopsis root ground tissue. Mol. Plant 9, 870-884. https://doi.org/10.1016/j.molp.2016.02.009
  39. Lee, S.A., Yoon, E.K., Heo, J.O., Lee, M.H., Hwang, I., Cheong, H., Lee, W.S., Hwang, Y.S., and Lim, J. (2012). Analysis of Arabidopsis glucose insensitive growth mutants reveals the involvement of the plastidial copper transporter PAA1 in glucose-induced intracellular signaling. Plant Physiol. 159, 1001-1012. https://doi.org/10.1104/pp.111.191726
  40. Liu, Y.G., Mitsukawa, N., Oosumi, T., and Whittier, R.F. (1995). Efficient isolation and mapping of Arabidopsis thaliana T‐DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457-463. https://doi.org/10.1046/j.1365-313X.1995.08030457.x
  41. Lukowitz, W., Gillmor, C.S., and Scheible, W.R. (2000). Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123, 795-805. https://doi.org/10.1104/pp.123.3.795
  42. Luschnig, C., Gaxiola, R., Grisafi, P., and Fink, G. (1998). EIR1, a root specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175-2187. https://doi.org/10.1101/gad.12.14.2175
  43. Nakajima, K., Sena, G., Nawy, T., and Benfey, P.N. (2001). Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307-311. https://doi.org/10.1038/35095061
  44. Pacurar, D.I., Pacurar, M.L., Bussell, J.D., Schwambach, J., Pop, T.I., Kowalczyk, M., Gutierrez, L., Cavel, E., Chaabouni, S., Ljung, K., et al. (2014). Identification of new adventitious rooting mutants amongst suppressors of the Arabidopsis thaliana superroot2 mutation. J. Exp. Bot. 65, 1605-18. https://doi.org/10.1093/jxb/eru026
  45. Percudani, R., and Peracchi, A. (2003). A genomic overview of pyridoxal-phosphate-dependent enzymes. EMBO Rep. 4, 850-854. https://doi.org/10.1038/sj.embor.embor914
  46. Pickett, F.B., Wilson, A.K., and Estelle, M. (1990). The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. 94, 1462-1466. https://doi.org/10.1104/pp.94.3.1462
  47. Robles, L., Stepanova, A.N., and Alonso J.M. (2013). Molecular mechanisms of ethylene-auxin interaction. Mol. Plant 6, 1734-1737. https://doi.org/10.1093/mp/sst113
  48. Roman, G., Lubarsky, B., Kieber, J. J., Rothenberg, M., and Ecker, J. R. (1995). Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139, 1393-1409.
  49. Rueschhoff, E.E., Gillikin, J.W., Sederoff, H.W., and Daub, M.E. (2013). The SOS4 pyridoxal kinase is required for maintenance of vitamin $B_6$-mediated processes in chloroplasts. Plant Physiol. Biochem. 63, 281-291. https://doi.org/10.1016/j.plaphy.2012.12.003
  50. Ruzicka, K., Ljung, K., Vanneste, S., Podhorska, R., Beeckman, T., Friml, J., and Benkova, E. (2007). Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19, 2197-2212. https://doi.org/10.1105/tpc.107.052126
  51. Sabatini, S., Heidstra, R., Wildwater, M., and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354-358. https://doi.org/10.1101/gad.252503
  52. Sang, Y., Barbosa, J.M., Wu, H., Locy, R.D., and Singh, N.K. (2007). Identification of a pyridoxine (pyridoxamine) 5′-phosphate oxidase from Arabidopsis thaliana. FEBS Lett. 581, 344-348. https://doi.org/10.1016/j.febslet.2006.12.028
  53. Sang, Y., Locy, R.D., Goertzen, L.R., Rashotte, A.M., Si, Y., Kang, K., and Singh, N.K. (2011). Expression, in vivo localization and phylogenetic analysis of a pyridoxine 5′-phosphate oxidase in Arabidopsis thaliana. Plant Physiol. Biochem. 49, 88-95. https://doi.org/10.1016/j.plaphy.2010.10.003
  54. Sarkar, A.K., Luijten, M., Miyashima, S., Lenhard, M., Hashimoto, T., Nakajima, K., Scheres, B., Heidstra, R., and Laux, T. (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811-814. https://doi.org/10.1038/nature05703
  55. Shi, H., Xiong, L., Stevenson, B., Lu, T., and Zhu, J.K. (2002). The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin $B_6$ in plant salt tolerance. Plant Cell 14, 575-588. https://doi.org/10.1105/tpc.010417
  56. Shi, H., and Zhu, J.K. (2002). SOS4, a pyridoxal kinase gene, is required for root hair development in Arabidopsis. Plant Physiol. 129, 585-593. https://doi.org/10.1104/pp.001982
  57. Soeno, K., Goda, H., Ishii, T., Ogura, T., Tachikawa, T., Sasaki, E., Yoshida, S., Fujioka, S., Asami, T., and Shimada, Y. (2010). Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis. Plant Cell Physiol. 51, 524-536. https://doi.org/10.1093/pcp/pcq032
  58. Stepanova, A.N., and Alonso, J.M. (2005). Ethylene signaling and response pathway: a unique signaling cascade with a multitude of inputs and outputs. Physiol. Plantarum 123, 195-206. https://doi.org/10.1111/j.1399-3054.2005.00447.x
  59. Stepanova, A.N., Hoyt, J.M., Hamilton, A.A., and Alonso, J.M. (2005). A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17, 2230-2242. https://doi.org/10.1105/tpc.105.033365
  60. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.Y., Dolezal, K., Schlereth, A., Jürgens, G., and Alonso, J.M. (2008). TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177-191. https://doi.org/10.1016/j.cell.2008.01.047
  61. Stepanova, A.N., Yun, J., Likhacheva, A.V., and Alonso, J.M. (2007). Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19, 2169-2185. https://doi.org/10.1105/tpc.107.052068
  62. Stepanova, A.N., Yun, J., Robles, L.M., Novak, O., He, W., Guo, H., Ljung, K., and Alonso, J.M. (2011). The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23, 3961-3973. https://doi.org/10.1105/tpc.111.088047
  63. Swarup, R., Parry, G., Graham, N., Allen, T., and Bennett, M. (2002). Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol. Biol. 49, 411-426.
  64. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M.J. (2007). Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19, 2186-2196. https://doi.org/10.1105/tpc.107.052100
  65. Tambasco-Studart, M., Titiz, O., Raschle, T., Forster, G., Amrhein, N., and Fitzpatrick, T.B. (2005). Vitamin $B_6$ biosynthesis in higher plants. Proc. Natl. Acad. Sci. USA 102, 13687-13692. https://doi.org/10.1073/pnas.0506228102
  66. Tao, Y., Ferrer, J.L., Ljung, K., Pojer, F., Hong, F., Long, J. A., Li, L., Moreno, J.E., Bowman, M.E., Ivans, L.J., et al. (2008). Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164-176. https://doi.org/10.1016/j.cell.2008.01.049
  67. Titiz, O., Tambasco-Studart, M., Warzych, E., Apel, K., Amrhein, N., Laloi, C., and Fitzpatrick, T.B. (2006). PDX1 is essential for vitamin $B_6$ biosynthesis, development and stress tolerance in Arabidopsis. Plant J. 48, 933-946. https://doi.org/10.1111/j.1365-313X.2006.02928.x
  68. Ubeda-Tomas, S., Federici, F., Casimiro, I., Beemster, G.T., Bhalerao, R., Swarup, R., Doerner, P., Haseloff, J., and Bennett, M.J. (2009). Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr. Biol. 19, 1194-1199. https://doi.org/10.1016/j.cub.2009.06.023
  69. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963-1971.
  70. Wagner, S., Bernhardt, A., Leuendorf, J.E., Drewke, C., Lytovchenko, A., Mujahed, N., Gurgui, C., Frommer, W.B., Leistner, E., Fernie, A.R., et al. (2006). Analysis of the Arabidopsis rsr4-1/pdx1-3 mutant reveals the critical function of the PDX1 protein family in metabolism, development, and vitamin $B_6$ biosynthesis. Plant Cell 18, 1722-1735. https://doi.org/10.1105/tpc.105.036269
  71. Waki, T., Miyashima, S., Nakanishi, M., Ikeda, Y., Hashimoto, T., and Nakajima, K. (2013). A GAL4-based targeted activation tagging system in Arabidopsis thaliana. Plant J. 73, 357-367. https://doi.org/10.1111/tpj.12049
  72. Wolters, H., and Jurgens, G. (2009). Survival of the flexible: hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 10, 305-317.
  73. Yoon, E.K., Dhar, S., Lee, M.H., Song, J.H., Lee, S.A., Kim, G., Jang, S., Choi, J.W., Choe, J.E., Kim, J.H., et al. (2016). Conservation and diversification of the SHR-SCR-SCL23 regulatory network in the development of the functional endodermis in Arabidopsis shoots. Mol. Plant 9, 1197-1209. https://doi.org/10.1016/j.molp.2016.06.007

Acknowledgement

Supported by : National Research Foundation