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http://dx.doi.org/10.14348/molcells.2018.0363

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

Kim, Gyuree (Department of Systems Biotechnology, Konkuk University)
Jang, Sejeong (Department of Systems Biotechnology, Konkuk University)
Yoon, Eun Kyung (Department of Systems Biotechnology, Konkuk University)
Lee, Shin Ae (Department of Systems Biotechnology, Konkuk University)
Dhar, Souvik (Department of Systems Biotechnology, Konkuk University)
Kim, Jinkwon (Department of Systems Biotechnology, Konkuk University)
Lee, Myeong Min (Department of Systems Biology, Yonsei University)
Lim, Jun (Department of Systems Biotechnology, Konkuk University)
Publication Information
Molecules and Cells / v.41, no.12, 2018 , pp. 1033-1044 More about this Journal
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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1 Gallagher, K.L., Paquette, A.J., Nakajima, K., and Benfey, P.N. (2004). Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14, 1847-1851.   DOI
2 Gazzarrini, S.., and McCourt, P. (2003). Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Ann. Bot. 91, 605-612.   DOI
3 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.   DOI
4 Guzman, P., and Ecker, J.R. (1990). Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2, 513-523.
5 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.   DOI
6 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.   DOI
7 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.   DOI
8 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.
9 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.   DOI
10 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.   DOI
11 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.   DOI
12 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.   DOI
13 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.   DOI
14 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.
15 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.   DOI
16 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.   DOI
17 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.   DOI
18 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.   DOI
19 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.   DOI
20 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.   DOI
21 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.   DOI
22 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.   DOI
23 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.   DOI
24 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.   DOI
25 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.
26 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.   DOI
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 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.   DOI
32 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.   DOI
33 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.   DOI
34 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.   DOI
35 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.
36 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.   DOI
37 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.   DOI
38 Wolters, H., and Jurgens, G. (2009). Survival of the flexible: hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 10, 305-317.
39 Bleecker, A.B., and Kende, H. (2000). Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 16, 1-18.   DOI
40 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.   DOI
41 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.
42 Chen, H., and Xiong, L. (2009b). The short-rooted vitamin $B_6$-deficient mutant pdx1 has impaired local auxin biosynthesis. Planta 229, 1303-1310.   DOI
43 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.   DOI
44 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.   DOI
45 Chen, H., and Xiong, L. (2009a). Localized auxin biosynthesis and postembryonic root development in Arabidopsis. Plant Signal. Behav. 4, 752-754.   DOI
46 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.   DOI
47 Clough, S., and Bent, A. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.   DOI
48 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.   DOI
49 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.   DOI
50 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.   DOI
51 Percudani, R., and Peracchi, A. (2003). A genomic overview of pyridoxal-phosphate-dependent enzymes. EMBO Rep. 4, 850-854.   DOI
52 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.   DOI
53 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.   DOI
54 Robles, L., Stepanova, A.N., and Alonso J.M. (2013). Molecular mechanisms of ethylene-auxin interaction. Mol. Plant 6, 1734-1737.   DOI
55 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.
56 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.   DOI
57 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.   DOI
58 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.   DOI
59 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.   DOI
60 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.   DOI
61 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.   DOI
62 Depuydt, S., and Hardtke, C.S. (2011). Hormone signalling crosstalk in plant growth regulation. Curr. Biol. 21, R365-R373.   DOI
63 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.   DOI
64 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.   DOI
65 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.   DOI
66 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.   DOI
67 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.   DOI
68 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.   DOI
69 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.   DOI
70 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.   DOI
71 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.   DOI
72 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.   DOI
73 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.   DOI