Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from Arabidopsis causes specific changes in root growth and xylem differentiation

Plant Journal

Volumn 78, Issue 3, 2014, Pages 359-371

  Köllmer, Ireen ^a   Novák, Ondřej ^b   Strnad, Miroslav ^b   Schmülling, Thomas ^a   Werner, Tomáš ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Arabidopsis thaliana; cytokinin; cytokinin oxidase dehydrogenase; cytosol; plant development; root meristem; xylem differentiation

Indexed keywords

GENES; PROTEINS; TISSUE;

ARABIDOPSIS THALIANA; CYTOKININ; CYTOKININ OXIDASE/DEHYDROGENASE; CYTOSOLS; PLANT DEVELOPMENT; ROOT MERISTEM; XYLEM DIFFERENTIATION;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; CKX7 PROTEIN, ARABIDOPSIS; CYTOKININ; GREEN FLUORESCENT PROTEIN; OXIDOREDUCTASE; PROTEIN KINASE; WOL PROTEIN, ARABIDOPSIS; ZEATIN;

ARABIDOPSIS; CELL DIFFERENTIATION; CYTOSOL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; PHYSIOLOGY; PLANT ROOT; SEEDLING; TRANSGENIC PLANT; XYLEM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIFFERENTIATION; CYTOKININS; CYTOSOL; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; MERISTEM; OXIDOREDUCTASES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN KINASES; RECEPTORS, CELL SURFACE; SEEDLING; XYLEM; ZEATIN;

EID: 84899655745     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12477     Document Type: Article

References (65)

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.
2. Bartrina, I., Otto, E., Strnad, M., Werner, T., and, Schmülling, T., (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell, 23, 69-80.
3. Becker, D., Kemper, E., Schell, J., and, Masterson, R., (1992) New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20, 1195-1197.
4. Bencivenga, S., Simonini, S., Benková, E., and, Colombo, L., (2012) The transcription factors BEL1 and SPL are required for cytokinin and auxin signaling during ovule development in Arabidopsis. Plant Cell, 24, 2886-2897.
5. Bishopp, A., Help, H., El-Showk, S., Weijers, D., Scheres, B., Friml, J., Benková, E., Mähönen, A.P., and, Helariutta, Y., (2011a) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 21, 917-926.
6. Bishopp, A., Lehesranta, S., Vatén, A., Help, H., El-Showk, S., Scheres, B., Helariutta, K., Mähönen, Ari.P., Sakakibara, H., and, Helariutta, Y., (2011b) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr. Biol. 21, 927-932.
7. Bradford, M.M., (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
8. Brenner, W.G., Romanov, G.A., Köllmer, I., Bürkle, L., and, Schmülling, T., (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J. 44, 314-333.
9. Cheng, C.-Y., Mathews, D., Eric Schaller, G., and, Kieber, J.J., (2013) Cytokinin-dependent specification of the functional megaspore in the Arabidopsis female gametophyte. Plant J. 73, 929-940.
10. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
11. Colõn-Carmona, A., You, R., Haimovitch-Gal, T., and, Doerner, P., (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J. 20, 503-508.
12. D'Agostino, I.B., Deruere, J., and, Kieber, J.J., (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 124, 1706-1717.
13. 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.
14. Dello Ioio, R., Linhares, F.S., and, Sabatini, S., (2008) Emerging role of cytokinin as a regulator of cellular differentiation. Curr. Opin. Plant Biol. 11, 23-27.
15. Dello Ioio, R., Galinha, C., Fletcher, A.G., et al. (2012) A PHABULOSA/cytokinin feedback loop controls root growth in Arabidopsis. Curr. Biol. 22, 1699-1704.
16. El Yacoubi, B., Bailly, M., and, de Crécy-Lagard, V., (2012) Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu. Rev. Genet. 46, 69-95.
17. Frébort, I., Šebela, M., Galuszka, P., Werner, T., Schmülling, T., and, Peč, P., (2002) Cytokinin oxidase/cytokinin dehydrogenase assay: optimized procedures and applications. Anal. Biochem. 306, 1-7.
18. Frébort, I., Kowalska, M., Hluska, T., Frébortová, J., and, Galuszka, P., (2011) Evolution of cytokinin biosynthesis and degradation. J. Exp. Bot. 62, 2431-2452.
19. Gajdošová, S., Spíchal, L., Kamínek, M., et al. (2011) Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J. Exp. Bot. 62, 2827-2840.
20. Galuszka, P., Frébortová, J., Werner, T., Yamada, M., Strnad, M., Schmülling, T., and, Frébort, I., (2004) Cytokinin oxidase/dehydrogenase genes in barley and wheat: cloning and heterologous expression. Eur. J. Biochem. 271, 3990-4002.
21. Galuszka, P., Popelková, H., Werner, T., Frébortová, J., Pospísilová, H., Mik, V., Köllmer, I., Schmülling, T., and, Frébort, I., (2007) Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. J. Plant Growth Regul. 26, 255-267.
22. García-Ponce de Leõn, B.G., Franco-Zorrilla, J.M., Rubio, V., Dahiya, P., Paz-Ares, J., and, Leyva, A., (2004) Interallelic complementation at the Arabidopsis CRE1 locus uncovers independent pathways for the proliferation of vascular initials and canonical cytokinin signalling. Plant J. 38, 70-79.
23. Gatz, C., Frohberg, C., and, Wendenburg, R., (1992) Stringent repression and homogeneous de-repression by tetracycline of a modified CaMV 35S promoter in intact transgenic tobacco plants. Plant J. 2, 397-404.
24. Gu, R., Fu, J., Guo, S., Duan, F., Wang, Z., Mi, G., and, Yuan, L., (2010) Comparative expression and phylogenetic analysis of maize cytokinin dehydrogenase/oxidase (CKX) gene family. J. Plant Growth Regul. 29, 428-440.
25. Higuchi, M., Pischke, M.S., Mähönen, A.P., et al. (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc. Natl Acad. Sci. USA, 101, 8821-8826.
26. Hirose, N., Takei, K., Kuroha, T., Kamada-Nobusada, T., Hayashi, H., and, Sakakibara, H., (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 59, 75-83.
27. Hutchison, C.E., Li, J., Argueso, C., et al. (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell, 18, 3073-3087.
28. Hwang, I., Sheen, J., and, Müller, B., (2012) Cytokinin signaling networks. Annu. Rev. Plant Biol. 63, 353-380.
29. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., and, Kakimoto, T., (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature, 409, 1060-1063.
30. Kasahara, H., Takei, K., Ueda, N., Hishiyama, S., Yamaya, T., Kamiya, Y., Yamaguchi, S., and, Sakakibara, H., (2004) Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in Arabidopsis. J. Biol. Chem. 279, 14049-14054.
31. Kinoshita-Tsujimura, K., and, Kakimoto, T., (2011) Cytokinin receptors in sporophytes are essential for male and female functions in Arabidopsis thaliana. Plant Signal. Behav. 6, 66-71.
32. Kondo, Y., Hirakawa, Y., Kieber, J.J., and, Fukuda, H., (2011) CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol. 52, 37-48.
33. Kowalska, M., Galuszka, P., Frébortová, J., Šebela, M., Béres, T., Hluska, T., Šmehilová, M., Bilyeu, K.D., and, Frébort, I., (2010) Vacuolar and cytosolic cytokinin dehydrogenases of Arabidopsis thaliana: Heterologous expression, purification and properties. Phytochemistry, 71, 1970-1978.
34. Kudo, T., Makita, N., Kojima, M., Tokunaga, H., and, Sakakibara, H., (2012) Cytokinin activity of cis-zeatin and phenotypic alterations induced by overexpression of putative cis-zeatin-O-glucosyltransferase in rice. Plant Physiol. 160, 319-331.
35. Kuroha, T., Ueguchi, C., Sakakibara, H., and, Satoh, S., (2006) Cytokinin receptors are required for normal development of auxin-transporting vascular tissues in the hypocotyl but not in adventitious roots. Plant Cell Physiol. 47, 234-243.
36. Laplaze, L., Benková, E., Casimiro, I., et al. (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell, 19, 3889-3900.
37. Mähönen, A.P., Bonke, M., Kauppinen, L., Riikonen, M., Benfey, P.N., and, Helariutta, Y., (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938-2943.
38. Mähönen, A.P., Higuchi, M., Tormakangas, K., Miyawaki, K., Pischke, M.S., Sussman, M.R., Helariutta, Y., and, Kakimoto, T., (2006a) Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr. Biol. 16, 1116-1122.
39. Mähönen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Tormakangas, K., Ikeda, Y., Oka, A., Kakimoto, T., and, Helariutta, Y., (2006b) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science, 311, 94-98.
40. Malamy, J., and, Benfey, P., (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development, 124, 33-44.
41. 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.
42. Miyashima, S., Sebastian, J., Lee, J.-Y., and, Helariutta, Y., (2013) Stem cell function during plant vascular development. EMBO J. 32, 178-193.
43. Miyawaki, K., Matsumoto-Kitano, M., and, Kakimoto, T., (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 37, 128-138.
44. Miyawaki, K., Tarkowski, P., Matsumoto-Kitano, M., Kato, T., Sato, S., Tarkowska, D., Tabata, S., Sandberg, G., and, Kakimoto, T., (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl Acad. Sci. USA, 103, 16598-16603.
45. Müller, B., and, Sheen, J., (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature, 453, 1094-1097.
46. Murashige, T., and, Skoog, F., (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
47. Nishimura, C., Ohashi, Y., Sato, S., Kato, T., Tabata, S., and, Ueguchi, C., (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell, 16, 1365-1377.
48. Novák, O., Tarkowski, P., Tarkowska, D., Doležal, K., Lenobel, R., and, Strnad, M., (2003) Quantitative analysis of cytokinins in plants by liquid chromatography-single-quadrupole mass spectrometry. Anal. Chim. Acta, 480, 207-218.
49. Ren, B., Chen, Q., Hong, S., Zhao, W., Feng, J., Feng, H., and, Zuo, J., (2013) The Arabidopsis eukaryotic translation initiation factor eIF5A-2 regulates root protoxylem development by modulating cytokinin signaling. Plant Cell, 25, 3841-3857.
50. Riefler, M., Novak, O., Strnad, M., and, Schmülling, T., (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell, 18, 40-54.
51. Romanov, G.A., Spíchal, L., Lomin, S.N., Strnad, M., and, Schmülling, T., (2005) A live cell hormone-binding assay on transgenic bacteria expressing a eukaryotic receptor protein. Anal. Biochem. 347, 129-134.
52. Růžička, K., Simásková, M., Duclercq, J., Petrásek, J., Zazímalová, E., Simon, S., Friml, J., Van Montagu, M.C.E., and, Benková, E., (2009) Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl Acad. Sci. USA, 106, 4284-4289.
53. Scheres, B., Di Laurenzio, L., Willemsen, V., Hauser, M.T., Janmaat, K., Weisbeek, P., and, Benfey, P.N., (1995) Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development, 121, 53-62.
54. Schmitz, R.Y., Skoog, F., Playtis, A.J., and, Leonard, N.J., (1972) Cytokinins: synthesis and biological activity of geometric and position isomers of zeatin. Plant Physiol. 50, 702-705.
55. Schmülling, T., Werner, T., Riefler, M., Krupková, E., and, Bartrina y Manns, I., (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J. Plant. Res. 116, 241-252.
56. Šmehilová, M., Galuszka, P., Bilyeu, K.D., Jaworek, P., Kowalska, M., Šebela, M., Sedlářová, M., English, J.T., and, Frébort, I., (2009) Subcellular localization and biochemical comparison of cytosolic and secreted cytokinin dehydrogenase enzymes from maize. J. Exp. Bot. 60, 2701-2712.
57. Spíchal, L., Rakova, N.Y., Riefler, M., Mizuno, T., Romanov, G.A., Strnad, M., and, Schmülling, T., (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol. 45, 1299-1305.
58. Werner, T., and, Schmülling, T., (2009) Cytokinin action in plant development. Curr. Opin. Plant Biol. 12, 527-538.
59. Werner, T., Motyka, V., Strnad, M., and, Schmülling, T., (2001) Regulation of plant growth by cytokinin. Proc. Natl Acad. Sci. USA, 98, 10487-10492.
60. Werner, T., Motyka, V., Laucou, V., Smets, R., Van Onckelen, H., and, Schmülling, T., (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell, 15, 2532-2550.
61. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T., and, Mizuno, T., (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017-1023.
62. Yang, S., Yu, H., Xu, Y., and, Goh, C.J., (2003) Investigation of cytokinin-deficient phenotypes in Arabidopsis by ectopic expression of orchid DSCKX1. FEBS Lett. 555, 291-296.
63. Yokoyama, A., Yamashino, T., Amano, Y.-I., Tajima, Y., Imamura, A., Sakakibara, H., and, Mizuno, T., (2007) Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. Plant Cell Physiol. 48, 84-96.
64. Yonekura-Sakakibara, K., Kojima, M., Yamaya, T., and, Sakakibara, H., (2004) Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol. 134, 1654-1661.
65. Zürcher, E., Tavor-Deslex, D., Lituiev, D., Enkeli, K., Tarr, P.T., and, Müller, B., (2013) A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol. 161, 1066-1075.