Arabidopsis Histidine-containing Phosphotransfer Factor 4 (AHP4) Negatively Regulates Secondary Wall Thickening of the Anther Endothecium during Flowering

  • Jung, Kwang Wook (School of Life Sciences and Biotechnology, Korea University) ;
  • Oh, Seung-Ick (School of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Yun Young (School of Life Sciences and Biotechnology, Korea University) ;
  • Yoo, Kyoung Shin (School of Life Sciences and Biotechnology, Korea University) ;
  • Cui, Mei Hua (School of Life Sciences and Biotechnology, Korea University) ;
  • Shin, Jeong Sheop (School of Life Sciences and Biotechnology, Korea University)
  • Received : 2007.08.14
  • Accepted : 2007.09.27
  • Published : 2008.04.30

Abstract

Cytokinins are essential hormones in plant development. $\underline{A}$rabidopsis $\underline{h}$istidine-containing $\underline{p}$hosphotransfer proteins (AHPs) are mediators in a multistep phosphorelay pathway for cytokinin signaling. The exact role of AHP4 has not been elucidated. In this study, we demonstrated young flower-specific expression of AHP4, and compared AHP4-overexpressing (Ox) trangenic Arabidopsis lines and an ahp4 knock-out line. AHP4-Ox plants had reduced fertility due to a lack of secondary cell wall thickening in the anther endothecium and inhibition of IRREGURAR XYLEMs (IRXs) expression in young flowers. Conversely, ahp4 anthers had more lignified anther walls than the wild type, and increased IRXs expression. Our study indicates that AHP4 negatively regulates thickening of the secondary cell wall of the anther endothecium, and provides new insight into the role of cytokinins in formation of secondary cell walls via the action of AHP4.

Keywords

AHPs;Anther Dehiscence;Arabidopsis;Cytokinin;Reduced Fertility;Secondary Wall

Acknowledgement

Supported by : Ministry of Science and Technology

References

  1. Liljegren, S.J., Roeder, A.H., Kempin, S.A., Gremski, K., Ostergaard, L., Guimil, S., Reyes, D.K., and Yanofsky, M.F. (2004). Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116, 843-853 https://doi.org/10.1016/S0092-8674(04)00217-X
  2. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco culture. Physiol. Plant 15, 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
  3. Werner, T., Motyka, V., Laucou, V., Smets, R., Van Onckelen, H., and Schmulling, 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 https://doi.org/10.1105/tpc.014928
  4. Jung, J.H., Yun, J., Seo, Y.H., and Park, C.M. (2005). Characterization of an Arabidopsis gene that mediates cytokinin signaling in shoot apical meristem development. Mol. Cells 19, 342-349
  5. Taylor, N.G., Howells, R.M., Huttly, A.K., Vickers, K., and Turner, S.R. (2003). Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. USA 100, 1450-1455
  6. Brown, D.M., Zeef, L.A., Ellis, J., Goodacre, R., and Turner, S.R. (2005). Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17, 2281-2295 https://doi.org/10.1105/tpc.105.031542
  7. Goldberg, R.B., Beals, T.P., and Sanders, P.M. (1993). Anther development: basic principles and practical applications. Plant Cell 5, 1217-1229 https://doi.org/10.1105/tpc.5.10.1217
  8. Yang, C., Xu, Z., Song, J., Conner, K., Vizcay Barrena, G., and Wilson, Z.A. (2007). Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. Plant Cell 19, 534-548 https://doi.org/10.1105/tpc.106.046391
  9. 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 https://doi.org/10.1046/j.1365-313x.1998.00343.x
  10. Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2005). The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17, 2993-3006 https://doi.org/10.1105/tpc.105.036004
  11. Riefler, M., Novak, O., Strnad, M., and Schmulling, 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 https://doi.org/10.1105/tpc.105.037796
  12. Mok, D.W., and Mok, M.C. (2001). Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 89-118 https://doi.org/10.1146/annurev.arplant.52.1.89
  13. Fukuda, H. (2004). Signals that control plant vascular cell differentiation. Nat. Rev. Mol. Cell Biol. 5, 379-391 https://doi.org/10.1038/nrm1364
  14. Hutchison, C.E., Li, J., Argueso, C., Gonzalez, M., Lee, E., Lewis, M.W., Maxwell, B.B., Perdue, T.D., Schaller, G.E., Alonso, J.M., et al. (2006). The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18, 3073-3087 https://doi.org/10.1105/tpc.106.045674
  15. Suzuki, T., Sakurai, K., Imamura, A., Nakamura, A., Ueguchi, C., and Mizuno, T. (2000). Compilation and characterization of histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in plants: AHP signal transducers of Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 64, 2486-2489 https://doi.org/10.1271/bbb.64.2486
  16. 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 https://doi.org/10.1038/35059117
  17. Miyata, S., Urao, T., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). Characterization of genes for two-component phosphorelay mediators with a single HPt domain in Arabidopsis thaliana. FEBS Lett. 437, 11-14 https://doi.org/10.1016/S0014-5793(98)01188-0
  18. Oka, A., Sakai, H., and Iwakoshi, S. (2002). His-Asp phosphorelay signal transduction in higher plants: receptors and response regulators for cytokinin signaling in Arabidopsis thaliana. Genes Genet. Syst. 77, 383-391 https://doi.org/10.1266/ggs.77.383
  19. Mahonen, 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 https://doi.org/10.1101/gad.189200
  20. Taylor, N.G., Scheible, W.R., Cutler, S., Somerville, C.R., and Turner, S.R. (1999). The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11, 769-780 https://doi.org/10.1105/tpc.11.5.769
  21. Ye, Z.H. (2002). Vascular tissue differentiation and pattern formation in plants. Annu. Rev. Plant Biol. 53, 183-202 https://doi.org/10.1146/annurev.arplant.53.100301.135245
  22. Kiba, T., Aoki, K., Sakakibara, H., and Mizuno, T. (2004). Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the wol cytokininreceptor mutant. Plant Cell Physiol. 45, 1063-1077 https://doi.org/10.1093/pcp/pch128
  23. 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 https://doi.org/10.1093/pcp/pci240
  24. Mitsuda, N., Iwase, A., Yamamoto, H., Yoshida, M., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2007). NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19, 270-280 https://doi.org/10.1105/tpc.106.047043
  25. Yamada, H., Koizumi, N., Nakamichi, N., Kiba, T., Yamashino, T., and Mizuno, T. (2004). Rapid response of Arabidopsis T87 cultured cells to cytokinin through His-to-Asp phosphorelay signal transduction. Biosci. Biotechnol. Biochem. 68, 1966-1976 https://doi.org/10.1271/bbb.68.1966
  26. 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 https://doi.org/10.1104/pp.124.4.1706
  27. Gattolin, S., Alandete-Saez, M., Elliott, K., Gonzalez-Carranza, Z., Naomab, E., Powell, C., and Roberts, J.A. (2006). Spatial and temporal expression of the response regulators ARR22 and ARR24 in Arabidopsis thaliana. J. Exp. Bot. 57, 4225-4233 https://doi.org/10.1093/jxb/erl205
  28. Tanaka, Y., Suzuki, T., Yamashino, T., and Mizuno, T. (2004). Comparative studies of the AHP histidine-containing phosphotransmitters implicated in His-to-Asp phosphorelay in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 68, 462-465 https://doi.org/10.1271/bbb.68.462
  29. Mahonen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Tormakangas, K., Ikeda, Y., Oka, A., Kakimoto, T., and Helariutta, Y. (2006). Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94-98 https://doi.org/10.1126/science.1118875