An Arabidopsis Homologue of Human Seven-in-Absentia-interacting Protein Is Involved in Pathogen Resistance

  • Kim, Youn-Sung (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Ham, Byung-Kook (School of Life Sciences and Biotechnology, Korea University) ;
  • Paek, Kyung-Hee (School of Life Sciences and Biotechnology, Korea University) ;
  • Park, Chung-Mo (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Chua, Nam-Hai (Laboratory of Plant Molecular Biology, Rockefeller University)
  • Received : 2006.02.06
  • Accepted : 2006.05.03
  • Published : 2006.06.30

Abstract

Human seven-in-absentia (SIAH)-interacting protein (SIP) is a component of the E3 ligase complex targeting beta-catenin for destruction. Arabidopsis has one SIP protein (AtSIP) with 32% amino acid sequence identity to SIP. To investigate the functions of AtSIP, we isolated an atsip knockout mutant, and generated transgenic plants overexpressing AtSIP. The growth rates and morphologies of the atsip and transgenic plants were indistinguishable from those of wild type. However, atsip plants were more susceptible to Pseudomonas syringae infection, and the transgenic plants overexpressing AtSIP were more resistant. Consistent with this, RNA blot analysis showed that the AtSIP gene is strongly induced by wounding and hydrogen peroxide treatment. In addition, when plants were infected with P. syringae, AtSIP was transiently induced prior to PR-1 induction. These observations show that Arabidopsis AtSIP plays a role in resistance to pathogenic infection.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation

References

  1. Austin, M. J., Muskett, P., Kahn, K., Feys, B. J., Jones, J. D. G., et al. (2002) Regulatory role of SGT1 in early R genemediated plant defenses. Science 295, 2077-2080 https://doi.org/10.1126/science.1067747
  2. Bursen, A., Moritz, S., Gaussmann, A., Dingermann, T., and Marschalek, R. (2004) Interaction of AF4 wild-type and AF4.MLL fusion protein with SIAH proteins: indication for t(4;11) pathobiology. Oncogene 23, 6237-6249 https://doi.org/10.1038/sj.onc.1207837
  3. Clough, S. J. and Bent, A. F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arbidopsis thaliana. Plant J. 16, 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x
  4. DeMoraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T., and Tumlinson, J. H. (1998) Hebivore-infested plants selectively attract parasitoids. Nature 393, 570-573 https://doi.org/10.1038/31219
  5. Filipek, A., Jastrzebska, B., Nowotny, M., Kwiatkowska, K., Hetman, M., et al. (2002) Ca2+-dependent translocation of the calcyclin-binding protein in neurons and neuoblastoma NB-2a cells. J. Biol. Chem. 277, 21103-21109 https://doi.org/10.1074/jbc.M111010200
  6. Germani, A., Romero, F., Houlard, M., Camonis, J., Gisselbrecht, S., et al. (1999) hSiah2 is a new Vav binding protein which inhibits Vav-mediated signaling pathways. Mol. Cell Biol. 19, 3798-3807 https://doi.org/10.1128/MCB.19.5.3798
  7. Germani, A., Bruzzoni-Giovanelli, H., Fellous, A., Gisselbrecht, S., Varin-Blank, N., et al. (2000) SIAH-1 interacts with alpha- tubulin and degrades the kinesin Kid by the proteasome pathway during mitosis. Oncogene 19, 5997-6006 https://doi.org/10.1038/sj.onc.1204002
  8. Grant, J. J. and Loake, G. J. (2000) Role of ROIs and cognate redox signaling in disease resistance. Plant Physiol. 124, 21-29 https://doi.org/10.1104/pp.124.1.21
  9. Gray, W. M., Muskett, P. R., Chuang, H., and Parker, J. E. (2003) Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. Plant Cell 15, 1310-1319 https://doi.org/10.1105/tpc.010884
  10. House, C. M., Frew, I. J., Huang, H. L., Wiche, G., Traficante, N., et al. (2003) A binding motif for Siah ubiquitin ligase. Proc. Natl. Acad. Sci. USA 100, 3101-3106 https://doi.org/10.1073/pnas.0534783100
  11. Hu, G., Chung, Y. L., Glover, T., Valentine, V., Look, A. T., et al. (1997) Characterization of human homologs of the Drosophila seven in absentia (sina) gene. Genomics 46, 103-111 https://doi.org/10.1006/geno.1997.4997
  12. Hui, D., Iqbal, J., Lehmann, K., Gase, K., Saluz, H. P., et al. (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural Nicotiana attenuate. V. Microarray analysis and further characterization of large scale changes in heibivore-induced mRNAs. Plant Physiol. 131, 1877-1893 https://doi.org/10.1104/pp.102.018176
  13. Jabs, T., Tschope, M., Colling, C., Hahlbrock, K., and Scheel, D. (1997) Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsely. Proc. Natl.Acad. Sci. USA 94, 4800-4805 https://doi.org/10.1073/pnas.94.9.4800
  14. Klüsener, B., Young, J. J., Murata, Y., Allen, G. J., Mori, I. C., et al. (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol. 130, 2152-2163 https://doi.org/10.1104/pp.012187
  15. Kost, B., Spielhofer, P., and Chua, N. H. (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J. 16, 393-401 https://doi.org/10.1046/j.1365-313x.1998.00304.x
  16. Kuo, H. F., Tsai, Y. F., Young, L. S., and Lin, C. Y. (2000) Ethanol treatment triggers a heat shock-like response but no thermotolerance in soybean (Glycine max cv. Kaohsiung No. 8) seedlings. Plant Cell Environ. 23, 1099-1108 https://doi.org/10.1046/j.1365-3040.2000.00621.x
  17. Levine, A., Pennell, R. I., Alvarez, M. E., Palmer, R., and Lamb, C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427-437 https://doi.org/10.1016/S0960-9822(02)00510-9
  18. Maffei, M., Bossi, S., Spiteller, D., Mithöfer, A., and Boland, W. (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol. 134, 1752-1762 https://doi.org/10.1104/pp.103.034165
  19. Matsuzawa, S. and Reed, J. C. (2001) Siah-1, SIP, and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol. Cell 7, 915-926 https://doi.org/10.1016/S1097-2765(01)00242-8
  20. Matsuzawa, S., Takayama, S., Froesch, B., Zapata, J. M., and Reed, J. C. (1998) p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by BAG-1. EMBO J. 17, 2736-2747 https://doi.org/10.1093/emboj/17.10.2736
  21. Moller, S. G., Kim, Y. S., Kunkel, T., and Chua, N. H. (2003) PP7 is a positive regulator of blue light signaling in Arabidopsis. Plant Cell 15, 1111-1119 https://doi.org/10.1105/tpc.008649
  22. Oliver, P. L., Bitoun, E., Clark, J., Jones, E. L., and Davies, K. E. (2004) Mediation of Af4 protein function in the cerebellum by Siah proteins. Proc. Natl. Acad. Sci. USA 101, 14901- 14906 https://doi.org/10.1073/pnas.0406196101
  23. Orozco-Cardenas, M. and Ryan, C. A. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 96, 6553-6557 https://doi.org/10.1073/pnas.96.11.6553
  24. Park, T. J., Hamanaka, H., Ohshima, T., Watanabe, N., Mikoshiba, K., et al. (2003) Inhibition of ubiquitin ligase Siah-1A by disabled-1. Biochem. Biophys. Res. Commun. 302, 671- 678 https://doi.org/10.1016/S0006-291X(03)00247-X
  25. Park, C. Y., Heo, W. D., Yoo, J. H., Lee, J. H., Kim, M. C., et al. (2004) Pathogenesis-related gene expression by specific calmodulin isoforms is dependent on NIM1, a key regulator of systemic acquired resistance. Mol. Cells 18, 207-213
  26. Santelli, E., Leone, M., Li, C., Fukushima, T., Preece, N. E., et al. (2005) Structural analysis of Siah1-Siah-interacting protein interactions and insights into the assembly of an E3 ligase multiprotein complex. J. Biol. Chem. 280, 34278-34287 https://doi.org/10.1074/jbc.M506707200
  27. Sisini, L., Passer, B. J., Amzallag-Elbaz, N., Juven-Gershon, T., Prieur, S., et al. (2001) Siah-1 binds and regulates the function of Numb. Proc. Natl. Acad. Sci. USA 98, 15067-15072 https://doi.org/10.1073/pnas.261571998
  28. Song, J. T., Lu, H., McDowell, J. M., and Greenberg, J. T. (2004) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 40, 200-212 https://doi.org/10.1111/j.1365-313X.2004.02200.x
  29. Tanikawa, J., Ichikawa-Iwata, E., Kanei-Ishii, C., Nakai, A., Matsukawa, S. I., et al. (2000) p53 suppresses the c-Mybinduced activation of heat shock transcription factor 3. J. Biol. Chem. 275, 15578-15585 https://doi.org/10.1074/jbc.M000372200
  30. Tor, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., et al. (2002) Arabidopsis SGT1b is required for defense signaling conferred by several downy mildew resistance genes. Plant Cell 14, 993-1003 https://doi.org/10.1105/tpc.001123
  31. Xie, Q., Guo, H. S., Dallman, G., Fang, S., Weissman, A. M., et al. (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167-170 https://doi.org/10.1038/nature00998
  32. Zhang, J., Guenther, M. G., Carthew, R. W., and Lazar, M. A. (1998) Proteasomal regulation of nuclear receptor corepressor- mediated repression. Genes Dev. 12, 1775-1780 https://doi.org/10.1101/gad.12.12.1775