Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Structure and Expression of OsUBP6, an Ubiquitin-Specific Protease 6 Homolog in Rice (Oryza sativa L.)

  • Moon, Yea Kyung (Department of Biology, College of Life Science and Biotechnology, Yonsei University) ;
  • Hong, Jong-Pil (Department of Biology, College of Life Science and Biotechnology, Yonsei University) ;
  • Cho, Young-Chan (Rice Research Division, National Institute of Crop Science, Rural Development Administration) ;
  • Yang, Sae-Jun (Rice Research Division, National Institute of Crop Science, Rural Development Administration) ;
  • An, Gynheung (Department of Life Science, Pohang University of Science and Technology) ;
  • Kim, Woo Taek (Department of Biology, College of Life Science and Biotechnology, Yonsei University)
  • Received : 2009.07.30
  • Accepted : 2009.09.02
  • Published : 2009.11.30
⟨ Previous Next ⟩

Abstract

Although the possible cellular roles of several ubiquitin-specific proteases (UBPs) were identified in Arabidopsis, almost nothing is known about UBP homologs in rice, a monocot model plant. In this report, we searched the rice genome database (http://signal.salk.edu/cgi-bin/RiceGE) and identified 21 putative UBP family members (OsUBPs) in the rice genome. These OsUBP genes each contain a ubiquitin carboxyl-terminal hydrolase (UCH) domain with highly conserved Cys and His boxes and were subdivided into 9 groups based on their sequence identities and domain structures. RT-PCR analysis indicated that rice OsUBP genes are expressed at varying degrees in different rice tissues. We isolated a full-length cDNA clone for OsUBP6, which possesses not only a UCH domain, but also an N-terminal ubiquitin motif. Bacterially expressed OsUBP6 was capable of dismantling K48-linked tetra-ubiquitin chains in vitro. Quantitative real-time RT-PCR indicated that OsUBP6 is constitutively expressed in different tissues of rice plants. An in vivo targeting experiment showed that OsUBP6 is predominantly localized to the nucleus in onion epidermal cells. We also examined how knock-out of OsUBP6 affects developmental growth of rice plants. Although homozygous T3 osubp6 T-DNA insertion mutant seedlings displayed slower growth relative to wild type seedlings, mature mutant plants appeared to be normal. These results raise the possibility that loss of OsUBP6 is functionally compensated for by an as-yet unknown OsUBP homolog during later stages of development in rice plants.

Keywords

Acknowledgement

Supported by : National Research Foundation, Rural Development Administration

References

  1. An, S., Park, S., Jeong, D.H., Lee, D.Y., Kang, H.G., Yu, J.H., Hur, J., Kim, S.R., Kim, Y.H., Lee, M., et al. (2003). Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiol. 133, 2040-2047 https://doi.org/10.1104/pp.103.030478
  2. Bonnet, J., Romier, C., Tora, L., and Devys, D. (2008). Trends Biochem. Sci. 33, 369-375 https://doi.org/10.1016/j.tibs.2008.05.005
  3. Byun, M.Y., Hong, J.-P., and Kim, W.T. (2008). Identification and characterization of three telomere repeat-binding factors in rice. Biochem. Biophys. Res. Commun. 372, 85-90 https://doi.org/10.1016/j.bbrc.2008.04.181
  4. Cho, S.K., Ryu, M.Y., Song, C., Kwak, J.M., and Kim, W.T. (2008). Arabidopsis PUB22 and PUB23 are homologous U-box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20, 1899-1914 https://doi.org/10.1105/tpc.108.060699
  5. Doelling, J.H., Yan, N., Kurepa, J., Walker, J., and Vierstra, R.D. (2001). The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J. 27, 393-405 https://doi.org/10.1046/j.1365-313X.2001.01106.x
  6. Doelling, J.H., Phillips, A.R., Soyler-Ogretim, G., Wise, J., Chandler, J., Callis, J., Otegui, M.S., and Vierstra, R.D. (2007). The ubiquitin- specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis. Plant Physiol. 145, 801-813 https://doi.org/10.1104/pp.106.095323
  7. Dreher, K., and Callis, J. (2007). Ubiquitin, hormones and biotic stress in plants. Ann. Bot. 99, 787-822 https://doi.org/10.1093/aob/mcl255
  8. Glickman, M.H., and Ciechanover, A. (2002). The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82, 373-428
  9. Hong, J.-P., Kim, S.M., Ryu, M.Y., Choe, S., Park, P.B., An, G., and Kim, W.T. (2005). Structure and expression of OsMRE11 in rice. J. Plant Biol. 48, 229-236 https://doi.org/10.1007/BF03030412
  10. Hong, J.-P., Byun, M.Y., Koo, D., An, K., Bang, J., Chung, I.K., An, G., and Kim, W.T. (2007). Suppression of rice telomere binding protein1 results in severe and gradual developmental de-fects accompanied by genome instability in rice. Plant Cell 19, 1770-1781 https://doi.org/10.1105/tpc.107.051953
  11. Hu, M., Li, P., Song, L., Jeffrey, P.D., Chernova, T.A., Wilkinson, K.D., Cohen, R.E., and Shi, Y. (2005). Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J. 24, 3747-3756 https://doi.org/10.1038/sj.emboj.7600832
  12. Jeon, J.S., Lee, S., Jung, K.H., Jun, S.H., Jeong, D.H., Lee, J., Kim, C., Jang, S., Yang, K., Nam, J., et al. (2000). T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 22, 561-570 https://doi.org/10.1046/j.1365-313x.2000.00767.x
  13. Joo, S., and Kim, W.T. (2007). A gaseous plant hormone ethylene: The signaling pathway. J. Plant Biol. 50, 109-116. Kim, S.Y. (2007). Recent advances in ABA signaling. J. Plant Biol. 50, 117-121 https://doi.org/10.1007/BF03030619
  14. Kim, J.H., Cheon, Y.M., Kim, B.-G., and Ahn, J.-H. (2008). Analysis of flavonoids and characterization of the OsFNS gene involved in flavone biosynthesis in rice. J. Plant Biol. 51, 97-101 https://doi.org/10.1007/BF03030717
  15. Komander, D., Clague, M.J., and Urbe, S. (2009). Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563 https://doi.org/10.1038/nrm2731
  16. Kraft, E., Stone, S.L., Ma, L., Su, N., Gao, Y., Lau, O.-S., Deng, X.-W., and Callis, J. (2005). Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol. 139, 1597-1611 https://doi.org/10.1104/pp.105.067983
  17. Lee, J.-H., Hong, J.-P., Oh, S.-K., Lee, S., Choi, D., and Kim, W.T. (2004). The ethylene-responsive factor like protein 1 (Ca ERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol. Biol. 55, 61-81 https://doi.org/10.1007/s11103-004-0417-6
  18. Lee, J.-H., Deng, X.W., and Kim, W.T. (2006). Possible role of light in the maintenance of EIN3/EIL1 stability in Arabidopsis seedlings. Biochem. Biophys. Res. Commun. 350, 484-491 https://doi.org/10.1016/j.bbrc.2006.09.074
  19. Lee, H., Oh, H.J., Ahn, H.M., Oh, C.J., Jeong, J.-H., Jeon, G.L., An, C.S., Choi, S.-B., and Kim, H.B. (2008). A sterol biosynthetic gene AtCYP51A2 promoter for constitutive and ectopic expression of a transgenic plants. J. Plant Biol. 51, 359-365 https://doi.org/10.1007/BF03036139
  20. Lee, H.K., Cho, S.K., Son, O., Xu, Z., Hwang, I., and Kim, W.T. (2009). Drought stress-induced Rma1H1, a RING membraneanchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21, 622-641 https://doi.org/10.1105/tpc.108.061994
  21. Liu, Y., Wang, F., Zhang, H., He, H., Ma, L., and Deng, X.W. (2008). Functional characterization of the Arabidopsis ubiquitin-specific protease gene family reveals specific role and redundancy of individual members in development. Plant J. 55, 844-856 https://doi.org/10.1111/j.1365-313X.2008.03557.x
  22. Love, K.R., Catic, A., Schlieker, C., and Ploegh, H.L. (2007). Mechanisms, biology and inhibitors of deubiquitinating enzymes. Nat. Chem. Biol. 3, 697-705 https://doi.org/10.1038/nchembio.2007.43
  23. Luo, M., Luo, M.-Z., Buzas, D., Finnegan, J., Helliwell, C., Dennis, E.S., Peacock, W.J., and Chaudhury, A. (2008). UBIQUITINSPECIFIC PROTEASE 26 is required for seed development and the repression of PHERES1 in Arabidopsis. Genetics 180, 229-236 https://doi.org/10.1534/genetics.108.091736
  24. Moon, J., Parry, G., and Estelle, M. (2004). The Ubiquitin-proteasome pathway and plant development. Plant Cell 16, 3181-3195 https://doi.org/10.1105/tpc.104.161220
  25. Moon, B.C., Choi, M.S., Kang, Y.H., Kim, M.C., Cheong, M.S., Park, C.Y., Yoo, J.H., Koo, S.C., Lee, S.M., Lim, C.O., et al. (2005). Arabidopsis ubiquitin-specific protease 6 (AtUBP6) interacts with calmodulin. FEBS Lett. 579, 3885-3890 https://doi.org/10.1016/j.febslet.2005.05.080
  26. Mukhopadhyay, D., and Riezman, H. (2007). Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205 https://doi.org/10.1126/science.1127085
  27. Nijman S.M.B., Luna-Vargas, M.P.A., Velds, A., Brummelkamp, T.R., Dirac, A.M.G., Sixma, T.K., and Bernards, R. (2005). A genome and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 https://doi.org/10.1016/j.cell.2005.11.007
  28. Pickart, C.M., and Eddins, M.J. (2004). Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695, 55-72 https://doi.org/10.1016/j.bbamcr.2004.09.019
  29. Rao-Naik, C., Chandler, J.S., McArdle, B., and Callis, J. (2000). Ubiquitin-specific proteases from Arabidopsis thaliana: Cloning of AtUBP5 and analysis of substrate specificity of AtUBP3, AtUBP4, and AtUBP5 using Escherichia coli in vivo and in vitro assays. Arch. Biochem. Biophys. 379, 198-208 https://doi.org/10.1006/abbi.2000.1874
  30. Seo, Y.S., Kim, E.Y., Mang, H.G., and Kim, W.T. (2008). Heterologous expression and biochemical and cellular characterization of CaPLA1 encoding a hot pepper phospholipase A1 homolog. Plant J. 53, 895-908 https://doi.org/10.1111/j.1365-313X.2007.03380.x
  31. Seo, Y.S., Kim, E.Y., Kim, J.H., and Kim, W.T. (2009). Enzymatic characterization of class I DAD1-like acylhydrolase members targeted to chloroplast in Arabidopsis. FEBS Lett. 583, 2301-2307 https://doi.org/10.1016/j.febslet.2009.06.021
  32. Schmitz, R.J., Tamada, Y., Doyle, M.R., Zhang, X., and Amasino, R.M. (2009). Histone H2B deubiquitination is required for transcriptional activation of FLOWERING LOCUS C and for proper control of flowering in Arabidopsis. Plant Physiol. 149, 1196-1204 https://doi.org/10.1104/pp.108.131508
  33. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55, 555-590 https://doi.org/10.1146/annurev.arplant.55.031903.141801
  34. Son, O., Cho, S.K., Kim, E.U., and Kim, W.T. (2009). Characterization of three Arabidopsis homologs of human RING membrane anchor E3 ubiquitin ligase. Plant Cell Rep. 28, 561-569 https://doi.org/10.1007/s00299-009-0680-8
  35. Sridhar, V.V., Kapoor, A., Zhang, K., Zhu, J., Zhou, T., Hasegawa, P.M., Bressan, R.A., and Zhu, J.-K. (2007). Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 447, 735-738 https://doi.org/10.1038/nature05864
  36. Stone, S.L., Hauksdottir, H., Troy, A., Herschleb, J., Kraft, E., and Callis, J. (2005). Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137, 13-30 https://doi.org/10.1104/pp.104.052423
  37. Vierstra, R.D. (2003). The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8, 135-142 https://doi.org/10.1016/S1360-1385(03)00014-1
  38. Vierstra, R.D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell. Biol. 10, 385-397 https://doi.org/10.1038/nrm2688
  39. Yan, N., Doelling, J.H., Falbel, T.G., Durski, A.M., and Vierstra, R.D. (2000). The ubiquitin-specific protease family from Arabidopsis. AtUPB1 and 2 are required for the resistance to the amino acid analog canavanine. Plant Physiol. 124, 1828-1843 https://doi.org/10.1104/pp.124.4.1828
  40. Yang, P., Smalle, J., Lee, S., Yan, N., Emborg, T.J., and Vierstra, R.D. (2007). Ubiquitin C-terminal hydrolases 1 and 2 affect shoot architecture in Arabidopsis. Plant J. 51, 441-457 https://doi.org/10.1111/j.1365-313X.2007.03154.x

Cited by

  1. Overexpression of OsRDCP1, a rice RING domain-containing E3 ubiquitin ligase, increased tolerance to drought stress in rice (Oryza sativa L.) vol.180, pp.6, 2011, https://doi.org/10.1016/j.plantsci.2011.02.008
  2. Population structure and association mapping of yield contributing agronomic traits in foxtail millet vol.33, pp.6, 2009, https://doi.org/10.1007/s00299-014-1564-0
  3. UBIQUITIN-SPECIFIC PROTEASES function in plant development and stress responses vol.94, pp.6, 2017, https://doi.org/10.1007/s11103-017-0633-5
  4. Construction and application of functional gene modules to regulatory pathways in rice vol.60, pp.4, 2017, https://doi.org/10.1007/s12374-017-0034-y
  5. Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Ric vol.10, pp.None, 2017, https://doi.org/10.1186/s12284-017-0170-5
  6. Plant Deubiquitinases and Their Role in the Control of Gene Expression Through Modification of Histones vol.8, pp.None, 2017, https://doi.org/10.3389/fpls.2017.02274
  7. Characterization of the Ubiquitin C-Terminal Hydrolase and Ubiquitin-Specific Protease Families in Rice ( Oryza sativa ) vol.9, pp.None, 2018, https://doi.org/10.3389/fpls.2018.01636
  8. FLA, which encodes a homolog of UBP, is required for chlorophyll accumulation and development of lemma and palea in rice vol.38, pp.3, 2009, https://doi.org/10.1007/s00299-018-2368-4
  9. Identification of QTLs Controlling Seedling Traits in Temperate Japonica Rice under Different Water Conditions vol.7, pp.2, 2009, https://doi.org/10.9787/pbb.2019.7.2.106
  10. Genome-Wide Identification and Characterization of the UBP Gene Family in Moso Bamboo (Phyllostachys edulis) vol.20, pp.17, 2019, https://doi.org/10.3390/ijms20174309
  11. Modulation of Abiotic Stress Responses in Rice by E3-Ubiquitin Ligases: A Promising Way to Develop Stress-Tolerant Crops vol.12, pp.None, 2009, https://doi.org/10.3389/fpls.2021.640193
  12. Pepper ubiquitin‐specific protease, CaUBP12, positively modulates dehydration resistance by enhancing CaSnRK2.6 stability vol.107, pp.4, 2009, https://doi.org/10.1111/tpj.15374