DOI QR코드

DOI QR Code

Members of the ran family of stress-inducible small GTP-binding proteins are differentially regulated in sweetpotato plants

  • Received : 2013.03.25
  • Accepted : 2013.03.27
  • Published : 2013.03.31

Abstract

Ran is a small GTP-binding protein that binds and subsequently hydrolyzes GTP. The functions of Ran in nuclear transport and mitotic progression are well conserved in plants and animals. In animal cells, stress treatments cause Ran relocalization and slowing of nuclear transport, but the role of Ran proteins in plant cells exposed to stress is still unclear. We have therefore compared Ran genes from three EST libraries construed from different cell types of sweetpotato and the distribution pattern of Ran ESTs differed according to cell type. We further characterized two IbRan genes. IbRan1 is a specific EST to the suspension cells and leaf libraries, and IbRan2 is specific EST to the root library. IbRan1 showed 94.6 % identity with IbRan2 at the amino acid level, but the C-terminal region of IbRan1 differed from that of IbRan2. These two genes showed tissue-specific differential regulation in wounded tissues. Chilling stress induced a similar expression pattern in both IbRan genes in the leaves and petioles, but they were differently regulated in the roots. Hydrogen peroxide treatment highly stimulated IbRan2 mRNA expression in the leaves and petioles, but had no significant effect on IbRan1 gene expression. These results showed that the transcription of these two IbRan genes responds differentially to abiotic stresses and that they are subjected to tissue-specific regulation. Plant Ran-type small G-proteins are a multigenic family, and the characterization of each Ran genes under various environmental stresses will contribute toward our understanding of the distinctive function of each plant Ran isoform.

Keywords

EST analysis;Tissue-specific expression;Wounding;Chilling;Hydrogen peroxide

References

  1. Schwoebel ED, Ho TH, Moore MS (2002) The mechanism of inhibition of Ran-dependent nuclear transport by cellular ATP depletion. J Cellular Biology 157:963-974 https://doi.org/10.1083/jcb.200111077
  2. Stochaj U, Rassadi R, Chiu J (2000) Stress mediated inhibition of the classical nuclear protein import pathway and nuclear accumulation of the small GTPase Gsp1p. FASEB J 14: 2130-2132 https://doi.org/10.1096/fj.99-0751fje
  3. Tameling WI, Baulcombe DC (2007) Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19:1682-1694 https://doi.org/10.1105/tpc.107.050880
  4. Vernoud V, Horton AC, Yang Z, Nielsen E (2003) Analysis of the small GTPase gene superfamily of Arabidopsis. Plant Physiology. 131:1191-1208 https://doi.org/10.1104/pp.013052
  5. Wang X, Xu Y, Han Y, Bao S, Jizhou D, Yuan M, Zhihong X, Chong K (2006) Overexpression of RAN1 in Rice and Arabisopsis Alters Primordial Meristem, Mitotic Progress, and Sensitivity to Auxin. Plant Phyiology 140:91-101
  6. Xu XM, Meier I (2007) The nuclear pore comes to the fore. Trends in Plant Science 13:20-27
  7. Yano A, Kodama Y, Koike A, Shinya T, Kim HJ, Matsumoto M, Ogita S, Wada Y, Ohad N, Sano H (2006) Interaction between methyl CpG-binding protein and Ran GTPase during cell division in tobacco cultured cells. Annual Botany 98:1179-1187 https://doi.org/10.1093/aob/mcl211
  8. You MK, Hur CG, Ahn YS, Suh MC, Jeong BC, Shin JS, Bae JM (2003) Identification of genes possibly related to storage root induction in sweet potato. FEBS Letter 536:101-105 https://doi.org/10.1016/S0014-5793(03)00035-8
  9. Zang A, Xu X, Neill SN, Cai W (2010) Overexpression of OsRAN1 in rice and Arabidopsis renders transgenic plants hypersensitive to salinity and osmotic stress. J Experimental Botany 61:777-789 https://doi.org/10.1093/jxb/erp341
  10. Zhao J, Zhang W, Zhao Y, Gong X, Glu L, Zhu G, Wang X, Gong Z, Schumaker KS, Guo Y (2007) SAD2, an importin-like protein, is required for UV-B response in Arabidopsis by mediating MYB4 nuclear trafficking. Plant Cell 19:3805-3818 https://doi.org/10.1105/tpc.106.048900
  11. Zhao J, Wang J, Zhang X (2011) Feedback regulation of Ran gene expression by Ran protein. Gene 485:85-90 https://doi.org/10.1016/j.gene.2011.06.008
  12. Kim S-H, Arnold D, Lioyd A, Roux S (2001) Antisense expression of an Arabidopsis Ran binding protein renders transgenic roots hypersensitive to auxin and alters auxin-induced root growth and development by arresting mitotic progress. Plant Cell 13:2619-2630 https://doi.org/10.1105/tpc.13.12.2619
  13. Kim YH, Hur CC, Shin YH, Bae JM, Song YS, Huh GH (2006) Identification and characterization of highly expressed genes in suspension-cultured cells of sweet potato. J Plant Biology 49:364-370 https://doi.org/10.1007/BF03178813
  14. Kodiha M, Chu A, Matusiewicz N, Stochaj U (2004) Multiple mechanisms promote the inhibition of classical nuclear import upon to severe oxidative stress. Cell Death and Differentiation 11:862-874 https://doi.org/10.1038/sj.cdd.4401432
  15. Lee Y, Kim MH, Kim SK, Kim SH (2008) Phytochrome-mediated differential gene expression of plant Ran/TC4 small Gproteins. Plant 228:215-224 https://doi.org/10.1007/s00425-008-0745-x
  16. Liu WF, Han F, Zang XB (2009) Ran GTPase regulates hemocytic phagocytosis of shrimp by interaction with myosin. J Proteome Research 8:1198-1206 https://doi.org/10.1021/pr800840x
  17. Ma L, Hong ZL, Zhang ZM (2007) Perinuclear and nuclear envelope localization of Arabidopsis Ran proteins. Plant Cell Reports 26:1373-1382 https://doi.org/10.1007/s00299-007-0367-y
  18. Mahajan R, Delphin C, Guan T, Gerace L, Melchior F (1997) A small ubiquitin-related polypeptide involved in targeting RanGAP to nuclear pore complex protein RanBP2. Cell 88:97-107 https://doi.org/10.1016/S0092-8674(00)81862-0
  19. Meier I (2007) Composition of the plant nuclear envelop: theme and variations. J Experimental Botany 58:27-34
  20. Merkle T, Haizel T, Matsamuto T, Hatter K, Dallmann G, Nagy F (994) Phenotype of the fission yeast cell cycle regulatory mutant piml-46 is suppressed by a tobacco cDNA encoding a small, Ran-like GTP-binding protein. Plant Jl 6:555-565 https://doi.org/10.1046/j.1365-313X.1994.6040555.x
  21. Miyamoto Y, Saiwaki T, Yaamshita J, Yasuda Y, Kotera I, Shibata S, Shigeta M, Hiraoka Y, Haraguchi T, Yoneda Y (2004) Cellular stresses induces the nuclear accumulation of importin alpha and cause a conventional nuclear mport block. J Cellular Biology 165:617-623 https://doi.org/10.1083/jcb.200312008
  22. Nanduri J, Tartakoff AM (2001) Perturbation of the nucleus: a novel Hog1p-independent, Pkc1p-dependent consequence of hyperosmotic shock in yeast. Molecular Biology of the Cell 12:1835-1841 https://doi.org/10.1091/mbc.12.6.1835
  23. Pay A, Resch K, Frohnmeyer H, Fejes E, Nagy F, Nick P (2002) Plant Ran GAPs are localized at the nuclear envelope in interphase and associated with microtubules in mitotic cells. Plant J 30:699-709 https://doi.org/10.1046/j.1365-313X.2002.01324.x
  24. Ren M, Villamarin A, Shin A (1995) Separate domains of the Ran GTPase interact with different factors to regulate nuclear protein import and RNA processing. Moleluar and Cellular Biology 15:2117-21124 https://doi.org/10.1128/MCB.15.4.2117
  25. Richards SA, Lounsbury KM, Macara IG (1995) The C-terminus of the nuclear RAN/TC4 GTPase atabilizes the GDP-bound state and mediates interactions with RCC1, RAN-GAP, and HTF9A/RANBP1. J Biological Chemistry 270:14405-14411 https://doi.org/10.1074/jbc.270.24.14405
  26. Sasaki K, Hiraga S, Ito H, Seo S, Matsui H, Ohashi Y (2002) A wound-inducible tobacco peroxidase gene expression preferentially in the vascular system. Plant Cell Physiology 43:108-117 https://doi.org/10.1093/pcp/pcf013
  27. Ach RA, Gruissem W (1994) A small nuclear GTP-binding protein from tomato suppresses a Schizosaccharomyces pombe cell-type cycle mutant. Proceeding of the National Academy of Science 91:5863-5867 https://doi.org/10.1073/pnas.91.13.5863
  28. Cho H-K, Park J-A, Pai H-S (2008) Physiological function of NbRanBP1 in Nicotiana benthamiana. Mol Cells 26:270-277
  29. Ciciarello M., Mangiacasale R., and Lavia P. (2007) Spatial control of mitosis by the GTPase Ran. Cellular and Molecular Life Science 64:1892-1914
  30. Clarke PR, Zhang C (2001) Ran GTPase: a master regulator of nuclear structure and function during the eukaryotic cell division cycle? Trends in Cell Biology 11:366-371 https://doi.org/10.1016/S0962-8924(01)02071-2
  31. Gorlich D, Kutay U (1999) Transport between the cell nucleus and the cytoplasm. Annual Review of Cell and Development Biology 15:607-660 https://doi.org/10.1146/annurev.cellbio.15.1.607
  32. Haizel T, Merkle T, Pay A, Fejes E, Nagy F (1997) Characterization of proteins that interact with the GTP-binding form of the regulatory GTPase in Arabidopsis. Plant J 11:93-103 https://doi.org/10.1046/j.1365-313X.1997.11010093.x
  33. Han F, Zang XB (2007) Characterization of a Ras-related nuclear protein (Ran protein) up-regulated in shrimp antiviral immunity. Fish Scellfish immunology 23:937-944 https://doi.org/10.1016/j.fsi.2007.01.022
  34. Hetzer M, Gruss OJ, Mattai IW (2002) The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nature Cellular Biology 4:E177-E184 https://doi.org/10.1038/ncb0702-e177
  35. Jeong SY, Rose A, Joseph J, Dasso M, Meier I (2005) Plantspecific mitotic targeting of RanGAP requires a functional WPP domain. Plant J 42: 270-282 https://doi.org/10.1111/j.1365-313X.2005.02368.x
  36. Kelly JB, Paschal BM (2007) Hyperosmotic stress signaling to the nucleus disrupts the Ran gradient and the production of RanGTP. Molecular Biology of the Cell 18:4365-4376 https://doi.org/10.1091/mbc.E07-01-0089

Cited by

  1. The Small G Protein AtRAN1 Regulates Vegetative Growth and Stress Tolerance in Arabidopsis thaliana vol.11, pp.6, 2016, https://doi.org/10.1371/journal.pone.0154787

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)