Molecules and Cells

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

Proteomic Identification of Differentially Expressed Proteins in Arabidopsis Mutant ntm1-D with Disturbed Cell Division

  • Lee, Kyung Hyeon (Protein Chemistry & Mass Spectrometry Laboratory, Department of Chemistry, Seoul National University) ;
  • Kim, Youn-Sung (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Park, Chung-Mo (Molecular Signaling Laboratory, Department of Chemistry, Seoul National University) ;
  • Kim, Hie-Joon (Protein Chemistry & Mass Spectrometry Laboratory, Department of Chemistry, Seoul National University)
  • Received : 2007.06.13
  • Accepted : 2007.08.14
  • Published : 2008.02.29
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Abstract

Proteome analysis was performed to identify proteins differentially expressed in an Arabidopsis mutant, ntm1-D. In this mutant the NAC transcription factor NTM1 is constitutively expressed and the resultant phenotypic changes include dwarfism, serrated leaves, and altered floral structures, probably due to reduced cell division. Marked elevation of proteins mediating environmental stress responses, including annexin, vegetative storage proteins, beta-glucosidase homolog 1, and glutathione transferases was observed. Overexpression of annexin was confirmed by RT-PCR and Western blotting. These observations suggest that the reduced growth observed in the ntm1-D mutant is caused by enhancement of its stress responses, possibly resulting in a cost in fitness.

Keywords

Acknowledgement

Supported by : National Research Laboratory(NRL)

References

  1. Berger, S., Bell, E., Sadka, A., and Mullet, J.E. (1995). Arabidopsis thaliana AtVsp is homologous to soybean Vsp$\alpha$ and Vsp$\beta$, genes encoding vegetative storage protein acid-phophatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27, 933-942 https://doi.org/10.1007/BF00037021
  2. Berger, S., Mitchell-Olds, T., and Stotz, H.U. (2002). Local and differential control of vegetative storage protein expression in response to herbivore damage in Arabidopsis thaliana. Physiol. Plant 114, 85-91 https://doi.org/10.1046/j.0031-9317.2001.1140112.x
  3. Breton, G., Vazquez-Tello, A., Danyluk, J., and Sarhan, F. (2000). Two novel intrinsic annexins accumulate in wheat membranes in response to low temperature. Plant Cell Physiol. 41, 177-184 https://doi.org/10.1093/pcp/41.2.177
  4. Cantero, A., Barthakur, S., Brushart, T.J., Chou, S., Morgan, R.O., Fernandez, M.P., Clark, G.B., and Roux, S.J. (2006). Expression profiling of the Arabidopsis annexin gene family during germination, de-etiolation and abiotic stress. Plant Physiol. Biochem. 44, 13-24 https://doi.org/10.1016/j.plaphy.2006.02.002
  5. Carroll, A.D., Moyen, C., Van Kesteren, P., Tooke, F., Battey, N.H., and Brownlee, C. (1998). $Ca^{2+}$, annexins and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell 10, 1267-1276 https://doi.org/10.1105/tpc.10.8.1267
  6. Chou, I.T. and Gasser, C.S. (1997). Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins. Plant Mol. Biol. 35, 873-892 https://doi.org/10.1023/A:1005930024796
  7. Clark, G.B., Sessions, A., Eastburn, D.J., and Roux, S.J. (2001). Differential expression of members of the annexin multigene family in Arabidopsis. Plant Physiol. 126, 1072-1084 https://doi.org/10.1104/pp.126.3.1072
  8. Delmer, D.P. and Potikha, T.S. (1997). Structures and functions of annexins in plants. Cell. Mol. Life Sci. 53, 546-553 https://doi.org/10.1007/s000180050070
  9. DeRidder, B.P., Dixon, D.P., Beussman, D.J., Edwards, R., and Goldsbrough, P.B. (2002). Induction of glutathione S-transerase in Arabidopsis by herbicides safeners. Plant Physiol. 130, 1497-1505 https://doi.org/10.1104/pp.010066
  10. De Veylder, L., Joubes, J., and Inze, D. (2003). Plant cell cycle transitions. Curr. Opin. Plant Biol. 6, 536-543 https://doi.org/10.1016/j.pbi.2003.09.001
  11. Dewitte, W. and Murray, J.A.H. (2003). The plant cell cycle. Annu. Rev. Plant Biol. 54, 235-264 https://doi.org/10.1146/annurev.arplant.54.031902.134836
  12. Dietz, K.J., Tavakoli, N., Kluge, C., Mimura, T., Sharma, S.S., Harris, G.C., Chardonnens, A.N., and Dack, D. (2001). Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J. Exp. Bot. 52, 1969-1980 https://doi.org/10.1093/jexbot/52.363.1969
  13. Dixon, D.P., Lapthorn, A., and Edwards, R. (2002). Plant glutathione transferases. Genome Biol. 3, REVIEWS 3004
  14. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., Tran, L.S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2004). A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stresssignaling pathway. Plant J. 39, 863-873 https://doi.org/10.1111/j.1365-313X.2004.02171.x
  15. Gerke, V. and Moss, S.E. (2002). Annexins: from structure to function. Physiol. Rev. 82, 331-371
  16. Gidrol, X., Sabelli, P.A., Fern, Y.S., and Kush, A.K. (1996). Annexin-like protein from Arabidopsis thaliana rescues oxyR mutant of Escherichia coli from $H_{2}O_{2}$ stress. Proc. Natl. Acad. Sci. USA 93, 11268-11273
  17. Gorecka, K.M., Postupolska, D.K., Henning, J., Buchet, R., and Pikula, S. (2005). Peroxidase activity of annexin 1 from Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 336, 868-875 https://doi.org/10.1016/j.bbrc.2005.08.181
  18. Gorg, A., Obermaier, C., Boguth, G., Harder, A., Scheibe, B., Wildgruber, R., and Weiss, W. (2000). The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21, 1037-1053 https://doi.org/10.1002/(SICI)1522-2683(20000401)21:6<1037::AID-ELPS1037>3.0.CO;2-V
  19. Görg, A., Weiss, W., and Dunn, M.J. (2004). Current twodimensional electrophoresis technology for proteomics. Proteomics 4, 3665-3685 https://doi.org/10.1002/pmic.200401031
  20. Hoppe, T., Matuschewski, K., Rape, M., Schlenker, S., Ulrich, H.D., and Jentsch, S. (2000). Activation of a membranebound transcription factor by regulated ubiquitin/proteasome- dependent processing. Cell 102, 577-586 https://doi.org/10.1016/S0092-8674(00)00080-5
  21. Hoppe, T., Rape, M., and Jentsch, S. (2001). Membrane-bound transcription factors: regulated release by RIP or RUP. Curr. Opin. Cell Biol. 12, 344-348
  22. Hosel, W. and Todenhagen, R. (1980). Characterization of a $\beta$- glucosidase from Glycine max which hydrolyses coniferin and syringin. Phytochemistry 19, 1349-1535
  23. Jaffe, H., Veeranna, and Pant, H.C. (1998). Characterization of serine and threonine phosphorylation sites in beta-elimination/ethanethiol addition-modified proteins by electrospray tandem mass spectrometry and database searching. Biochemistry 37, 16211-16224 https://doi.org/10.1021/bi981264p
  24. Kim, Y.S., Kim, S.G., Park, J.E., Park, H.Y., Lim, M.H., Chua, N.H., and Park, C.-M. (2006). A membrane-bound NAC transcription factor, NTM1 regulates cell division in Arabidopsis. Plant Cell 18, 3132-3144 https://doi.org/10.1105/tpc.106.043018
  25. Kim, S.G., Kim, S.Y., and Park, C.-M. (2007). membraneassociated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226, 647-654 https://doi.org/10.1007/s00425-007-0513-3
  26. Kiyosue, T., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1993). Characterization of two cDNAs (ERD11 and ERD13) for dehydration- inducible genes that encode putative glutathione Stransferases in Arabidopsis thaliana L. FEBS Lett. 335, 189-192 https://doi.org/10.1016/0014-5793(93)80727-C
  27. Knight, H., Trewavas, A.J., and Knight, M.R. (1996). Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8, 489-503 https://doi.org/10.1105/tpc.8.3.489
  28. Kopka, J., Pical, C., Hetherington, A.M., and Muller-Rober, B. (1998). $Ca^{2+}$/phospholipid-binding (C2) domain in multiple plant proteins: novel components of the calcium-sensing apparatus. Plant Mol. Biol. 36, 627-637 https://doi.org/10.1023/A:1005915020760
  29. Kovacs, I, Ayaydin, F., Oberschall, A., Ipacs, I., Bottka, S., Pongor, S., Dudits, D., and Tóth, E.C. (1998). Immunolocalization of a novel annexin like protein encoded by a stress and abscisic acid responsive gene in alfalfa. Plant J. 15, 185-197 https://doi.org/10.1046/j.1365-313X.1998.00194.x
  30. Krishna, R.G. and Wold, F. (1993). Post-translational modification of proteins. Adv. Enzymol. Relat. Areas Mol. Biol. 67, 3256-3298
  31. Kusano, H., Asano, T., Shimada, H., and Kadowaki, K. (2005). Molecular characterization of ONAC300, a novel NAC gene specifically expressed at early stages in various developing tissues of rice. Mol. Gen. Genomics 272, 616-626 https://doi.org/10.1007/s00438-004-1097-2
  32. Lee, K., Bae, D., and Lim, D. (2002). Evaluation of parameters in peptide mass fingerprinting for protein identification by MALDI-TOF mass spectrometry. Mol. Cells 13, 175-184
  33. Lee, S.M., Lee, E.J., Yang, E.J., Lee, J.E., Park, A.R., Song, W.H., and Park, O.K. (2004). Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. Plant Cell 16, 1378-1391 https://doi.org/10.1105/tpc.021683
  34. Marrs, K.A. (1996). The functions and regulation of glutathione S-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 127-158 https://doi.org/10.1146/annurev.arplant.47.1.127
  35. Matsushima, R., Fukao, Y., Nishimura, M., and Hara-Nishimura, I. (2004). NAI1 gene encodes a basic-helix-loop-helix-type putative transcription factor that regulates the formation of an endoplasmic reticulum-derived structure, the ER body. Plant Cell 16, 1536-1549 https://doi.org/10.1105/tpc.021154
  36. Mattiacci, L., Dicke, M., and Posthumus, M.A. (1995). beta- Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc. Natl. Acad. Sci. USA 92, 2036-2040
  37. Meijer, M. and Murray, J.A. (2001). Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4, 44-49 https://doi.org/10.1016/S1369-5266(00)00134-5
  38. Mignery, G.A., Pikaard, C.S., and Park, W.D. (1988). Molecular characterization of the patatin multigene family of potato. Gene 62, 27-44 https://doi.org/10.1016/0378-1119(88)90577-X
  39. Miller, C.O., Skoog, F., von Saltza, M.H., and Strong, M. (1955). Kinetin, a cell division factor from deoxyribonucleic acid. J. Am. Chem. Soc. 77, 1392-1392 https://doi.org/10.1021/ja01610a105
  40. 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
  41. Morgan, R.O. and Fernandez, M.P. (1997). Distinct annexin subfamilies in plants and protists diverged prior to animal annexins and from a common ancestor. J. Mol. Evol. 44, 178-188 https://doi.org/10.1007/PL00006134
  42. Moss, S.E. and Morgan, R.O. (2004). The annexins. Genome Biol. 5, 219-227 https://doi.org/10.1186/gb-2004-5-4-219
  43. Nicholas, K.U., Forney, C.F., and Paulson, A.T. (2002). A rapid capillary gel electrophoresis method for the quantitative determination of RuBisCo in spinach. Phytochem. Anal. 13, 39-44 https://doi.org/10.1002/pca.613
  44. Nutricati, E., Miceli, A., Blando, F., and De Bellis, L. (2006). Characterization of two Arabidopsis thaliana glutathione S-transferases. Plant Cell Rep. 25, 997-1005 https://doi.org/10.1007/s00299-006-0146-1
  45. Patarca, R. (1996). Protein phosphorylation and dephosphorylation in physiologic and oncologic processes. Crit. Rev. Oncol. 7, 343-434 https://doi.org/10.1615/CritRevOncog.v7.i5-6.20
  46. Park, J.E., Park, J.Y., Kim, Y.S., Staswick, P.E., Jeon, J., Yun, J., Kim, S.Y., Kim, J., Lee, Y.H., and Park, C.M. (2007). GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282, 10036-10046 https://doi.org/10.1074/jbc.M610524200
  47. Posewitz, M.C. and Tempst, P. (1999). Immobilized gallium (III) affinity chromatography of phosphopeptides. Anal. Chem. 71, 2883-2892 https://doi.org/10.1021/ac981409y
  48. Reymond, P., Bodenhausen, N., Van Poecke, R.M.P., Krishnamurthy, V., Dicke, M., and Farmer, E.E. (2004). A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132-3147 https://doi.org/10.1105/tpc.104.026120
  49. Riou-Khamlichi, C., Huntleq, R., Jacqmard, A., and Murray, J.A. (1999). Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283, 1541-1544 https://doi.org/10.1126/science.283.5407.1541
  50. Shih, M.C., Heinrich, P., and Goodman, H.M. (1991). Cloning and chromosomal mapping of nuclear genes encoding chloroplast and cytosolic glyceraldehyde-3-phosphate-dehydrogenase from Arabidopsis thaliana. Gene 104, 133-138 https://doi.org/10.1016/0378-1119(91)90242-4
  51. Stotz, H.U., Pittendrigh, B.R., Kroymann, J., Weniger, K., Fritsche, J., Bauke, A., and Mitchell-Olds, T. (2000). Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against cotton worm but not diamondback moth. Plant Physiol. 124, 1007-1017 https://doi.org/10.1104/pp.124.3.1007
  52. Utsugi, S., Sakamoto, W., Murata, M., and Motoyoshi, F. (1998). Arabidopsis thaliana vegetative storage protein (VSP) genes: gene organization and tissue-specific expression. Plant Mol. Biol. 38, 565-576 https://doi.org/10.1023/A:1006072014605
  53. Veylder, L. D., Joubes, J., and Inze, D. (2003). Plant cell cycle transitions. Curr. Opin. Plant Biol. 6, 536-643 https://doi.org/10.1016/j.pbi.2003.09.001
  54. Vik, A. and Rine, J. (2000). Membrane biology: membrane-regulated transcription. Curr. Biol. 10, R869-R871 https://doi.org/10.1016/S0960-9822(00)00822-8
  55. Wagner, U., Edwards, R., Dixon, D.P., and Mauch, F. (2002). Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515-532 https://doi.org/10.1023/A:1015557300450
  56. Wang, P., Duan, W., Takabayashi, A., Endo, T., Shikanai, T., Ye, J.Y., and Mi, H. (2006). Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol. 141, 465-474 https://doi.org/10.1104/pp.105.070490
  57. White, P.J., Bowen, H.C., Demidchik, V., Nichols, C., and Davies, J.M. (2002). Genes for calcium-permeable channels in the plasma membrane of plant root cells Signal transduction mechanisms in plants: an overview. Biochem. Biophys. Acta 1564, 299-309 https://doi.org/10.1016/S0005-2736(02)00509-6
  58. Wittenbach, V.A. (1983). Purification and characterization of a soybean leaf storage glycoprotein. Plant Physiol. 73, 125-129 https://doi.org/10.1104/pp.73.1.125
  59. Xie, D.X., Feys, B.F., James, S., Nieto-Rostro, M., and Turner, J.G. (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091-1094 https://doi.org/10.1126/science.280.5366.1091
  60. Xu, Z., Treviño, L.E., Zeng, L., Lalgondar, L., Bevan, D., Winkel, B., Mohamed, A., Cheng, C.L., Shih, M.C., Poulton, J., et al. (2004). Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol. Biol. 55, 343-367 https://doi.org/10.1007/s11103-004-0790-1
  61. Yoshida, S., Tamaoki, M., Shikano, T., Nakajima, N., Ogawa, D., Ioki, M., Aono, M., Kubo, A., Kamada, H., Inoue, Y., et al. (2006). Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol. 47, 304-308 https://doi.org/10.1093/pcp/pci246