DOI QR코드

DOI QR Code

Flooding Stress-Induced Glycine-Rich RNA-Binding Protein from Nicotiana tabacum

  • Lee, Mi-Ok (School of Biological Sciences and Institute of Molecular Biology and Genetics, Seoul National University) ;
  • Kim, Keun Pill (School of Biological Sciences and Institute of Molecular Biology and Genetics, Seoul National University) ;
  • Kim, Byung-gee (School of Chemical and Biological Engineering, Seoul National University) ;
  • Hahn, Ji-Sook (School of Chemical and Biological Engineering, Seoul National University) ;
  • Hong, Choo Bong (School of Biological Sciences and Institute of Molecular Biology and Genetics, Seoul National University)
  • Received : 2008.07.11
  • Accepted : 2008.10.17
  • Published : 2009.01.31

Abstract

A cDNA clone for a transcript preferentially expressed during an early phase of flooding was isolated from Nicotiana tabacum. Nucleotide sequencing of the cDNA clone identified an open reading frame that has high homology to the previously reported glycine-rich RNA-binding proteins. The open reading frame consists of 157 amino acids with an N-terminal RNA-recognition motif and a C-terminal glycine-rich domain, and thus the cDNA clone was designated as Nicotiana tabaccum glycine-rich RNA-binding protein-1 (NtGRP1). Expression of NtGRP1 was upregulated under flooding stress and also increased, but at much lower levels, under conditions of cold, drought, heat, high salt content, and abscisic acid treatment. RNA homopolymer-binding assay showed that NtGRP1 binds to all the RNA homopolymers tested with a higher affinity to poly r(G) and poly r(A) than to poly r(U) and poly r(C). Nucleic acid-binding assays showed that NtGRP1 binds to ssDNA, dsDNA, and mRNA. NtGRP1 suppressed expression of the fire luciferase gene in vitro, and the suppression of luciferase gene expression could be rescued by addition of oligonucleotides. Collectively, the data suggest NtGRP1 as a negative modulator of gene expression by binding to DNA or RNA in bulk that could be advantageous for plants in a stress condition like flooding.

Keywords

Acknowledgement

Supported by : Korean Research Foundation, Ministry of Education and Human Resources Development

References

  1. Agarwal, S., and Grover, A. (2005). Isolation and transcription profiling of low-$O_{2}$stress-associated cDNA clones from the floodingstress-tolerant FR13A rice genotype. Ann. Bot. 96, 831-844 https://doi.org/10.1093/aob/mci233
  2. Alb, M.M., and Pages, M. (1998). Plant proteins containing the RNA-recognition motif. Trends Plant Sci. 3, 15-21 https://doi.org/10.1016/S1360-1385(97)01151-5
  3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 https://doi.org/10.1093/nar/25.17.3389
  4. Bae, W., Xia, B., Inouye, M., and Severinov, K. (2000). Escherichia coli CspA-family RNA chaperones are transcription antiterminators. Proc. Natl. Acad. Sci. USA 97, 7784-7789 https://doi.org/10.1073/pnas.97.14.7784
  5. Bove, J., Kim, C.Y., Gibson, C.A., and Assmann, S.M. (2008). Characterization of wound-responsive RNA-binding proteins and their splice variants in Arabidopsis. Plant Mol. Biol. 67, 71-88 https://doi.org/10.1007/s11103-008-9302-z
  6. Boyer, J. (1962). Should we regularly use city water coming from river? Rev. Prat. 12, 3559-3563
  7. Carpenter, C.D., Kreps, J.A., and Simon, A.E. (1994). Genes encoding glycine-rich Arabidopsis thaliana proteins with RNAbinding motifs are influenced by cold treatment and an endogenous circadian rhythm. Plant Physiol. 104, 1015-1025 https://doi.org/10.1104/pp.104.3.1015
  8. Cho, E.K., Lee, Y.K., and Hong, C.B. (2005). A cyclophilin from Griffithsia japonica has thermoprotective activity and is affected by CsA. Mol. Cells 20, 142-150
  9. Condit, C.M., McLean, B.G., and Meagher, R.B. (1990). Characterization of the expression of the petunia glycine-rich protein-1 gene product. Plant Physiol. 93, 596-602 https://doi.org/10.1104/pp.93.2.596
  10. Dat, J.F., Capell, N., Folzer, H., Bourgeade, P., and Badot, P.M. (2004). Sensing and signaling during plant flooding. Plant Physiol. Biochem. 42, 273-282 https://doi.org/10.1016/j.plaphy.2004.02.003
  11. Dennis, E.S., Dolferus, R., Ellis, M., Rahman, M., Wu, Y., Hoeren, F.U., Grover, A., Ismond, K.P., Good, A.G., and Peacock, W.J. (2000). Molecular strategies for improving waterlogging tolerance in plants. J. Exp. Bot. 51, 89-97 https://doi.org/10.1093/jexbot/51.342.89
  12. Drew, M.C., He, C.J., and Morgan, P.W. (2000). Programmed cell death and aerenchyma formation in roots. Trends Plant Sci. 5, 123-127 https://doi.org/10.1016/S1360-1385(00)01570-3
  13. Dunn, M.A., Brown, K., Lightowlers, R., and Hughes, M.A. (1996). A low-temperature-responsive gene from barley encodes a protein with single-stranded nucleic acid-binding activity which is phosphorylated in vitro. Plant Mol. Biol. 30, 947-959 https://doi.org/10.1007/BF00020806
  14. Fedoroff, N.V. (2002). RNA-binding proteins in plants: the tip of an iceberg? Curr. Opin. Plant Biol. 5, 452-459 https://doi.org/10.1016/S1369-5266(02)00280-7
  15. Fukami-Kobayashi, K., Tomoda, S., and Go, M. (1993). Evolutionary clustering and functional similarity of RNA-binding proteins. FEBS Lett. 335, 289-293 https://doi.org/10.1016/0014-5793(93)80749-K
  16. Fusaro, A.F., Bocca, S.N., Ramos, R.L., Barroco, R.M., Magioli, C., Jorge, V.C., Coutinho, T.C., Rangel-Lima, C.M., De Rycke, R., Inze, D., et al. (2007). AtGRP2, a cold-induced nucleocytoplasmic RNA-binding protein, has a role in flower and seed development. Planta 225, 1339-1351 https://doi.org/10.1007/s00425-006-0444-4
  17. Gendra, E., Moreno, A., Alba, M.M., and Pages, M. (2004). Interaction of the plant glycine-rich RNA-binding protein MA16 with a novel nucleolar DEAD box RNA helicase protein from Zea mays. Plant J. 38, 875-886 https://doi.org/10.1111/j.1365-313X.2004.02095.x
  18. Gomez, J., Sanchez-Martinez, D., Stiefel, V., Rigau, J., Puigdomenech, P., and Pages, M. (1988). A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334, 262-264 https://doi.org/10.1038/334262a0
  19. Hanano, S., Sugita, M., and Sugiura, M. (1996). Structure and expression of the tobacco nuclear gene encoding RNA-binding protein RZ-1: the existence of an intron in the 3'-untranslated region. DNA Res. 3, 65-71 https://doi.org/10.1093/dnares/3.2.65
  20. Higgins, C.F. (1991). Stability and degradation of mRNA. Curr. Opin. Cell Biol. 3, 1013-1018 https://doi.org/10.1016/0955-0674(91)90122-F
  21. Hirose, T., Sugita, M., and Sugiura, M. (1993). cDNA structure, expression and nucleic acid-binding properties of three RNAbinding proteins in tobacco: occurrence of tissue-specific alternative splicing. Nucleic Acids Res. 21, 3981-3987 https://doi.org/10.1093/nar/21.17.3981
  22. Horvath, D.P., and Olson, P.A. (1998). Cloning and characterization of cold-regulated glycine-rich RNA-binding protein genes from leafy spurge (Euphorbia esula L.) and comparison to heterologous genomic clones. Plant Mol. Biol. 38, 531-538 https://doi.org/10.1023/A:1006050208670
  23. Jiang, W., Hou, Y., and Inouye, M. (1997). CspA, the major coldshock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272, 196-202 https://doi.org/10.1074/jbc.272.1.196
  24. Karlson, D., Nakaminami, K., Toyomasu, T., and Imai, R. (2002). A cold-regulated nucleic acid-binding protein of winter wheat shares a domain with bacterial cold shock proteins. J. Biol. Chem. 277, 35248-35256 https://doi.org/10.1074/jbc.M205774200
  25. Kenan, D.J., Query, C.C., and Keene, J.D. (1991). RNA recognition: towards identifying determinants of specificity. Trends Biochem. Sci. 16, 214-220 https://doi.org/10.1016/0968-0004(91)90088-D
  26. Kim, Y.O., Kim, J.S., and Kang, H. (2005). Cold-inducible zinc finger- containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J. 42, 890-900 https://doi.org/10.1111/j.1365-313X.2005.02420.x
  27. Kim, Y.O., Pan, S., Jung, C.H., and Kang, H. (2007). A zinc fingercontaining glycine-rich RNA-binding protein, atRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions. Plant Cell Physiol. 48, 1170-1181 https://doi.org/10.1093/pcp/pcm087
  28. Klok, E.J., Wilson, I.W., Wilson, D., Chapman, S.C., Ewing, R.M., Somerville, S.C., Peacock, W.J., Dolferus, R., and Dennis, E.S. (2002). Expression profile analysis of the low-oxygen response in Arabidopis root cultures. Plant Cell 14, 2481-2494 https://doi.org/10.1105/tpc.004747
  29. Knight, H., and Knight, M.R. (2001). Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci. 6, 262-267 https://doi.org/10.1016/S1360-1385(01)01946-X
  30. Kwak, K.J., Kim, Y.O., and Kang, H. (2005). Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J. Exp. Bot. 56, 3007-3016 https://doi.org/10.1093/jxb/eri298
  31. Lee, M.O., Hwang, J.H., Lee, D.H., and Hong, C.B. (2007). Gene expression profile for Nicotiana tabacum in the early phase of flooding stress. J. Plant Biol. 50, 496-503 https://doi.org/10.1007/BF03030689
  32. Lee, H., Cho, K.H., Kim, I.-C., Yim, J.H., Lee, H.K., and Lee, Y.K. (2008). Expressed sequence tag analysis of antarctic hairgrass Deschampsia antarctica from King Geroge Island, Antarctica. Mol. Cells 25, 258-264
  33. Lorkovic, Z.J., and Barta, A. (2002). Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30, 623-635 https://doi.org/10.1093/nar/30.3.623
  34. Ludevid, D., Hofte, H., Himelblau, E., and Chrispeels, M.J. (1992). The expression pattern of the tonoplast intrinsic protein $\gamma$-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol. 100, 1633-1639 https://doi.org/10.1104/pp.100.4.1633
  35. Mahajan, S., and Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139-158 https://doi.org/10.1016/j.abb.2005.10.018
  36. Maris, C., Dominguez, C., and Allain, F.H. (2005). The RNA recognition motif, a plastic RNA-binding platform to regulate posttranscriptional gene expression. FEBS J. 272, 2118-2131 https://doi.org/10.1111/j.1742-4658.2005.04653.x
  37. Masaki, S., Yamada, T., Hirasawa, T., Todaka, D., and Kanekatsu, M. (2008). Proteomic analysis of RNA-binding proteins in dry seeds of rice after fractionation by ssDNA affinity column chromatography. Biotechnol. Lett. 30, 955-960 https://doi.org/10.1007/s10529-007-9619-8
  38. Moriguchi, K., Sugita, M., and Sugiura, M. (1997). Structure and subcellular localization of a small RNA-binding protein from tobacco. Plant J. 12, 215-221 https://doi.org/10.1046/j.1365-313X.1997.12010215.x
  39. Mousavi, A., and Hotta, Y. (2005). Glycine-rich proteins: a class of novel proteins. Appl. Biochem. Biotechnol. 120, 169-174 https://doi.org/10.1385/ABAB:120:3:169
  40. Nakaminami, K., Karlson, D.T., and Imai, R. (2006). Functional conservation of cold shock domains in bacteria and higher plants. Proc. Natl. Acad. Sci. USA 103, 10122-10127 https://doi.org/10.1073/pnas.0603168103
  41. Nomata, T., Kabeya, Y., and Sato, N. (2004). Cloning and characcharacterization of glycine-rich RNA-binding protein cDNAs in the moss Physcomitrella patens. Plant Cell Physiol. 45, 48-56 https://doi.org/10.1093/pcp/pch005
  42. Palusa, S.G., Ali, G.S., and Reddy, A.S. (2007). Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J. 49, 1091-1107 https://doi.org/10.1111/j.1365-313X.2006.03020.x
  43. Phadtare, S., and Inouye, M. (1999). Sequence-selective interactions with RNA by CspB, CspC and CspE, members of the CspA family of Escherichia coli. Mol. Microbiol. 33, 1004-1014 https://doi.org/10.1046/j.1365-2958.1999.01541.x
  44. Query, C.C., Bentley, R.C., and Keene, J.D. (1989). A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell 57, 89-101 https://doi.org/10.1016/0092-8674(89)90175-X
  45. Raab, S., Toth, Z., de Groot, C., Stamminger, T., and Hoth, S. (2006). ABA-responsive RNA-binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta 224, 900-914 https://doi.org/10.1007/s00425-006-0282-4
  46. Rochaix, J.D. (2001). Posttranscriptional control of chloroplast gene expression. From RNA to photosynthetic complex. Plant Physiol. 125, 142-144 https://doi.org/10.1104/pp.125.1.142
  47. Saab, I.N., and Sachs, M.M. (1996). A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiol. 112, 385-391 https://doi.org/10.1104/pp.112.1.385
  48. Sachetto-Martins, G., Franco, L.O., and de Oliveira, D.E. (2000). Plant glycine-rich proteins: a family or just proteins with a common motif? Biochim. Biophys. Acta 1492, 1-14 https://doi.org/10.1016/S0167-4781(00)00064-6
  49. Sambrook, J., Fritsch E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (New York: Cold Spring Harbor Laboratory)
  50. Shinozuka, H., Hisano, H., Yoneyama, S., Shimamoto, Y., Jones, E.S., Forster, J.W., Yamada, T., and Kanazawa, A. (2006). Gene expression and genetic mapping analyses of a perennial ryegrass glycine-rich RNA-binding protein gene suggest a role in cold adaptation. Mol. Genet. Genomics 275, 399-408 https://doi.org/10.1007/s00438-005-0095-3
  51. Simpson, G.G., and Filipowicz, W. (1996). Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery. Plant Mol. Biol. 32, 1-41 https://doi.org/10.1007/BF00039375
  52. Stephen, J.R., Dent, K.C., and Finch-Savage, W.E. (2003). A cDNA encoding a cold-induced glycine-rich RNA binding protein from Prunus avium expressed in embryonic axes. Gene 320,177-183 https://doi.org/10.1016/S0378-1119(03)00826-6
  53. Thieringer, H.A., Jones, P.G., and Inouye, M. (1998). Cold shock and adaptation. Bioessays 20, 49-57 https://doi.org/10.1002/(SICI)1521-1878(199801)20:1<49::AID-BIES8>3.0.CO;2-N
  54. van Nocker, S., and Vierstra, R.D. (1993). Two cDNAs from Arabidopsis thaliana encode putative RNA binding proteins containing glycine-rich domains. Plant Mol. Biol. 21, 695-699 https://doi.org/10.1007/BF00014552

Cited by

  1. Proteomic profiling of proteins associated with the rejuvenation of Sequoia sempervirens (D. Don) Endl vol.8, pp.None, 2009, https://doi.org/10.1186/1477-5956-8-64
  2. Transcriptome profiling of Fusarium solani f. sp. eumartii -infected potato tubers provides evidence of an inducible defense response vol.75, pp.1, 2009, https://doi.org/10.1016/j.pmpp.2010.09.002
  3. Molecular cloning and characterization of RNA binding protein genes from the wild radish vol.34, pp.6, 2009, https://doi.org/10.1007/s13258-012-0088-7
  4. Comparative proteomic analysis reveals the mechanisms governing cotton fiber differentiation and initiation vol.75, pp.3, 2012, https://doi.org/10.1016/j.jprot.2011.09.025
  5. Beyond transcription: RNA-binding proteins as emerging regulators of plant response to environmental constraints vol.182, pp.None, 2009, https://doi.org/10.1016/j.plantsci.2011.02.004
  6. A glycine-rich RNA-binding protein can mediate physiological responses in transgenic plants under salt stress vol.39, pp.2, 2009, https://doi.org/10.1007/s11033-011-0830-2
  7. EgRBP42 encoding an hnRNP-like RNA-binding protein from Elaeis guineensis Jacq. is responsive to abiotic stresses vol.31, pp.10, 2009, https://doi.org/10.1007/s00299-012-1297-x
  8. Comparisons of protein profiles of beech bark disease resistant and susceptible American beech ( Fagus grandifolia ) vol.11, pp.None, 2013, https://doi.org/10.1186/1477-5956-11-2
  9. Circadian oscillation and development-dependent expression of glycine-rich RNA binding proteins in tomato fruits vol.41, pp.4, 2009, https://doi.org/10.1071/fp13239
  10. Structural basis of nucleic acid binding by Nicotiana tabacum glycine-rich RNA-binding protein: implications for its RNA chaperone function vol.42, pp.13, 2009, https://doi.org/10.1093/nar/gku468
  11. The rice OsDG2 encoding a glycine-rich protein is involved in the regulation of chloroplast development during early seedling stage vol.33, pp.5, 2014, https://doi.org/10.1007/s00299-013-1549-4
  12. An anther-specific gene PhGRP is regulated by PhMYC2 and causes male sterility when overexpressed in petunia anthers vol.36, pp.9, 2017, https://doi.org/10.1007/s00299-017-2163-7
  13. Proteomic Analysis of Phloem Proteins Leads to the Identification of Potential Candidates for JA-Mediated RKN-Resistant Elements in Solanum lycopersicum vol.36, pp.1, 2009, https://doi.org/10.1007/s00344-016-9622-1
  14. Functional conservation of MtFPA, a nucleus-localized RNA-recognition motif-binding protein that regulates flowering time in Medicago truncatula vol.12, pp.1, 2009, https://doi.org/10.1007/s11816-018-0470-2
  15. Protective roles of plant proteins in conferring tolerance to heat stress vol.42, pp.9, 2009, https://doi.org/10.1080/01904167.2019.1589501
  16. Identification and characterisation of a glycine-rich RNA-binding protein as an endogenous suppressor of RNA silencing from Nicotiana glutinosa vol.249, pp.6, 2009, https://doi.org/10.1007/s00425-019-03122-5
  17. Molecular Characterization, Expression Pattern and Function Analysis of Glycine-Rich Protein Genes Under Stresses in Chinese Cabbage ( Brassica rapa L. ssp. pekinensis ) vol.11, pp.None, 2020, https://doi.org/10.3389/fgene.2020.00774
  18. Physiological Responses of Two Contrasting Kiwifruit (Actinidia spp.) Rootstocks against Waterlogging Stress vol.10, pp.12, 2009, https://doi.org/10.3390/plants10122586