DOI QR코드

DOI QR Code

Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice

  • Chang-Qing, Zhang (College of Agronomy and Biotechnology, China Agricultural University) ;
  • Shunsaku, Nishiuchi (Asian Natural Environmental Science Center (ANESC), the University of Tokyo) ;
  • Shenkui, Liu (Alkali Soil Natural Environmental Science Center, Northeast Forestry University) ;
  • Tetsuo, Takano (Asian Natural Environmental Science Center (ANESC), the University of Tokyo)
  • 투고 : 2007.10.11
  • 심사 : 2008.03.17
  • 발행 : 2008.06.30

초록

Two full-length cDNAs, PutPMP3-1 and PutPMP3-2, encoding PMP3 family proteins were isolated from Puccinellia tenuiflora, a monocotyledonous halophyte. Expression of both genes was induced by low temperature, salt stress, dehydration, ABA, and $NaHCO_3$. Transcripts of PutPMP3-2 were more strongly induced by these stresses relative to those of PutPMP3-1, particularly under low temperature and dehydration conditions. Expression of PutPMP3-1 and PutPMP3-2 in yeast mutants lacking the PMP3 gene can functionally complement the membrane hyper-polarization and salt sensitivity phenotypes resulting from PMP3 deletion. To compare the functions of PutPMP3-1 and PutPMP3-2, the orthologous genes in rice (OsLti6a and OsLti6b) were isolated. Both OsLti6a and OsLti6b could functionally complement the loss of PMP3 in yeast. PutPMP3-2 and OsLti6a were more effective in reversing membrane hyperpolarization than PutPMP3-1 and OsLti6b. However, the four yeast transformants each showed similar levels of salt tolerance. These results imply that these PMP3 family members don't function identically under different stress tolerance conditions.

키워드

참고문헌

  1. Bray, E., Bailey-Serresand, J. and Weretilnyk, E. (2000) Responses to abiotic stresses. In Biochemistry and Molecular Biology of Plants, B. Buchanan, W. Gruissem, and J.R. Rockville, eds (Rockville, MD: American Society of Plant Biologists), pp. 1158-1203.
  2. Wang, W., Vinocur, B. and Altman, A. (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 218, 1-14. https://doi.org/10.1007/s00425-003-1105-5
  3. Shinozaki, K., Yamaguchi-Shinozaki, K. and Seki, M. (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6, 410-417. https://doi.org/10.1016/S1369-5266(03)00092-X
  4. Arce, D. P., Tonón, C., Zanetti, M. E., Godoy, A. V., Hirose, S. and Casalongué, C. A. (2006) The potato transcriptional co-activator StMBF1 is up-regulated in response to oxidative stress and interacts with the TATA-box binding protein. J. Biochem. Mol. Biol. 39, 355-360. https://doi.org/10.5483/BMBRep.2006.39.4.355
  5. Uemura, M., Joseph, R. A. and Steponkus, P. L. (1995) Cold acclimation of Arabidopsis thaliana: Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol. 109, 15-30. https://doi.org/10.1104/pp.109.1.15
  6. Koike, M., Takezawa, D., Arakawa, K. and Yoshida, S. (1997) Accumulation of 19-kDa plasma membrane polypeptide during induction of freezing tolerance in wheat suspension- cultured cells by abscisic acid. Plant Cell Physiol. 38, 707-716. https://doi.org/10.1093/oxfordjournals.pcp.a029224
  7. Kawamura, Y. and Uemura, M. (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 36, 141-154. https://doi.org/10.1046/j.1365-313X.2003.01864.x
  8. Koike, M., Sutoh, K., Kawakami, A., Torada, A., Oono, K. and Imai, R. (2005) Molecular characterization of a coldinduced plasma membrane protein gene from wheat. Mol. Gen. Genomics. 274, 445-453. https://doi.org/10.1007/s00438-005-0050-3
  9. Chen, F., Yuan, Y., Li, Q. and He, Z. (2007) Proteomic analysis of rice plasma membrane reveals proteins involved in early defense response to bacterial blight. Proteomics 7, 1529-1539. https://doi.org/10.1002/pmic.200500765
  10. Nohzadeh Malakshah, S., Habibi Rezaei, M., Heidari, M. and Hosseini Salekdeh, G. (2007) Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci. Biotechnol. Biochem. 71, 2144-2154 https://doi.org/10.1271/bbb.70027
  11. Goddard, N. J., Dunn, M. A., Zhang, L., White, A. J., Jack, P. L. and Hughes, M. A. (1993) Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, blt101. Plant Mol. Biol. 23, 871-879. https://doi.org/10.1007/BF00021541
  12. Gulick, P. J., Shen, W. and An, H. (1994) ESI3, a stress-induced gene from Lophopyrum elongatum. Plant Physiol. 104, 799-800. https://doi.org/10.1104/pp.104.2.799
  13. Morsy, M. R., Almutairi, A. M., Gibbons, J., Yun, S. J. and de Los Reyes, B. G. (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene. 344, 171-180 https://doi.org/10.1016/j.gene.2004.09.033
  14. Inada, M., Ueda, A., Shi, W. and Takabe, T. (2005) A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na+ and K+ accumulation under salt stress. Planta. 220, 395-402. https://doi.org/10.1007/s00425-004-1358-7
  15. Navarre, C. and Goffeau, A. (2000) Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO. J. 19, 2515-2524. https://doi.org/10.1093/emboj/19.11.2515
  16. Nylander, M., Heino, P., Helenius, E., Palva, T., Ronne, H. and Welin, B. V. (2001) The low-temperature- and salt-induced RCI2A gene of Arabidopsis complements the sodium sensitivity caused by a deletion of the homologous yeast gene SNA1. Plant Mol. Biol. 45, 341-352. https://doi.org/10.1023/A:1006451914231
  17. Mitsuya, S., Taniguchi, M., Miyake, H. and Takabe, T. (2005) Disruption of RCI2A leads to over-accumulation of Na+ and increased salt sensitivity in Arabidopsis thaliana plants. Planta. 222, 1001-1009. https://doi.org/10.1007/s00425-005-0043-9
  18. Medina, J., Rodríguez-Franco, M., Peñalosa, A., Carrascosa, M. J., Neuhaus, G. and Salinas, J. (2005) Arabidopsis mutants deregulated in RCI2A expression reveal new signaling pathways in abiotic stress responses. Plant J. 42, 586-597. https://doi.org/10.1111/j.1365-313X.2005.02400.x
  19. Peng, Y. H., Zhu, Y. F., Mao, Y. Q., Wang, S. M., Su, W. A. and Tang, Z. C. (2004) Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+. J. Exp. Bot. 55, 939-949. https://doi.org/10.1093/jxb/erh071
  20. Wang, Y. C., Chu, Y. G., Liu, G. F., Wang, M. H., Jiang, J., Hou, Y. J., Qu, G. Z. and Yang, C. P. (2007) Identification of expressed sequence tags in an alkali grass (Puccinellia tenuiflora) cDNA library. J. Plant Physiol. 164, 78-89. https://doi.org/10.1016/j.jplph.2005.12.006
  21. Wang, Y. C., Yang, C. P., Liu, G. F. and Jiang, J. (2007) Development of a cDNA microarray to identify gene expression of Puccinellia tenuiflora under saline-alkali stress. Plant Physiol. Biochem. 45, 567-576. https://doi.org/10.1016/j.plaphy.2007.05.006
  22. Capel, J., Jarillo, J. A., Salinas, J. and Martinez-Zapater, J. M. (1997) Two homologous low-temperature- inducible genes from Arabidopsis encode highly hydrophobic proteins. Plant Physiol. 115, 569-576. https://doi.org/10.1104/pp.115.2.569
  23. Krogh, A., Larsson, B., Heijne, von G. and Sonnhammer, E. L. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305, 567-580. https://doi.org/10.1006/jmbi.2000.4315
  24. Lauchli, A. and Schubert, S. (1989) The role of calcium in the regulation of membrane and cellular growth processes under salt stress. In J.H. Cherry(ed.), Environmental Stress in Plants. NATO ASI Series, Vol. G19. Springer-Verlag, Berlin, pp. 131-138.
  25. Vitart V., Baxter I., Doerner P., Harper J. F. (2001) Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis. Plant J. 27, 191-201. https://doi.org/10.1046/j.1365-313x.2001.01081.x

피인용 문헌

  1. Arabidopsis heterotrimeric G protein β subunit, AGB1, regulates brassinosteroid signalling independently of BZR1 vol.64, pp.11, 2013, https://doi.org/10.1093/jxb/ert159
  2. Fine mapping of the qLOP2 and qPSR2-1 loci associated with chilling stress tolerance of wild rice seedlings vol.128, pp.1, 2015, https://doi.org/10.1007/s00122-014-2420-x
  3. Characterization of a chloroplast localized wheat membrane protein (TaRCI) and its role in heat, drought and salinity stress tolerance in Arabidopsis thaliana. vol.4, 2015, https://doi.org/10.1016/j.plgene.2015.09.005
  4. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture vol.92, 2013, https://doi.org/10.1016/j.envexpbot.2012.08.004
  5. Molecular cloning and expression of two plasma membrane protein 3 (SmPMP3) genes from Salvia miltiorrhiza vol.60, pp.1, 2013, https://doi.org/10.1134/S1021443712060179
  6. Smart Engineering of Genetic Resources for Enhanced Salinity Tolerance in Crop Plants vol.35, pp.3, 2016, https://doi.org/10.1080/07352689.2016.1245056
  7. A putative myristoylated 2C-type protein phosphatase, PP2C74, interacts with SnRK1 in Arabidopsis vol.586, pp.6, 2012, https://doi.org/10.1016/j.febslet.2012.02.019
  8. Metal-Binding Ability of VIP1: A bZIP Protein in Arabidopsis thaliana vol.32, pp.7, 2013, https://doi.org/10.1007/s10930-013-9512-3
  9. A bZIP protein, VIP1, interacts with Arabidopsis heterotrimeric G protein β subunit, AGB1 vol.71, 2013, https://doi.org/10.1016/j.plaphy.2013.07.024
  10. Analysis of Functions of VIP1 and Its Close Homologs in Osmosensory Responses of Arabidopsis thaliana vol.9, pp.8, 2014, https://doi.org/10.1371/journal.pone.0103930
  11. Expression levels and promoter activities of candidate salt tolerance genes in halophytic and glycophytic Brassicaceae vol.99, 2014, https://doi.org/10.1016/j.envexpbot.2013.10.006
  12. A U-Box E3 Ubiquitin Ligase, PUB20, Interacts with the Arabidopsis G-Protein β Subunit, AGB1 vol.7, pp.11, 2012, https://doi.org/10.1371/journal.pone.0049207
  13. Physiological and molecular mechanisms of plant salt tolerance vol.115, pp.1, 2013, https://doi.org/10.1007/s11120-013-9813-6
  14. Transcriptional Responses of a Bicarbonate-Tolerant Monocot, Puccinellia tenuiflora, and a Related Bicarbonate-Sensitive Species, Poa annua, to NaHCO3 Stress vol.16, pp.1, 2014, https://doi.org/10.3390/ijms16010496
  15. Na2CO3 -responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses vol.6, pp.1, 2016, https://doi.org/10.1038/srep32717
  16. Cloning of a high-affinity K+ transporter gene PutHKT2;1 from Puccinellia tenuiflora and its functional comparison with OsHKT2;1 from rice in yeast and Arabidopsis vol.60, pp.12, 2009, https://doi.org/10.1093/jxb/erp184
  17. Isolation and Characterization of Maize PMP3 Genes Involved in Salt Stress Tolerance vol.7, pp.2, 2012, https://doi.org/10.1371/journal.pone.0031101
  18. Physiological and Molecular Features ofPuccinellia tenuifloraTolerating Salt and Alkaline-Salt Stress vol.55, pp.3, 2013, https://doi.org/10.1111/jipb.12013
  19. Arabidopsis G-protein β subunit AGB1 interacts with NPH3 and is involved in phototropism vol.445, pp.1, 2014, https://doi.org/10.1016/j.bbrc.2014.01.106
  20. Role of the Plasma Membrane in Saline Conditions: Lipids and Proteins vol.81, pp.4, 2015, https://doi.org/10.1007/s12229-015-9156-4
  21. CsRCI2A and CsRCI2E genes show opposite salt sensitivity reaction due to membrane potential control vol.38, pp.2, 2016, https://doi.org/10.1007/s11738-016-2072-3
  22. Comparative Proteomic Analysis of Puccinellia tenuiflora Leaves under Na2CO3 Stress vol.14, pp.1, 2013, https://doi.org/10.3390/ijms14011740
  23. Molecular characterization and expression analysis of pearl millet plasma membrane proteolipid 3 ( Pmp3 ) genes in response to abiotic stress conditions vol.10, 2017, https://doi.org/10.1016/j.plgene.2017.05.002
  24. Isolation and characterization of a Δ1-pyrroline-5-carboxylate synthetase (NtP5CS) from Nitraria tangutorum Bobr. and functional comparison with its Arabidopsis homologue vol.41, pp.1, 2014, https://doi.org/10.1007/s11033-013-2893-8
  25. A Chloroplast-Localized Rubredoxin Family Protein Gene from Puccinellia tenuiflora (PutRUB) Increases NaCl and NaHCO3 Tolerance by Decreasing H2O2 Accumulation vol.17, pp.6, 2016, https://doi.org/10.3390/ijms17060804
  26. Ectopic Expression of Aeluropus littoralis Plasma Membrane Protein Gene AlTMP1 Confers Abiotic Stress Tolerance in Transgenic Tobacco by Improving Water Status and Cation Homeostasis vol.18, pp.4, 2017, https://doi.org/10.3390/ijms18040692
  27. Arabidopsis heterotrimeric G protein β subunit interacts with a plasma membrane 2C-type protein phosphatase, PP2C52 vol.1823, pp.12, 2012, https://doi.org/10.1016/j.bbamcr.2012.10.001
  28. Stage- and tissue-specific expression of rice OsIsu1 gene encoding a scaffold protein for mitochondrial iron–sulfur-cluster biogenesis vol.31, pp.8, 2009, https://doi.org/10.1007/s10529-009-0004-7
  29. Identification and characterization of the RCI2 gene family in maize (Zea mays) vol.93, pp.3, 2014, https://doi.org/10.1007/s12041-014-0421-9
  30. Physiological and Proteomic Analysis of Salinity Tolerance inPuccinellia tenuiflora vol.10, pp.9, 2011, https://doi.org/10.1021/pr101102p
  31. Plant abiotic stress-related RCI2/PMP3s: multigenes for multiple roles vol.243, pp.1, 2016, https://doi.org/10.1007/s00425-015-2386-1
  32. Proteomic discovery of H2O2 response in roots and functional characterization of PutGLP gene from alkaligrass vol.248, pp.5, 2018, https://doi.org/10.1007/s00425-018-2940-8
  33. Overexpression of AlTMP2 gene from the halophyte grass Aeluropus littoralis in transgenic tobacco enhances tolerance to different abiotic stresses by improving membrane stability and deregulating some stress-related genes vol.255, pp.4, 2018, https://doi.org/10.1007/s00709-018-1223-3
  34. Physiological and comparative proteomic analyses of saline-alkali NaHCO3-responses in leaves of halophyte Puccinellia tenuiflora pp.1573-5036, 2019, https://doi.org/10.1007/s11104-019-03955-9