biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 59:55-64, 2015 | DOI: 10.1007/s10535-014-0468-8

Overexpression of maize chloride channel gene ZmCLC-d in Arabidopsis thaliana improved its stress resistance

S. Wang1, S. Z. Su1, Y. Wu1, S. P. Li1, X. H. Shan1, H. K. Liu1, S. Wang1, Y. P. Yuan1,*
1 College of Plant Science, Jilin University, Changchun, P.R. China

In plant cells, anion channels and transporters are essential for key functions. Members of the chloride channel (CLC) family located in intracellular organelles are required for anion accumulation, pH adjustment, and salt tolerance. Here, we cloned a maize (Zea mays L.) CLC gene, named ZmCLC-d, and found that its transcription was up-regulated under cold, drought, salt, and heat stresses, and after hydrogen peroxide (H2O2) and abscisic acid (ABA) treatments. The overexpression of ZmCLC-d in Arabidopsis conferred tolerance to cold, drought, and salt stresses; this tolerance was primarily displayed by an increased germination rate, root length, plant survival rate, antioxidant enzyme (catalase, peroxidase, and superoxide dismutase) activities, and a reduced accumulation of Cl- in transgenic plants as compared with wild type (WT) plants. The accumulation of H2O2 and superoxide anion in leaves of the ZmCLC-d-overexpressing plants is much less than that of the WT plants. The expressions of some stress related genes, such as CBF1, CBF2, CBF3, DREB2A, and RCI2A, increased to a greater extent in the ZmCLC-d-overexpressing plants than in the WT. Our results strongly suggest that ZmCLC-d played an important role in stress tolerance.

Keywords: catalase; cold; heat; H2O2; peroxidase; superoxide dismutase; water stress; Zea mays
Subjects: chloride channel; cold stress; temperature - low; water stress; catalase; peroxidase; superoxide dismutase; salinity; amino acid sequences; transgenic plants; hydrogen peroxide; superoxide radical; malondialdehyde; maize

Received: December 19, 2013; Revised: June 1, 2014; Accepted: June 19, 2014; Published: January 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Wang, S., Su, S.Z., Wu, Y., Li, S.P., Shan, X.H., Liu, H.K., Wang, S., & Yuan, Y.P. (2015). Overexpression of maize chloride channel gene ZmCLC-d in Arabidopsis thaliana improved its stress resistance. Biologia plantarum, 59(1), 55-64. doi: 10.1007/s10535-014-0468-8
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filebpl-201501-0007_S1.pdf

    File size: 82.36 kB

    References

    1. Anderson, M.E., Greenwald, R.A. (ed.): Handbook of Methods for Oxygen Radical Research. CRC Press, Boca Raton, 1985.
    2. Bateman, A., Coin, L., Durbin, R., Finn, R.D., Hollich, V., Griffiths-Jones, S., Eddy, S.R.: The Pfam protein families database. - Nucl. Acids Res, 32(Suppl. 1): D138-D141, 2004. Go to original source...
    3. Bergsdorf, E.Y., Zdebik, A.A., Jentsch, T.J.: Residues important for nitrate/proton coupling in plant and mammalian CLC transporters. - J. biol. Chem. 284: 11184-11193, 2009. Go to original source...
    4. Clough, S.J., Bent, A.F.: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. - Plant J. 16: 735-743, 1998. Go to original source...
    5. De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J.M., Thomine, S., Gambale, F., Barbier-Brygoo, H.: The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. - Nature 442: 939-942, 2006. Go to original source...
    6. Diédhiou, C.J., Golldack, D.: Salt-dependent regulation of chloride channel transcripts in rice. - Plant Sci. 170: 793-800, 2006. Go to original source...
    7. Dubouzet, J. G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E. G., Miura, S., Yamaguchi-Shinozaki, K.: OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high salt- and cold-responsive gene expression. - Plant J. 33: 751-763, 2003. Go to original source...
    8. Geelen, D., Lurin, C., Bouchez, D., Frachisse, J.M., Lelièvre, F., Courtial, B., Maurel, C.: Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. - Plant J. 21: 259-267, 2000. Go to original source...
    9. Hänsch, R., Mendel, R.R.: Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). - Curr. Opin. Plant Biol. 12: 259-266, 2009. Go to original source...
    10. Harada, H., Kuromori, T., Hirayama, T., Shinozaki, K., Leigh, R.A.: Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate levels. - J. exp. Bot. 55: 2005-2014, 2004. Go to original source...
    11. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J. Plant cellular and molecular responses to high salinity. - Annu. Rev. Plant Biol. 51: 463-499, 2000. Go to original source...
    12. Hechenberger, M., Schwappach, B., Fischer, W.N., Frommer, W.B., Jentsch, T.J., Steinmeyer, K.: A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. - J. biol. Chem. 271: 33632-33638, 1996. Go to original source...
    13. Huang, J.G., Yang, M., Liu, P., Yang, G.D., Wu, C.A., Zheng, C.C.: GhDREB1 enhances abiotic stress tolerance, delays GA-mediated development and represses cytokinin signalling in transgenic Arabidopsis. - Plant Cell Environ. 32: 1132-1145, 2009. Go to original source...
    14. Isayenkov, S., Isner, J.C., Maathuis, F.J.: Vacuolar ion channels: roles in plant nutrition and signalling. - FEBS Lett. 584: 1982-1988, 2010. Go to original source...
    15. Jentsch, T.J.: CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. - Crit. Rev. Biotechnol. 43: 3-36, 2008. Go to original source...
    16. Jossier, M., Kroniewicz, L., Dalmas, F., Le Thiec, D., Ephritikhine, G., Thomine, S., Leonhardt, N.: The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. - Plant J. 64: 563-576, 2010. Go to original source...
    17. Kizis, D.: Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. - Plant J. 30: 679-689, 2002. Go to original source...
    18. Kurkela, S., Franck, M.: Cloning and characterization of a coldand ABA-inducible Arabidopsis gene. - Plant. mol. Biol. 15: 137-144, 1990. Go to original source...
    19. Läuchli, A.: Salt exclusion: an adaptation of legumes for crops and pastures under saline conditions. - In: Staples, R.C. (ed.): Salinity Tolerance in Plants: Strategies for Crop Improvement. Pp. 171-187. Wiley, New York 1984.
    20. Letunic, I., Copley, R.R., Schmidt, S., Ciccarelli, F.D., Doerks, T., Schultz, J., Bork, P.: SMART 4.0: towards genomic data integration. - Nucl. Acids Res. 32(Suppl 1): D142-D144, 2004. Go to original source...
    21. Li, W.Y.F., Wong, F.L., Tsai, S.N., Phang, T.H., Shao, G., Lam, H.M.: Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY) -2 cells. - Plant Cell Environ. 29: 1122-1137, 2006. Go to original source...
    22. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K.: Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low temperature-responsive gene expression, respectively, in Arabidopsis. - Plant Cell 10: 1391-1406, 1998. Go to original source...
    23. Lv, Q.D., Tang, R.J., Liu, H., Gao, X.S., Li, Y.Z., Zheng, H.Q., Zhang, H.X.: Cloning and molecular analyses of the Arabidopsis thaliana chloride channel gene family. - Plant Sci. 176: 650-661, 2009. Go to original source...
    24. Marmagne, A., Vinauger Douard, M., Monachello, D., De Longevialle, A.F., Charon, C., Allot, M., Ephritikhine, G.: Two members of the Arabidopsis CLC (chloride channel) family, AtCLCe and AtCLCf, are associated with thylakoid and Golgi membranes, respectively. - J. exp. Bot. 58: 3385-3393, 2007. Go to original source...
    25. Medina, J., Rodríguez Franco, M., Peñalosa, A., Carrascosa, M.J., Neuhaus, G., Salinas, J.: Arabidopsis mutants deregulated in RCI2A expression reveal new signaling pathways in abiotic stress responses. - Plant J. 42: 586-597, 2005. Go to original source...
    26. Mindell, J.A., Maduke, M.: ClC chloride channels. - Genome Biol. 2: 3000-3001, 2001. Go to original source...
    27. Monachello, D., Allot, M., Oliva, S., Krapp, A., Daniel-Vedele, F., Barbier-Brygoo, H., Ephritikhine, G.: Two anion transporters AtClCa and AtClCe fulfil interconnecting but not redundant roles in nitrate assimilation pathways. - New Phytol. 183: 88-94, 2009. Go to original source...
    28. Mukhopadhyay, A., Vij, S., Tyagi, A.K.: Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. - Proc. nat. Acad. Sci. USA 101: 6309-6314, 2004. Go to original source...
    29. Munns, R., Tester, M.: Mechanisms of salinity tolerance. - Annu. Rev. Plant Biol. 59: 651-681, 2008. Go to original source...
    30. Nakamura, A., Fukuda, A., Sakai, S., Tanaka, Y.: Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). - Plant Cell Physiol. 47: 32-42, 2006. Go to original source...
    31. Orozco-Cárdenas, M.L., Ryan, C.A.: Hydrogen peroxide is generated systematically in plant leaves by wounding and systemin via the octadecanoid pathway. - Proc. nat. Acad. Sci. USA 96: 6553-6557, 1999. Go to original source...
    32. Storey, R., Walker, R.R.: Citrus and salinity. - Sci. Hort. 78: 39-81, 1998. Go to original source...
    33. Sun, J., Li, L., Liu, M., Wang, M., Ding, M., Deng, S., Chen, S.: Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. - Plant Cell Tissue Organ Cult. 103: 205-215, 2010. Go to original source...
    34. Tampieri, E., Baraldi, E., Carnevali, F., Frascaroli, E., De Santis, A.: The activity of plant inner membrane anion channel (PIMAC) can be performed by a chloride channel (CLC) protein in mitochondria from seedlings of maize populations divergently selected for cold tolerance. - J. Bioener. Biomembr. 43: 611-621, 2011. Go to original source...
    35. Teakle, N.L., Tyerman, S.D.: Mechanisms of Cl-transport contributing to salt tolerance. - Plant Cell Environ. 33: 566-589, 2010. Go to original source...
    36. Thomashow, M.F.: Role of cold-responsive genes in plant freezing tolerance. - Plant Physiol. 118: 1-8, 1998. Go to original source...
    37. Von der Fecht-Bartenbach, J., Bogner, M., Dynowski, M., Ludewig, U.: CLC-b-mediated NO3 -/H+ exchange across the tonoplast of Arabidopsis vacuoles. - Plant Cell Physiol. 51: 960-968, 2010. Go to original source...
    38. Von der Fecht-Bartenbach, J.V.D., Bogner, M., Krebs, M., Stierhof, Y. D., Schumacher, K., Ludewig, U.: Function of the anion transporter AtCLC-d in the trans-Golgi network. - Plant J. 50: 466-474, 2007. Go to original source...
    39. Wang, X., Xu, W.Z., Xu, Y.Y., Chong, K., Xu, Z.H., Xia, G.X.: Wheat RAN1, a nuclear small G protein, is involved in regulation of cell division in yeast. - Plant Sci. 167: 1183-1190, 2004. Go to original source...
    40. Wang, X., Yang, P., Gao, Q., Liu, X., Kuang, T., Shen, S., He, Y.: Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. - Planta 228: 167-177, 2008. Go to original source...
    41. Wege, S., Jossier, M., Filleur, S., Thomine, S., Barbier-Brygoo, H., Gambale, F., De Angeli, A.: The proline 160 in the selectivity filter of the Arabidopsis NO3 -/H+ exchanger AtCLCa is essential for nitrate accumulation in planta. - Plant J. 63: 861-869, 2010. Go to original source...
    42. White, P.J., Broadley, M.R.: Chloride in soils and its uptake and movement within the plant: a review. - Ann. Bot. 88: 967-988, 2001. Go to original source...
    43. Xin, Z.: Temperature sensing and cold acclimation. - Curr. Opin. Plant Biol. 4: 241-246, 2001. Go to original source...
    44. Yang, G., Zou, H., Wu, Y., Liu, H., Yuan, Y.: Identification and characterisation of candidate genes involved in chilling responses in maize (Zea mays L.). - Plant Cell Tissue Organ Cult. 106: 127-141, 2011. Go to original source...
    45. Zifarelli, G., Pusch, M.: CLC transport proteins in plants. - FEBS Lett. 584: 2122-2127, 2010. Go to original source...

    Return to the content