Skip to main content
Log in

Chloride Channels and Transporters of the CLC Family in Plants

  • REVIEWS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Proteins of the chloride channel family CLC (ChLoride Channel) are found in prokaryotes and eukaryotes. The family includes anion channels and anion/proton antiporters. In plants, the CLC proteins are found in various tissues and diverse intracellular membranes. They perform multiple functions and play important physiological roles, such as nitrate and chloride homeostasis at the cellular and whole plant levels, the regulation of transmembrane electrical potential and lumenal pH in organelles, the distribution of newly synthesized proteins among intracellular compartments, and the formation of plant resistance to biotic and abiotic stress factors. This review describes the currently known CLC proteins of plant origin whose genes are identified at the molecular-genetic and functional levels; the properties of CLC proteins from Arabidopsis thaliana (L.) Heynh. and other plant species are discussed with emphasis on the results obtained in the last decade. The functional and structural aspects of plant CLC proteins, as well as their physiological roles under normal and stressful conditions, are considered. A hypothesis is put forward that the endosomes and the proteins of the CLC family localized in endosomal membranes are involved in maintaining the anionic balance in the cytoplasm. The prospects of further studies on plant CLC proteins are briefly considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Miller, C. and White, M.M., A voltage-dependent chloride conductance channel from Torpedo electroplax membrane, Ann. New York Acad. Sci., 1980, vol. 341.https://doi.org/10.1111/j.1749-6632.1980.tb47197.x

  2. Jentsch, T.J., Steinmeyer, K., and Schwarz, G., Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in Xenopus oocytes, Nature, 1990, vol. 348, p. 510. https://doi.org/10.1038/348510a0

    Article  PubMed  CAS  Google Scholar 

  3. Miller, C., ClC chloride channels viewed through a transporter lens, Nature, 2006, vol. 440, p. 484. https://doi.org/10.1038/nature04713

    Article  PubMed  CAS  Google Scholar 

  4. Barbier-Brygoo, H., Vinauger, M., Colcombet, J., Ephritikhine, G., Frachisse, J.M., and Maurel, C., Anion channels in higher plants: functional characterization, molecular structure and physiological role, BBA–Biomembranes, 2000, vol. 1465, p. 199. https://doi.org/10.1016/S0005-2736(00)00139-5

  5. Accardi, A., Structure and gating of CLC channels and exchangers, J. Physiol., 2015, vol. 593, p. 4129. https://doi.org/10.1113/JP270575

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Fahike, C., Yu, H.T., Beck, C.L., Rhodes, T.H., and George, J., Pore-forming segments in voltage-gated chloride channels, Nature, 1997, vol. 390, p. 529. https://doi.org/10.1038/37391

    Article  CAS  Google Scholar 

  7. Barbier-Brygoo, H., de Angeli, A., Filleur, S., Frachisse, J.-M., Gambale, F., Thomine, S., and Wege, S., Anion channels/transporters in plants: from molecular bases to regulatory networks, Annu. Rev. Plant Biol., 2011, vol. 62, p. 25. https://doi.org/10.1146/annurev-arplant-042110-103741

    Article  PubMed  CAS  Google Scholar 

  8. Dutzler, R., Campbell, E.B., Cadene, M., Chait, B.T., and MacKinnon,R.,X-ray structure of a CLC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity, Nature, 2002, vol. 415, p. 287. https://doi.org/10.1038/415287a

    Article  PubMed  CAS  Google Scholar 

  9. Dutzler, R.,Campbell, E.B., and MacKinnon,R.,Gating the selectivity filter in ClC chloride channels, Scien-ce, 2003, vol. 300, p. 108. https://doi.org/10.1126/science.1082708

    Article  CAS  Google Scholar 

  10. Picollo, A., Malvezzi, M., Houtman, J.C.D., and Accardi, A., Basis of substrate binding and conservation of selectivity in the CLC family of channels and transporters, Nat. Struct. Mol. Biol., 2009, vol. 16, p. 1294. https://doi.org/10.1038/nsmb.1704

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Zifarelli, G. and Pusch, M., Conversion of the 2Cl/1H+ antiporter ClC-5 in a \({\text{NO}}_{3}^{ - }\)/H+ antiporter by a single point mutation, EMBO J., 2009, vol. 28, p. 175. https://doi.org/10.1038/emboj.2008.284

    Article  PubMed  PubMed Central  Google Scholar 

  12. Bergsdorf, E.Y., Zdebik, A.A., and Jentsch, T.J., Residues important for nitrate/proton coupling in plant and mammalian CLC transporters, J. Biol. Chem., 2009, vol. 284, p. 11184. https://doi.org/10.1074/jbc.M901170200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Wege, S., Jossier, M., Filleur, S., Thomine, S., Barbier-Brygoo, H., Gambale, F., and de Angeli, A., The proline 160 in the selectivity filter of the Arabidopsis \({\text{NO}}_{3}^{ - }\)/H+ exchanger AtCLCa is essential for nitrate accumulation in planta, Plant J., 2010, vol. 63, p. 861. https://doi.org/10.1111/j.1365-313X.2010.04288.x

    Article  PubMed  Google Scholar 

  14. Accardi, A., Walden, M., Nguitragool, W., Jayaram, H., Williams, C., and Miller, C., Separate ion pathways in a Cl/H+ exchanger, J. Gen. Physiol., 2005, vol. 126, p. 563. https://doi.org/10.1085/jgp.200509417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Jentsch, T.J. and Pusch, M., CLC chloride channels and transporters: structure, function, physiology, and disease, Physiol. Rev., 2018, vol. 98, p. 1493. https://doi.org/10.1152/physrev.00047.2017

    Article  PubMed  CAS  Google Scholar 

  16. Wei, P., Che, B., Shen, L., Cui, Y., Wu, S., Cheng, C., Liu, F., Li, M.W., Yu, B., and Lam, H.M., Identification and functional characterization of the chloride channel gene, GsCLC-c2 from wild soybean, BMC Plant Biol., 2019, vol. 19, p. 121. https://doi.org/10.1186/s12870-019-1732-z

    Article  PubMed  PubMed Central  Google Scholar 

  17. Zhang, H., Jin, J., Jin, L., Li, Z., Xu, G., Wang, R., Zhang, J., Zhai, N., Chen, Q., Liu, P., Chen, X., Zheng, Q., and Zhou, H., Identification and analysis of the chloride channel gene family members in tobacco (Nicotiana tabacum), Gene, 2018, vol. 676, p. 56. https://doi.org/10.1016/j.gene.2018.06.073

    Article  PubMed  CAS  Google Scholar 

  18. Liao, Q., Zhou, T., Yao, J.Y., Han, Q.F., Song, H.X., Guan, C.Y., Hua, Y.P., and Zhang, Z.H., Genome-scale characterization of the vacuole nitrate transporter Chloride Channel (CLC) genes and their transcriptional responses to diverse nutrient stresses in allotetraploid rapeseed, PLoS One, 2018, vol. 13: e0208648.https://doi.org/10.1371/journal.pone.0208648

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lv, Q., Tang, R., Liu, H., Gao, X., Li, Y., Zheng, H., and Zhang, H., Cloning and molecular analyses of the Arabidopsis thaliana chloride channel gene family, Plant Sci., 2009, vol. 176, p. 650. https://doi.org/10.1016/j.plantsci.2009.02.006

    Article  CAS  Google Scholar 

  20. Von der Fecht-Bartenbach, J., Bogner, M., Krebs, M., Stierhof, Y.D., Schumacher, K., and Ludewig, U., Function of the anion transporter AtCLC-d in the trans-Golgi network, Plant J., 2007, vol. 50, p. 466. https://doi.org/10.1111/j.1365-313X.2007.03061.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Sun, H., Shen, L., Qin, Y., Liu, X., Hao, K., Li, Y., Wang, J., Yang, J., and Wang, F., CLC-Nt1 affects Po-tato Virus Y infection via regulation of endoplasmic reticulum luminal pH, New Phytol., 2018, vol. 220, p. 539. https://doi.org/10.1111/nph.15310

    Article  PubMed  CAS  Google Scholar 

  22. Jentsch, T.J., CLC chloride channels and transporters: from genes to protein structure, pathology and physiology, Crit. Rev. Biochem. Mol. Biol., 2008, vol. 43, p. 3. https://doi.org/10.1080/10409230701829110

    Article  PubMed  CAS  Google Scholar 

  23. Jentsch, T.J., Discovery of CLC transport proteins: cloning, structure, function and pathophysiology, J. Physiol., 2015, vol. 593, p. 4091. https://doi.org/10.1113/JP270043

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Stauber, T., Weinert, T., and Jentsch, T.J., Cell biology and physiology of CLC chloride channels and transporters, Compr. Physiol., 2012, vol. 2, p. 1701. https://doi.org/10.1002/cphy.c110038

    Article  PubMed  Google Scholar 

  25. Poroca, D.R., Pelis, R.M., and Chappe, V.M., ClC channels and transporters: structure, physiological functions, and implications in human chloride channelopathies, Front. Pharmacol., 2017, vol. 8, p. 151. https://doi.org/10.3389/fphar.2017.00151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Zifarelli, G. and Pusch, M., CLC transport proteins in plants, FEBS Lett., 2010, vol. 584, p. 2122. https://doi.org/10.1016/j.febslet.2009.12.042

    Article  PubMed  CAS  Google Scholar 

  27. Hechenberger, M., Schwappach, B., Fischer, W.N., Frommer, W.B., Jentsch, T.J., and 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., 1996, vol. 271, p. 33632. https://doi.org/10.1074/jbc.271.52.33632

    Article  PubMed  CAS  Google Scholar 

  28. Marmagne, A., Vinauger-Douard, M., Monachello, D., de Longevialle, A.F., Charon, C., Allot, M., Rappaport, F., Wollman, F.A., Barbier-Brygoo, H., and 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., 2007, vol. 58, p. 3385. https://doi.org/10.1093/jxb/erm187

    Article  PubMed  CAS  Google Scholar 

  29. Nguyen, C.T., Agorio, A., Jossier, M., Depré, S., Thomine, S., and Filleur, S., Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana, Plant Cell Physiol., 2015, vol. 57, p. 764. https://doi.org/10.1093/pcp/pcv169

    Article  PubMed  CAS  Google Scholar 

  30. Jossier, M., Kroniewicz, L., Dalmas, F., Le Thiec, D., Ephritikhine, G., Thomine, S., Barbier-Brygoo, H., Vavasseur, A., Filleur, S., and Leonhardt, N., The A-rabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance, Plant J., 2010, vol. 64, p. 563. https://doi.org/10.1111/j.1365-313X.2010.04352.x

    Article  PubMed  CAS  Google Scholar 

  31. De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J.M., Thomine, S., Gambale, F., and Barbier-Brygoo, H., The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles, N-ature, 2006, vol. 442, p. 939. https://doi.org/10.1038/nature05013

    Article  CAS  Google Scholar 

  32. Von der Fecht-Bartenbach, J., Bogner, M., Dynowski, M., and Ludewig, U., CLC-b-mediated \({\text{NO}}_{3}^{ - }\)/H+ exchange across the tonoplast of Arabidopsis vacuoles, Plant Cell Physiol., 2010, vol. 51, p. 960. https://doi.org/10.1093/pcp/pcq062

    Article  PubMed  Google Scholar 

  33. Geelen, D., Lurin, C., Bouchez, D., Frachisse, J.M., Lelièvre, F., Courtial, B., Barbier-Brygoo, H., and Maurel, C., Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content, Plant J., 2000, vol. 21, p. 259. https://doi.org/10.1046/j.1365-313X.2000.00680.x

    Article  PubMed  CAS  Google Scholar 

  34. Wege, S., de Angeli, A., Droillard, M.J., Kroniewicz, L., Merlot, S., Cornu, D., Gambale, F., Martinoia, E., Barbier-Brygoo, H., Thomine, S., Leonhardt, N., and Filleur, S., Phosphorylation of the vacuolar anion exchanger AtCLCa is required for the stomatal response to abscisic acid, Sci. Signal., 2014, vol. 7: ra65.https://doi.org/10.1126/scisignal.2005140

    Article  PubMed  CAS  Google Scholar 

  35. Gifford, M.L., Dean, A., Gutierrez, R.A., Coruzzi, G.M., and Birnbaum, K.D., Cell-specific nitrogen responses mediate developmental plasticity, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, p. 803. https://doi.org/10.1073/pnas.0709559105

    Article  PubMed  Google Scholar 

  36. Carpaneto, A., Boccaccio, A., Lagostena, L., Di Zanni, E., and Scholz-Starke, J., The signaling lipid phosphatidylinositol-3,5-bisphosphate targets plant CLC-a anion/H+ exchange activity, EMBO Rep., 2017, vol. 18, p. 1100. https://doi.org/10.15252/embr.201643814

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. De Angeli, A., Moran, O., Wege, S., Filleur, S., Ephritikhine, G., Thomine, S., Barbier-Brygoo, H., and Gambale, F., ATP binding to the C terminus of the Arabidop-sis thaliana nitrate/proton antiporter, AtCLCa, regulates nitrate transport into plant vacuoles, J. Biol. Chem., 2009, vol. 284, p. 26526.doihttps://doi.org/10.1074/jbc.M109.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Monachello, D., Allot, M., Oliva, S., Krapp, A., Daniel-Vedele, F., Barbier-Brygoo, H., and Ephritikhine, G., Two anion transporters AtCLCa and AtCLCe fulfil interconnecting but not redundant roles in nitrate assimilation pathways, New Phytol., 2009, vol. 183, p. 88. https://doi.org/10.1111/j.1469-8137.2009.02837.x

    Article  PubMed  CAS  Google Scholar 

  39. Han, Y.L., Song, H.X., Liao, Q., Yu, Y., Jian, S.F., Lepo, J.E., Liu, Q., Rong, X.M., Tian, C., Zeng, J., Guan, C.Y., Ismail, A.M., and Zhang, Z.H., Nitrogen use efficiency is mediated by vacuolar nitrate sequestration capacity in roots of Brassica napus, Plant Physiol., 2016, vol. 170, p. 1684. https://doi.org/10.1104/pp.15.01377

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Whiteman, S.A., Serazetdinova, L., Jones, A.M.E., Sanders, D., Rathjen, J., Peck, S.C., and Maathuis, F.J.M., Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Ar-abidopsis thaliana, Proteomics, 2008, vol. 8, p. 3536. https://doi.org/10.1002/pmic.200701104

    Article  PubMed  CAS  Google Scholar 

  41. Hu, R., Zhu, Y., Wei, J., Chen, J., Shi, H., Shen, G., and Zhang, H., Overexpression of PP2A-C5 that encodes the catalytic subunit 5 of protein phosphatase 2A in Arabidopsis confers better root and shoot development under salt conditions, Plant Cell Environ., 2017, vol. 40, p. 150. https://doi.org/10.1111/pce.12837

    Article  PubMed  CAS  Google Scholar 

  42. Kharitonashvili, E.V., Chernyi, S.G., and Alekhina, N.D., Formation of the nitrate storage pool in roots of wheat seedlings, Russ. Plant Physiol., 1993, vol. 40, p. 443.

    CAS  Google Scholar 

  43. Izmailov, S.F., Saturation and utilization of nitrate pools in pea and sugar beet leaves, Russ. J. Plant Physiol., 2004, vol. 51, p. 189.

    Article  CAS  Google Scholar 

  44. Bläsing, O.E., Gibon, Y., Günther, M., Höhne, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheible, W.R., and Stitt, M., Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis, Plant Cell, 2005, vol. 17, p. 3257. https://doi.org/10.1105/tpc.105.035261

  45. Harada, H., Kuromori, T., Hirayama, T., Shinozaki, K., and 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., 2004, vol. 55, p. 2005. https://doi.org/10.1093/jxb/erh224

    Article  PubMed  CAS  Google Scholar 

  46. Vialaret, J., Di Pietro, M., Hem, S., Maurel, C., Rossignol, M., and Santoni, V., Phosphorylation dynamics of membrane proteins from Arabidopsis roots submitted to salt stress, Proteomics, 2014, vol. 14, p. 1058. https://doi.org/10.1002/pmic.201300443

    Article  PubMed  CAS  Google Scholar 

  47. Guo, W., Zuo, Z., Cheng, X., Sun, J., Li, H., Li, L., and Qiu, J.L., The chloride channel family gene CLCd negatively regulates pathogen-associated molecular pattern (PAMP)-triggered immunity in Arabidopsis, J. Exp. Bot., 2014, vol. 65, p. 1205. https://doi.org/10.1093/jxb/ert484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Herdean, A., Nziengui, H., Zsiros, O., Solymosi, K., Garab, G., Lundin, B., and Spetea, C., The Arabidopsis thylakoid chloride channel AtCLCe functions in chloride homeostasis and regulation of photosynthetic electron transport, Front. Plant Sci., 2016, vol. 7, p. 115. https://doi.org/10.3389/fpls.2016.00115

    Article  PubMed  PubMed Central  Google Scholar 

  49. Lurin, C., Geelen, D., Barbier-Brygoo, H., Guern, J., and Maurel, C., Cloning and functional expression of a plant voltage-dependent chloride channel, Plant Cell, 1996, vol. 8, p. 701.https://doi.org/10.1105/tpc.8.4.701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Lurin, C., Güclü, J., Cheniclet, C., Carde, J.P., Barbier-Brygoo, H., and Maurel, C., CLC-Nt1, a putative chloride channel protein of tobacco, co-localizes with mitochondrial membrane markers, Biochem. J., 2000, vol. 348, p. 291. https://doi.org/10.1042/0264-6021:3480291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Diédhiou, C.J. and Golldack, D., Salt-dependent regulation of chloride channel transcripts in rice, Plant Sci., 2006, vol. 170, p. 793. https://doi.org/10.1016/j.plantsci.2005.11.014

  52. Nakamura, A., Fukuda, A., Sakai, S., and 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., 2006, vol. 47, p. 32.https://doi.org/10.1093/pcp/pci220

    Article  PubMed  CAS  Google Scholar 

  53. Li, W.Y.F., Wong, F.L., Tsai, S.N., Phang, T.H., Shao, G., and Lam, H.M., Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells, Plant Cell Environ., 2006, vol. 29, p. 1122. https://doi.org/10.1016/j.diamond.2005.12.024

    Article  PubMed  CAS  Google Scholar 

  54. Tampieri, E., Baraldi, E., Carnevali, F., Frascaroli, E., and 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. Bioenerg. Biomembr., 2011, vol. 43, p. 611. https://doi.org/10.1007/s10863-011-9386-z

    Article  PubMed  CAS  Google Scholar 

  55. Yang, G., Zou, H., Wu, Y., Liu, H., and Yuan, Y., Identification and characterisation of candidate genes involved in chilling responses in maize (Zea mays L.), Plant Cell Tissue Organ Cult., 2011, vol. 106, p. 127. https://doi.org/10.1007/s11240-010-9900-8

    Article  CAS  Google Scholar 

  56. Wang, S., Su, S.Z., Wu, Y., Li, S.P., Shan, X.H., Liu, H.K., Wang, S., and Yuan, Y.P., Overexpression of maize chloride channel gene ZmCLC-d in Arabido-psis thaliana improved its stress resistance, Biol-. Plant., 2015, vol. 59, p. 55. https://doi.org/10.1007/s10535-014-0468-8

    Article  CAS  Google Scholar 

  57. Wei, Q., Liu, Y., Zhou, G., Li, Q., Yang, C., and Peng, S., Overexpression of CsCLCc, a chloride channel gene from Poncirus trifoliata, enhances salt tolerance in Arabidopsis, Plant Mol. Biol. Rep., 2013, vol. 31, p. 1548. https://doi.org/10.1007/s11105-013-0592-1

    Article  CAS  Google Scholar 

  58. Wei, Q.J., Gu, Q.Q., Wang, N.N., Yang, C.Q., and Peng, S.A., Molecular cloning and characterization of the chloride channel gene family in trifoliate orange, Biol. Plant., 2015, vol. 59, p. 645. https://doi.org/10.1007/s10535-015-0532-z

    Article  CAS  Google Scholar 

  59. Zhou, C., Wang, H., Zhu, J., and Liu, Z., Molecular cloning, subcellular localization and functional analysis of ThCLC-a from Thellungiella halophila, Plant Mol. Biol. Rep., 2013, vol. 31, p. 783. https://doi.org/10.1007/s11105-012-0545-0

    Article  CAS  Google Scholar 

  60. Nedelyaeva, O.I., Shuvalov, A.V., Mayorova, O.V., Yurchenko, A.A., Popova, L.G., Balnokin, Y.V., and Karpichev, I.V., Cloning and functional analysis of S-aCLCc1, a gene belonging to the chloride channel family (CLC), from the halophyte Suaeda altissima (L.) Pall, Dokl. Biochem. Biophys., 2018, vol. 481, p. 186. https://doi.org/10.1134/S1607672918040026

    Article  PubMed  CAS  Google Scholar 

  61. Nedelyaeva, O.I., Shuvalov, A.V., Karpichev, I.V., Beliaev, D.V., Myasoedov, N.A., Khalilova, L.A., Khramov, D.E., Popova, L.G., and Balnokin, Y.V., Molecular cloning and characterisation of SaCLCa1, a novel protein of the chloride channel (CLC) family from the halophyte Suaeda altissima (L.) Pall, J. Plant Physiol., 2019, vol. 240, p. 152995.https://doi.org/10.1016/j.jplph.2019.152995

    Article  PubMed  CAS  Google Scholar 

  62. Adkar-Purushothama, C.R., Iyer, P.S., and Perreault, J.P., Potato spindle tuber viroid infection triggers degradation of chloride channel protein CLC-b-like and ribosomal protein S3a-like mRNAs in tomato plants, Sci. Rep., 2017, vol. 7, p. 8341.https://doi.org/10.1038/s41598-017-08823-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Wong, T.H., Li, M.W., Yao, X.Q., and Lam, H.M., The GmCLC1 protein from soybean functions as a chloride ion transporter, J. Plant Physiol., 2013, vol. 170, p. 101. https://doi.org/10.1016/j.jplph.2012.08.003

    Article  PubMed  CAS  Google Scholar 

  64. Wei, P., Wang, L., Liu, A., Yu, B., and Lam, H.M., GmCLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean, Front. Plant Sci., 2016, vol. 7, p. 1082.https://doi.org/10.3389/fpls.2016.01082

    Article  PubMed  PubMed Central  Google Scholar 

  65. Sun, W., Deng, D., Yang, L., Zheng, X., Yu, J., Pan, H., and Zhuge, Q., Overexpression of the chloride channel gene (GmCLC1) from soybean increases salt tolerance in transgenic Populus deltoides × P. euramericana “Nanlin895,” Plant Omics, 2013,vol. 6,p. 347.

    CAS  Google Scholar 

  66. Yang, L., Jin, Y., Huang, W., Sun, Q., Liu, F., and Huang, X., Full-length transcriptome sequences of ephemeral plant Arabidopsis pumila provides insight into gene expression dynamics during continuous salt stress, BMC Genomics, 2018, vol. 19, p. 717.https://doi.org/10.1186/s12864-018-5106-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Migocka, M., Warzybok, A., Papierniak, A., and Kłobus, G., \({\text{NO}}_{3}^{ - }\)/H+ antiport in the tonoplast of cucumber root cells is stimulated by nitrate supply: evidence for a reversible nitrate-induced phosphorylation of vacuolar \({\text{NO}}_{3}^{ - }\)/H+ antiport, PLoS One, 2013, vol. 8: e73972.https://doi.org/10.1371/journal.pone.0073972

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Xing, A., Ma, Y., Wu, Z., Nong, S., Zhu, J., Sun, H., Tao, J., Wen, B., Zhu, X., Fang, W., Li, X., and Wang, Y., Genome-wide identification and expression analysis of the CLC superfamily genes in tea plants (C-amellia sinensis), Funct. Integr. Genomics, 2020, https://doi.org/10.1007/s10142-019-00725-9

  69. Li, Q., Ding, G., Yang, N., White, P.J., Ye, X., Cai, H., Lu, J., Shi, L., and Xu, F., Comparative genome and transcriptome analysis unravels key factors of nitrogen use efficiency in Brassica napus L.,Plant Cell Environ., 2019, vol. 43, p. 712. https://doi.org/10.1111/pce.13689

    Article  PubMed  CAS  Google Scholar 

  70. Bassil, E., Ohto, M., Esumi, T., Tajima, H., Zhu, Z., Cagnac, O., Belmonte, M., Peleg, Z., Yamaguchi, T., and Blumwald, E., The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development, Plant Cell, 2011, vol. 23, p. 224. https://doi.org/10.1105/tpc.110.079426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Shuvalov, A.V., Orlova, J.V., Khalilova, L.A., Myasoedov, N.A., Andreev, I.M., Belyaev, D.V., and Balnokin, Y.V., Evidence for the functioning of a Cl/H+ antiporter in the membranes isolated from root cells of the halophyte Suaeda altissima and enriched with Golgi membranes, Russ. J. Plant Physiol., 2015, vol. 62, p. 45. https://doi.org/10.1134/s1021443715010124

    Article  CAS  Google Scholar 

  72. Balnokin, Y.V., Kurkova, E.B., Khalilova, L.A., Myasoedov, N.A., and Yusufov, A.G., Pinocytosis in the root cells of a salt-accumulating halophyte Suaeda al-tissima and its possible involvement in chloride transport, Russ. J. Plant Physiol., 2007, vol. 54, p. 797. https://doi.org/10.1134/S102144370706012X

    Article  CAS  Google Scholar 

  73. Hamaji, K., Nagira, M., Yoshida, K., Ohnishi, M., Oda, Y., Uemura, T., Goh, T., Sato, M.H., Morita, M.T., Tasaka, M., Hasezawa, S.I., Nakano, A., Hara-Nishimura, I., Maeshima, M., Fukaki, H., et al., Dynamic aspects of ion accumulation by vesicle traffic under salt stress in Arabidopsis, Plant Cell Physiol., 2009, vol. 50, p. 2023. https://doi.org/10.1093/pcp/pcp143

    Article  PubMed  CAS  Google Scholar 

  74. Baral, A., Irani, N.G., Fujimoto, M., Nakano, A., Mayor, S., and Mathew, M.K., Salt-induced remodeling of spatially restricted clathrin-independent endocytic pathways in Arabidopsis root, Plant Cell, 2015, vol. 27, p. 1297. https://doi.org/10.1105/tpc.15.00154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Orlova, Y.V., Sergienko, O.V., Khalilova, L.A., Voronkov, A.S., Fomenkov, A.A., Nosov, A.V., Popova, L.G., Shuvalov, A.V., Ryabova, A.V., and Balnokin, Y.V., Sodium transport by endocytic vesicles in cultured Arabidopsis thaliana (L.) Heynh. cells, In Vitro Cell. Dev. Biol.: Plant, 2019, vol. 55, p. 359. https://doi.org/10.1007/s11627-019-10005-7

    Article  CAS  Google Scholar 

  76. Khalilova, L.A., Sergienko, O.V., Orlova, Y.V., Myasoedov, N.A., Karpichev, I.V., and Balnokin, Y.V., Arabidopsis thaliana mutant with T-DNA insertion in the Flot1 (At5g2525) gene promotor possesses increased resistance to NaCl, Russ. J. Plant Physiol., 2020, vol. 67, p. 275. https://doi.org/10.1134/S1021443720020077

    Article  CAS  Google Scholar 

  77. Mimura, T., Kura-Hotta, M., Tsujimura, T., Ohnishi, M., Miura, M., Okazaki, Y., Mimura, M., Maeshima, M., and Washitani-Nemoto, S., Rapid increase of vacuolar volume in response to salt stress, Planta, 2003, vol. 216, p. 397. https://doi.org/10.1007/s00425-002-0878-2

    Article  PubMed  CAS  Google Scholar 

  78. Ivanova, T.V., Maiorova, O.V., Orlova, Y.V., Kuznetsova, E.I., Khalilova, L.A., Myasoedov, N.A., Balnokin, Y.V., and Tsydendambaev, V.D., Cell ultrastructure and fatty acid composition of lipids in vegetative organs of Chenopodium album L. under salt stress conditions, Russ. J. Plant Physiol., 2016, vol. 63, p. 763. https://doi.org/10.1134/S1021443716060054

    Article  CAS  Google Scholar 

  79. Jaillais, Y., Fobis-Loisy, I., Miège, C., and Gaude, T., Evidence for a sorting endosome in Arabidopsis root cells, Plant J., 2008, p. 237. https://doi.org/10.1111/j.1365-313X.2007.03338.x

  80. Feraru, E., Feraru, M.I., Asaoka, R., Paciorek, T., de Rycke, R., Tanaka, H., Nakano, A., and Frimla, J., BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis, Plant Cell, 2012, vol. 24, p. 3074. https://doi.org/10.1105/tpc.112.098152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Cui, Y., Shen, J., Gao, C., Zhuang, X., Wang, J., and Jiang, L., Biogenesis of plant prevacuolar multivesicular bodies, Mol. Plant, 2016, vol. 9, p. 774. https://doi.org/10.1016/j.molp.2016.01.011

    Article  PubMed  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

We are grateful to Doctor of Science, leading researcher of the Laboratory for Ion Transport and Salt Tolerance at Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, L.G. Popova for critical reading of the manuscript and helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. I. Nedelyaeva.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any studies with human participants or animals performed by any of the authors.

CONFLICT OF INTEREST

The authors declare they have no conflicts of interest.

Additional information

Translated by A. Bulychev

Abbreviations: CBS-domain—cystathionine-β-synthase domain; CLC—chloride channel; EPR—endoplasmic reticulum; GA—Golgi apparatus; WT—wild type.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nedelyaeva, O.I., Shuvalov, A.V. & Balnokin, Y.V. Chloride Channels and Transporters of the CLC Family in Plants. Russ J Plant Physiol 67, 767–784 (2020). https://doi.org/10.1134/S1021443720050106

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443720050106

Keywords:

Navigation