The Arabidopsis thylakoid chloride channel AtCLCe functions in chloride homeostasis and regulation of photosynthetic electron transport

Frontiers in Plant Science

Volumn 7, Issue FEB2016, 2016, Pages

  Herdean, Andrei ^a   Nziengui, Hugues ^a   Zsiros, Ottó ^b   Solymosi, Katalin ^c   Garab, Győző ^b   Lundin, Björn ^a   Spetea, Cornelia ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Arabidopsis thaliana; Chlorophyll fluorescence; CLC channel; Electron microscopy; Photosynthetic electron transport; Proton motive force; State transition; Thylakoid membrane

Indexed keywords

EID: 84958524202     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00115     Document Type: Article

References (60)

1. Accardi, A., and Miller, C. (2004). Secondary active transport mediated by a prokaryotic homologue of ClC Cl-channels. Nature 427, 803-807. doi: 10.1038/nature02314.
2. Anderson, J. M., Horton, P., Kim, E. H., and Chow, W. S. (2012). Towards elucidation of dynamic structural changes of plant thylakoid architecture. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 3515-3524. doi: 10.1098/rstb.2012.0373.
3. Armbruster, U., Carrillo, L. R., Venema, K., Pavlovic, L., Schmidtmann, E., Kornfeld, A., et al. (2014). Ion antiport accelerates photosynthetic acclimation in fluctuating light environments. Nat. Commun. 5, 5439. doi: 10.1038/ncomms6439.
4. Barbier-Brygoo, H., De Angeli, A., Filleur, S., Frachisse, J. M., Gambale, F., Thomine, S., et al. (2011). Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu. Rev. Plant Biol. 62, 25-51. doi: 10.1146/annurev-arplant-042110-103741.
5. Barzda, V., Mustárdy, L., and Garab, G. (1994). Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes. Biochemistry 33, 10837-10841. doi: 10.1021/bi00201a034.
6. +-ATPase and upregulating its transport activity. Mol. Cell Biol. 27, 7781-7790. doi: 10.1128/MCB.00430-07.
7. Bellafiore, S., Barneche, F., Peltier, G., and Rochaix, J. D. (2005). State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433, 892-895. doi: 10.1038/nature03286.
8. + channel controls photosynthetic light utilization in plants. Science 342, 114-118. doi: 10.1126/science.1242113.
9. Chuartzman, S. G., Nevo, R., Shimoni, E., Charuvi, D., Kiss, V., Ohad, I., et al. (2008). Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20, 1029-1039. doi: 10.1105/tpc.107.055830.
10. Cruz, J. A., Avenson, T. J., Kanazawa, A., Takizawa, K., Edwards, G. E., and Kramer, D. M. (2005). Plasticity in light reactions of photosynthesis for energy production and photoprotection. J. Exp. Bot. 56, 395-406. doi: 10.1093/jxb/eri022.
11. Cruz, J. A., Sacksteder, C. A., Kanazawa, A., and Kramer, D. M. (2001). Contribution of electric field (Δψ) to steady-state transthylakoid proton motive force (pmf) in vitro and in vivo. Control of pmf parsing into Δψ and ΔpH by ionic strength. Biochemistry 40, 1226-1237. doi: 10.1021/bi0018741.
12. Cseh, Z., Rajagopal, S., Tsonev, T., Busheva, M., Papp, E., and Garab, G. (2000). Thermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity. Biochemistry 39, 15250-15257. doi: 10.1021/bi001600d.
13. Damkjaer, J. T., Kereïche, S., Johnson, M. P., Kovacs, L., Kiss, A. Z., Boekema, E. J., et al. (2009). The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in Arabidopsis.Plant Cell 21, 3245-3256. doi: 10.1105/tpc.108.064006.
14. De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J. M., Thomine, S., Gambale, F., et al. (2006). The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442, 939-942. doi: 10.1038/nature05013.
15. De Angeli, A., Moran, O., Wege, S., Filleur, S., Ephritikhine, G., Thomine, S., et al. (2009). ATP binding to the C terminus of the Arabidopsis thaliana nitrate/proton antiporter, AtCLCa, regulates nitrate transport into plant vacuoles. J. Biol. Chem. 284, 26526-26532. doi: 10.1074/jbc.M109.005132.
16. De Angeli, A., Thomine, S., Frachisse, J. M., Ephritikhine, G., Gambale, F., and Barbier-Brygoo, H. (2007). Anion channels and transporters in plant cell membranes.FEBS Lett. 581, 2367-2374. doi: 10.1016/j.febslet.2007.04.003.
17. Dutzler, R., Campbell, E. B., Cadene, M., Chait, B. T., and MacKinnon, R. (2002). X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 415, 287-294. doi: 10.1038/415287a.
18. Feng, L., Campbell, E. B., Hsiung, Y., and MacKinnon, R. (2010). Structure of a eukaryotic CLC transporter defines an intermediate state in the transport cycle.Science 330, 635-641. doi: 10.1126/science.1195230.
19. Finazzi, G., Petroutsos, D., Tomizioli, M., Flori, S., Sautron, E., Villanova, V., et al. (2015). Ions channels/transporters and chloroplast regulation. Cell Calcium 58, 86-97. doi: 10.1016/j.ceca.2014.10.002.
20. Garab, G., Kieleczawa, J., Sutherland, J. C., Bustamante, C., and Hind, C. (1991). Organization of pigment-protein complexes into macrodomains in the thylakoid membranes of wild-type and chlorophyll b-less mutant of barley as revealed by circular dichroism. Photochem. Photobiol. 54, 273-281. doi: 10.1111/j.1751-1097.1991.tb02016.x.
21. Garab, G., and van Amerongen, H. (2009). Linear dichroism and circular dichroism in photosynthesis research. Photosynth. Res. 101, 135-146. doi: 10.1007/s11120-009-9424-4.
22. Guo, W., Zuo, Z., Cheng, X., Sun, J., Li, H., Li, L., et al. (2014). The chloride channel family gene CLCd negatively regulates pathogen-associated molecular pattern (PAMP)-triggered immunity in Arabidopsis. J. Exp. Bot. 65, 1205-1215. doi: 10.1093/jxb/ert484.
23. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009). Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16, 334-342. doi: 10.1038/nsmb.1559.
24. Hind, G., Nakatani, H. Y., and Izawa, S. (1974). Light-dependent redistribution of ions in suspensions of chloroplast thylakoid membranes. Proc. Natl Acad. Sci. U.S.A. 71, 1484-1488. doi: 10.1073/pnas.71.4.1484.
25. Jentsch, T. J. (2015). Discovery of CLC transport proteins: cloning, structure, function and pathophysiology. J. Physiol. 593, 4091-4109. doi: 10.1113/jp270043.
26. Jentsch, T. J., Steinmeyer, K., and Schwarz, G. (1990). Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in Xenopus oocytes.Nature 348, 510-514. doi: 10.1038/348510a0.
27. Jossier, M., Kroniewicz, L., Dalmas, F., Le Thiec, D., Ephritikhine, G., Thomine, S., et al. (2010). The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant J. 64, 563-576. doi: 10.1111/j.1365-313X.2010.04352.x.
28. Kirchhoff, H. (2013). Architectural switches in plant thylakoid membranes.Photosynth. Res. 116, 481-487. doi: 10.1007/s11120-013-9843-0.
29. Kirchhoff, H., Hall, C., Wood, M., Herbstová, M., Tsabari, O., Nevo, R., et al. (2011). Dynamic control of protein diffusion within the granal thylakoid lumen. Proc. Natl. Acad. Sci. U.S.A. 108, 20248-20253. doi: 10.1073/pnas.1104141109.
30. Kramer, D. M., Cruz, J. A., and Kanazawa, A. (2003). Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 8, 27-32. doi: 10.1016/S1360-1385(02)00010-9.
31. Krapp, A., David, L. C., Chardin, C., Girin, T., Marmagne, A., Leprince, A. S., et al. (2014). Nitrate transport and signalling in Arabidopsis. J. Exp. Bot. 65, 789-798. doi: 10.1093/jxb/eru001.
32. Kunz, H. H., Gierth, M., Herdean, A., Satoh-Cruz, M., Kramer, D. M., Spetea, C., et al. (2014). Plastidial transporters KEA1,-2, and-3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111, 7480-7485. doi: 10.1073/pnas.1323899111.
33. Lichtenthaler, H. K., and Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. B 603, 591-592. doi: 10.1042/bst0110591.
34. Lunde, C., Jensen, P. E., Haldrup, A., Knoetzel, J., and Scheller, H. V. (2000). The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408, 613-615. doi: 10.1038/35046121.
35. Lv, Q. D., Tang, R. J., Liu, H., Gao, X. S., Li, Y. Z., Zheng, H. Q., et al. (2009). Cloning and molecular analyses of the Arabidopsis thaliana chloride channel gene family.Plant Sci. 176, 650-661. doi: 10.1016/j.plantsci.2009.02.006.
36. Marmagne, A., Vinauger-Douard, M., Monachello, D., De Longevialle, A. F., Charon, C., Allot, M., et al. (2007). 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. doi: 10.1093/jxb/erm187.
37. Monachello, D., Allot, M., Oliva, S., Krapp, A., Daniel-Vedele, F., Barbier-Brygoo, H., et al. (2009). Two anion transporters AtClCa and AtClCe fulfil interconnecting but not redundant roles in nitrate assimilation pathways. New Phytol. 183, 88-94. doi: 10.1111/j.1469-8137.2009.02837.x.
38. Nash, D., Miyao, M., and Murata, N. (1985). Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim. Biophys. Acta 807, 127-133. doi: 10.1016/0005-2728(85)90115-X.
39. Nguyen, C. T., Agorio, A., Jossier, M., Depré, S., Thomine, S., and Filleur, S. (2015). Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol. doi: 10.1093/pcp/pcv169. [Epub ahead of print].
40. Nilkens, M., Kress, E., Lambrev, P., Miloslavina, Y., Müller, M., Holzwarth, A. R., et al. (2010). Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim. Biophys. Acta 1797, 466-475. doi: 10.1016/j.bbabio.2010.01.001.
41. Pfeil, B. E., Schoefs, B., and Spetea, C. (2014). Function and evolution of channels and transporters in photosynthetic membranes. Cell Mol. Life Sci. 71, 979-998. doi: 10.1007/s00018-013-1412-3.
42. Pottosin, I., and Dobrovinskaya, O. (2015). Ion channels in native chloroplast membranes: challenges and potential for direct patch-clamp studies. Front. Physiol. 6:396. doi: 10.3389/fphys.2015.00396.
43. Pottosin, I. I., and Schönknecht, G. (1995). Patch clamp study of the voltage-dependent anion channel in the thylakoid membrane. J. Membr. Biol. 148, 143-156. doi: 10.1007/BF00207270.
44. Pottosin, I., and Shabala, S. (2015). Transport across chloroplast membranes: optimizing photosynthesis for adverse environmental conditions. Mol. Plant. doi: 10.1016/j.molp.2015.10.006. [Epub ahead of print].
45. Pribil, M., Labs, M., and Leister, D. (2014). Structure and dynamics of thylakoids in land plants. J. Exp. Bot. 65, 1955-1972. doi: 10.1093/jxb/eru090.
46. Ruban, A. V., Johnson, M. P., and Duffy, C. D. (2012). The photoprotective molecular switch in the photosystem II antenna. Biochim. Biophys. Acta 1817, 167-181. doi: 10.1016/j.bbabio.2011.04.007.
47. Schansker, G., Tóth, S. Z., and Strasser, R. J. (2005). Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim. Biophys. Acta 1706, 250-261. doi: 10.1016/j.bbabio.2004.11.006.
48. Schönknecht, G., Hedrich, R., Junge, W., and Raschke, K. (1988). A voltage-dependent chloride channel in the photosynthetic membrane of a higher-plant. Nature 336, 589-592. doi: 10.1038/336589a0.
49. Schreiber, U., and Klughammer, C. (2008). New accessory for the DUAL-PAM-100: The P515/535 module and examples of its application. PAM Appl. Notes 1, 1-10. Available online at: http://walz.com/downloads/pan/PAN07001_ed2.pdf.
50. Solymosi, K., and Bertrand, M. (2012). Soil metals, chloroplasts, and secure crop production: a review. Agron. Sustain. Dev. 32, 245-272. doi: 10.1007/s13593-011-0019-z.
51. Strasser, R. J., Srivastava, A., and Tsimilli-Michael, M. (2000). "The fluorescence transient as a tool to characterize and screen photosynthetic samples," in Probing Photosynthesis: Mechanism, Regulation and Adaptation, eds M. Yunus, U. Pathre, and P. Mohanty (London: Taylor and Francis), 445-483.
52. Strasser, R. J., Tsimilli-Michael, M., and Srivastava, A. (2004). "Analysis of the chlorophyll a fluorescence transient," in Chlorophyll a Fluorescence: A Signature of Photosynthesis, eds G. C. Papageorgiou and Govindjee (Dordrecht: Springer-Verlag), 321-362.
53. Takizawa, K., Kanazawa, A., and Kramer, D. M. (2008). Depletion of stromal Pi induces high 'energy-dependent'antenna exciton quenching (qE) by decreasing proton conductivity at CFO-CF1 ATP synthase. Plant Cell Environ. 31, 235-243. doi: 10.1111/j.1365-3040.2007.01753.x.
54. Teardo, E., Frare, E., Segalla, A., De Marco, V., Giacometti, G. M., and Szabò, I. (2005). Localization of a putative ClC chloride channel in spinach chloroplasts. FEBS Lett. 579, 4991-4996. doi: 10.1016/j.febslet.2005.08.005.
55. Tikkanen, M., Piippo, M., Suorsa, M., Sirpiö, S., Mulo, P., Vainonen, J., et al. (2006). State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol. Biol. 62, 779-793. doi: 10.1007/s11103-006-9088-9.
56. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55-60. doi: 10.1038/nature09913.
57. von der Fecht-Bartenbach, J., Bogner, M., Dynowski, M., and Ludewig, U. (2010). CLC-b-mediated NO-3/H+ exchange across the tonoplast of Arabidopsis vacuoles.Plant Cell Physiol. 51, 960-968. doi: 10.1093/pcp/pcq062.
58. von der Fecht-Bartenbach, J., Bogner, M., Krebs, M., Stierhof, Y. D., Schumacher, K., and Ludewig, U. (2007). Function of the anion transporter AtCLC-d in the trans-Golgi network. Plant J. 50, 466-474. doi: 10.1111/j.1365-313X.2007.03061.x.
59. Wege, S., Jossier, M., Filleur, S., Thomine, S., Barbier-Brygoo, H., Gambale, F., et al. (2010). The proline 160 in the selectivity filter of the Arabidopsis NO(3)(-)/H(+) exchanger AtCLCa is essential for nitrate accumulation in planta. Plant J. 63, 861-869. doi: 10.1111/j.1365-313X.2010.04288.x.
60. Yoshioka-Nishimura, M., Nanba, D., Takaki, T., Ohba, C., Tsumura, N., Morita, N., et al. (2014). Quality control of photosystem II: direct imaging of the changes in the thylakoid structure and distribution of FtsH proteases in spinach chloroplasts under light stress. Plant Cell Physiol. 55, 1255-1265. doi: 10.1093/pcp/pcu079.