Distribution of Cd and other cations between the stroma and thylakoids: a quantitative approach to the search for Cd targets in chloroplasts
- 113 Downloads
Abstract
Plant growth and photosynthetic activity are usually inhibited due to the overall action of Cd on a whole organism, though few cadmium cations can invade chloroplasts in vivo. We found that in vivo, the major portion of Cd in barley chloroplasts is located in the thylakoids (80%), and the minor portion is in the stroma (20%). Therefore, the electron-transport chain in the thylakoids would be the likely target for direct Cd action in vivo. In vitro, we found the distribution of Cd to be shifted to the stroma (40–60%). In barley chloroplasts, the major portions of Mg, Fe, Mn, and Cu were found to be located in the thylakoids, and most Ca, Zn, and K in the stroma. This finding was true for both control and Cu- or Fe-treated plants. Treatment with Cd affected the contents of all cations, and the largest portions of Ca and Zn were in the thylakoids. Alterations of the K and Mn contents were caused by Cd, Cu, or Fe treatment; the levels of other cations in chloroplasts were changed specifically by Cd treatment. The quantity of Cd in chloroplasts was small in comparison to that of Mg, Ca, and Fe. In thylakoids, the amount of Cd was similar to that of Cu and comparable to the levels of Zn and Mn. Accordingly, the possible targets for direct Cd action in thylakoids are the Mn cluster, plastocyanin, carbonic anhydrase, or FtsH protease. The quantity of Cd in thylakoids is sufficient to replace a cation nearly completely at one of these sites or partially (20–30%) at many of these sites.
Keywords
Plant Cadmium Cations Chloroplast Thylakoid Stroma Cation distributionAbbreviations
- EDTA
Ethylenediaminetetraacetic acid
- Fo′
Minimal Chl fluorescence in light
- Fm′
Maximal Chl fluorescence in light
- Fs
Steady-state Chl fluorescence
- HM
Heavy metal
- Me
Metal
- NADP+
Nicotinamide adenine dinucleotide phosphate, oxidized form
- OEC
Oxygen evolving complex of PSII
- Pc
Plastocyanin
- Pm′
Maximal amplitude of P700 change in light
- PPO
Polyphenol oxidase
- PSI
Photosystem I
- PSII
Photosystem II
- SD
Standard deviation
- SE
Standard error
- SOD
Superoxide dismutase
- WT
Wild type (not mutant)
Notes
Acknowledgements
The work was supported by Grant No. 14-14-00584 from the Russian Science Foundation.
Supplementary material
References
- Aguirre G, Pilon M (2016) Copper delivery to chloroplast proteins and its regulation. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01250 Google Scholar
- Andresen E, Küpper H (2013) Cadmium toxicity in plants. In: Sigel A, Sigel H, Sigel R (eds) Cadmium: from toxicity to essentiality. Metal ions in life sciences, vol 11. Springer, Dordrecht, pp 395–413. https://doi.org/10.1007/978-94-007-5179-8_13 CrossRefGoogle Scholar
- Aravind P, Prasad MNV (2004) Carbonic anhydrase impairment in cadmium-treated Ceratophyllum demersum L. (free floating freshwater macrophyte): toxicity reversal by zinc. J Anal At Spectrom 19:52–57. https://doi.org/10.1039/B307282G CrossRefGoogle Scholar
- Baker AJM (1981) Accumulators and excluders—strategies in response of plants to heavy metals. J Plant Nutr 3:643–654. https://doi.org/10.1080/01904168109362867 CrossRefGoogle Scholar
- Banci L, Bertini I, Cabelli DE, Hallewell RA, Tung JW, Viezzoli MS (1991) A characterization of copper/zinc superoxide dismutase mutants at position 124 Zinc-deficient proteins. FEBS J 196:123–128. https://doi.org/10.1111/j.1432-1033.1991.tb15794.x Google Scholar
- Barcelo J, Vazquez MD, Poschenrieder Ch (1988) Structural and ultrastructural disorders in cadmium-treated bush bean plants (Phaseolus vulgaris L.). New Phytol 108:37–49. https://doi.org/10.1111/j.1469-8137.1988.tb00202.x CrossRefGoogle Scholar
- Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709. https://doi.org/10.1007/s004250000439 CrossRefGoogle Scholar
- Baszynski T, Wajda L, Krol M, Wolinska D, Krupa Z, Tukendorf Z (1980) Photosynthetic activities of cadmium-treated tomato plants. Physiol Plant 48:365–370. https://doi.org/10.1111/j.1399-3054.1980.tb03269.x CrossRefGoogle Scholar
- Bazzaz MB, Govindjee (1974) Effects of cadmium nitrate on spectral characteristics and light reactions of chloroplasts. Environ Lett 6:1–12CrossRefGoogle Scholar
- Bazzaz FA, Rolfe GL, Carlson RW (1974) Effect of Cd on photosynthesis and transpiration of excised leaves of corn and sunflower. Physiol Plant 32:373–376. https://doi.org/10.1111/j.1399-3054.1974.tb03154.x CrossRefGoogle Scholar
- Blaby-Haas CE, Merchant SS (2013) Metal homeostasis: sparing and salvaging metals in chloroplasts. Encycl Inorg Bioinorg Chem. https://doi.org/10.1002/9781119951438.eibc2113 Google Scholar
- Burzynski M, Klobus G (2004) Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress. Photosynthtica 42:505–510. https://doi.org/10.1007/S11099-005-0005-2 CrossRefGoogle Scholar
- Chow WS, Fan D-Y, Oguchi R, Jia H, Losciale P, Park Y-I, He J, Öquist G, Shen Y-G, Anderson JM (2012) Quantifying and monitoring functional photosystem II and the stoichiometry of the two photosystems in leaf segments: approaches and approximations. Photosynth Res 113:63–74. https://doi.org/10.1007/s11120-012-9740-y CrossRefGoogle Scholar
- Church WB, Guss JM, Potter JJ, Freeman HC (1986) The crystal structure of mercury-substituted Poplar Plastocyanin at 1.9-Å Resolution. J Biol Chem 261:234–237. http://www.jbc.org/content/261/1/234.long
- Ci D, Jiang D, Wollenweber B, Dai T, Jing Q, Cao W (2010) Cadmium stress in wheat seedlings: growth, cadmium accumulation and photosynthesis. Acta Physiol Plant 32:365–373. https://doi.org/10.1007/s11738-009-0414-0 CrossRefGoogle Scholar
- Cullen JT, Maldonado MT (2013) Biogeochemistry of cadmium and its release to the environment. In: Sigel A, Sigel H, Sigel R (eds) Cadmium: from toxicity to essentiality. Metal ions in life sciences, vol 11. Springer, Dordrecht, pp 31–62. https://doi.org/10.1007/978-94-007-5179-8_2 CrossRefGoogle Scholar
- Delperee C, Lutts S (2008) Growth inhibition occurs independently of cell mortality in tomato (Solanum lycopersicum) exposed to high cadmium concentrations. J Integr Plant Biol 50:300–310. https://doi.org/10.1111/j.1744-7909.2007.00625.x CrossRefGoogle Scholar
- Demmig B, Gimmler H (1983) Properties of the isolated intact chloroplast at cytoplasmic K+ concentrations I. Light-induced cation uptake into intact chloroplasts is driven by an electrical potential difference. Plant Physiol 73:169–174. https://doi.org/10.1104/pp.73.1.169 CrossRefGoogle Scholar
- Faller P, Kienzler K, Krieger-Liszkay A (2005) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim Biophys Acta 1706:158–164. https://doi.org/10.1016/j.bbabio.2004.10.005 CrossRefGoogle Scholar
- Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875. https://doi.org/10.1105/tpc.105.033589 CrossRefGoogle Scholar
- Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46. https://doi.org/10.1016/j.envexpbot.2012.04.006 CrossRefGoogle Scholar
- Gross EL (1993) Plastocyanin: structure and function. Photosynth Res 37:103–116. https://doi.org/10.1007/BF02187469 CrossRefGoogle Scholar
- Iglesias AA, Andreo CS (1984) Involvement of thiol groups in the activity of phosphoenolpyruvate carboxylase from maize leaves. Photosynth Res 5:215–226. https://doi.org/10.1007/BF00030021 CrossRefGoogle Scholar
- Jansson H, Hansson Ö (2008) Competitive inhibition of electron donation to photosystem 1 by metal-substituted plastocyanin. Biochim Biophys Acta 1777:1116–1121. https://doi.org/10.1016/j.bbabio.2008.03.032 CrossRefGoogle Scholar
- Jozefczak M, Bohler S, Schat H, Horemans N, Guisez Y, Remans T, Vangronsveld J, Cuypers A (2015) Both the concentration and redox state of glutathione and ascorbate influence the sensitivity of arabidopsis to cadmium. Ann Bot 116:601–612. https://doi.org/10.1093/aob/mcv075 CrossRefGoogle Scholar
- Klaus AA, Lysenko EA, Kholodova VP (2013) Maize plant growth and accumulation of photosynthetic pigments at short- and longterm exposure to cadmium. Russ J Plant Physiol 60:250–259. https://doi.org/10.1134/S1021443713020118 CrossRefGoogle Scholar
- Lee MJ, Ayaki H, Goji J, Kitamura K, Nishio H (2006) Cadmium restores in vitro splicing activity inhibited by zinc-depletion. Arch Toxicol 80:638. https://doi.org/10.1007/s00204-006-0104-2 CrossRefGoogle Scholar
- Li EH, Miles CD (1975) Effects of cadmium on photoreaction II of chloroplasts. Plant Sci Lett 5:33–40. https://doi.org/10.1016/0304-4211(75)90040-1 CrossRefGoogle Scholar
- Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1 CrossRefGoogle Scholar
- Lin Y-F, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206. https://doi.org/10.1007/s00018-012-1089-z CrossRefGoogle Scholar
- Lysenko EA, Klaus AA, Pshybytko NL, Kusnetsov VV (2015) Cadmium accumulation in chloroplasts and its impact on chloroplastic processes in barley and maize. Photosynth Res 125:291–303. https://doi.org/10.1007/s11120-014-0047-z CrossRefGoogle Scholar
- Maret W, Moulis J-M (2013) The bioinorganic chemistry of cadmium in the context of its toxicity. In: Sigel A, Sigel H, Sigel R (eds) Cadmium: from toxicity to essentiality. Metal ions in life sciences, vol 11. Springer, Dordrecht, pp 1–29. https://doi.org/10.1007/978-94-007-5179-8_1 CrossRefGoogle Scholar
- Maury WJ, Huber SC, Moreland DE (1981) Effects of magnesium on intact chloroplasts II. Cation specificity and involvement of the envelope ATPase in (sodium) potassium/proton exchange across the envelope. Plant Physiol 68:1257–1263. https://doi.org/10.1104/pp.68.6.1257 CrossRefGoogle Scholar
- Nakatani HY, Barber J, Minski MJ (1979) The influence of the thylakoid membrane surface properties on the distribution of ions in chloroplasts. Biochem Biophys Acta 545:24–35. https://doi.org/10.1016/0005-2728(79)90110-5 Google Scholar
- Nishimura K, Kato Y, Sakamoto W (2016) Chloroplast proteases: updates on proteolysis within and across suborganellar compartments. Plant Phys 171:2280–2293. https://doi.org/10.1104/pp.16.00330 Google Scholar
- Nobel PS (1969) Light-induced changes in the ionic content of chloroplasts in Pisum sativum. Biochem Biophys Acta 172:134–143. https://doi.org/10.1016/0005-2728(69)90098-X Google Scholar
- Pagliano C, Raviolo M, Dalla Vecchia F, Gabbrielli R, Gonnelli C, Rascio N, Barbato R, La Rocca N (2006) Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). J Photochem Photobiol B 84:70–78. https://doi.org/10.1016/j.jphotobiol.2006.01.012 CrossRefGoogle Scholar
- Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environ Geochem Health 32:1–12. https://doi.org/10.1007/s10653-009-9273-2 CrossRefGoogle Scholar
- Pätsikkä E, Kairavuo M, Šeršen F, Aro E-M, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367. https://doi.org/10.1104/pp.004788 CrossRefGoogle Scholar
- Pietrini F, Iannelli MA, Pasqualini S, Massacci A (2003) Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. Plant Physiol 133:829–837. https://doi.org/10.1104/pp.103.026518 CrossRefGoogle Scholar
- Pilon M, Ravet K, Tapken W (2011) The biogenesis and physiological function of chloroplast superoxide dismutases. Biochim Biophys Acta 1807:989–998. https://doi.org/10.1016/j.bbabio.2010.11.002 CrossRefGoogle Scholar
- Portis AR, Heldt HW (1976) Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of CO2 fixation. Biochim Biophys Acta 449:434–446. https://doi.org/10.1016/0005-2728(76)90154-7 CrossRefGoogle Scholar
- Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62:267–278. https://doi.org/10.1016/j.envexpbot.2007.09.002 CrossRefGoogle Scholar
- Schneider A, Steinberger I, Herdean A, Gandini C, Eisenhut M, Kurz S, Morper A, Hoecker N, Rühle T, Labs M, Flügge U-I, Geimer S, Schmidt SB, Husted S, Weber APM, Spetea C, Leister D (2016) The evolutionarily conserved protein PHOTOSYNTHESIS AFFECTED MUTANT71 is required for efficient manganese uptake at the thylakoid membrane in Arabidopsis. Plant Cell 28:892–910. https://doi.org/10.1105/tpc.15.00812 Google Scholar
- Seregin IV, Ivanov VB (2001) Physiological aspects of cadmium and lead toxic effects on higher plants. Russ J Plant Physiol 48:523–544. https://doi.org/10.1023/A:1016719901147 CrossRefGoogle Scholar
- Shi GR, Cai QS (2008) Photosynthetic and anatomic responses of peanut leaves to cadmium stress. Photosynthetica 46:627–630. https://doi.org/10.1007/s11099-008-0107-8 CrossRefGoogle Scholar
- Shikanai T, Müller-Moulé P, Munekage Y, Niyogi KK, Pilon M (2003) PAA1, a P-Type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–1346. https://doi.org/10.1105/tpc.011817 CrossRefGoogle Scholar
- Siedlecka A, Baszynski T (1993) Inhibition of electron flow around photosystem I in chloroplasts of Cd-treated maize plants is due to Cd-induced iron deficiency. Physiol Plant 87:199–202. https://doi.org/10.1111/j.1399-3054.1993.tb00142.x CrossRefGoogle Scholar
- Sigfridsson KGV, Bernat G, Mamedov F, Styring S (2004) Molecular interference of Cd2+ with Photosystem II. Biochim Biophys Acta 1659:19–31. https://doi.org/10.1016/j.bbabio.2004.07.003 CrossRefGoogle Scholar
- Solti A, Kovács K, Müller B, Vázquez S, Hamar E, Pham HD, Tóth B, Abadia J, Fodor F (2016) Does a voltage-sensitive outer envelope transport mechanism contributes to the chloroplast iron uptake? Planta 244:1303–1313. https://doi.org/10.1007/s00425-016-2586-3 CrossRefGoogle Scholar
- Tang L, Ying R-R, Jiang D, Zeng X-W, Morel J-L, Tang Y-T, Qiu R-L (2013) Impaired leaf CO2 diffusion mediates Cd-induced inhibition of photosynthesis in the Zn/Cd hyperaccumulator Picris divaricata. Plant Physiol Biochem 73:70–76. https://doi.org/10.1016/j.plaphy.2013.09.008 CrossRefGoogle Scholar
- Toth T, Zsiros O, Kis M, Garab G, Kovacs L (2012) Cadmium exerts its toxic effects on photosynthesis via a cascade mechanism in the cyanobacterium, Synechocystis PCC 6803. Plant Cell Environ 35:2075–2086. https://doi.org/10.1111/j.1365-3040.2012.02537.x CrossRefGoogle Scholar
- Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60. https://doi.org/10.1038/nature09913 CrossRefGoogle Scholar
- Wang H, Zhao SC, Liu RL, Zhou W, Jin JY (2009) Changes of photosynthetic activities of maize (Zea mays L.) seedlings in response to cadmium stress. Photosynthetica 47:277–283. https://doi.org/10.1007/s11099-009-0043-2 CrossRefGoogle Scholar
- Weigel HJ (1985) The effect of Cd2+ on photosynthetic reactions of mesophyll protoplasts. Physiol Plant 63:192–200. https://doi.org/10.1111/j.1399-3054.1985.tb01902.x CrossRefGoogle Scholar
- Whatley FR, Ordin L, Arnon DI (1951) Distribution of micronutrient metals in leaves and chloroplast fragments. Plant Physiol 26:414–418. https://doi.org/10.1104/pp.26.2.414 CrossRefGoogle Scholar
- Wu FB, Zhang GP, Yu JS (2003) Genotypic differences in effect of Cd on photosynthesis and chlorophyll fluorescence of barley (Hordeum vulgare L.). Bull Environ Contam Toxicol 71:1272–1281. https://doi.org/10.1007/s00128-003-8718-z Google Scholar
- Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM (2008) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61. https://doi.org/10.1038/nature06636 CrossRefGoogle Scholar
- Ying R-R, Qiu R-L, Tang Y-T, Hu P-J, Qiu H, Chen H-R, Shi T-H, Morel J-L (2010) Cadmium tolerance of carbon assimilation enzymes and chloroplast in Zn/Cd hyperaccumulator Picris divaricata. J Plant Phys 167:81–87. https://doi.org/10.1016/j.jplph.2009.07.005 CrossRefGoogle Scholar
- Zhu R, Sheila M, Macfie SM, Ding Z (2005) Cadmium-induced plant stress investigated by scanning electrochemical microscopy. J Exp Bot 56:2831–2838. https://doi.org/10.1093/jxb/eri275 CrossRefGoogle Scholar