Biologia plantarum 64: 447-453, 2020 | DOI: 10.32615/bp.2020.061

Leaf nutrient homeostasis and maintenance of photosynthesis integrity contribute to adaptation of the pea mutant SGECdt to cadmium

A.A. BELIMOV1,*, I.C. DODD2, V.I. SAFRONOVA1, K.-J. DIETZ3
1 All-Russia Research Institute for Agricultural Microbiology, Pushkin, 196608, Saint-Petersburg, Russia
2 Lancaster Environment Centre, Lancaster University, LA1 4YQ, Lancaster, United Kingdom
3 Biochemistry and Physiology of Plants, Bielefeld University, D-33501, Bielefeld, Germany

Cadmium (Cd) is a highly toxic and widespread soil pollutant, which negatively affects various aspects of plant growth and physiology. Here, the role of photosynthesis in response to Cd was investigated in the Cd-tolerant pea (Pisum sativum L.) mutant SGECdt. The wild type SGE and the mutant SGECdt were grown in a hydroponic solution supplemented with 1, 3, or 4 µM CdCl2 for 12 d. Root and shoot biomasses of the Cd-treated SGECdt were significantly higher than of SGE. Cadmium had little effect on the quantum yield of photosystem II (φPSII) and chlorophyll content of intact leaves of both pea genotypes. However, when leaf slices were taken from Cd-exposed plants and incubated with high Cd concentrations, the SGECdt mutant showed 1.5 - 2 times higher φPSII values than SGE, with genotypic differences maximal at 0.1 and 1 mM CdCl2. In contrast, when leaf slices were taken from plants previously unexposed to Cd, both pea genotypes exhibited similar φPSII values. Cadmium content in leaves and mesophyll protoplasts of Cd-treated SGECdt were about 2 - 3 times higher than in SGE ones. The mutant leaves and mesophyll protoplasts had also higher Ca, Mg, Mn, and Zn content. Thus, SGECdt acclimated to Cd during growth in the Cd-supplemented nutrient solution by developing a molecular mechanism related to photosynthetic integrity. A higher foliar nutrient content likely allows enhanced photosynthesis by counteracting the damage of leaves caused by Cd.

Keywords: calcium, chlorophyll, magnesium, manganese, protoplast, quantum yield of photosystem II, zinc.

Received: October 28, 2019; Revised: April 9, 2020; Accepted: April 21, 2020; Published online: June 8, 2020Show citation

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BELIMOV, A.A., DODD, I.C., SAFRONOVA, V.I., & DIETZ, K.-J. (2020). Leaf nutrient homeostasis and maintenance of photosynthesis integrity contribute to adaptation of the pea mutant SGECdt to cadmium. Biologia plantarum64, 447-453. doi: 10.32615/bp.2020.061.
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References

  1. Balakhnina, T.I., Kosobryukhov, A.A., Ivanov, A.A., Kreslavskii, V.D.: The effect of cadmium on CO2 exchange, variable fluorescence of chlorophyll, and the level of antioxidant enzymes in pea leaves. - Russ. J. Plant Physiol. 52: 15-20, 2005. Go to original source...
  2. Baryla, A., Carrier, P., Franck, F., Coulomb, C., Sahut, C., Havaux, M.: Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. - Planta 212: 696-709, 2001. Go to original source...
  3. Belimov, A.A., Dodd, I.C., Safronova, V.I., Malkov, N.V., Davies, W.J., Tikhonovich I.A.: The cadmium tolerant pea (Pisum sativum L.) mutant SGECdt is more sensitive to mercury: assessing plant water relations. - J. exp. Bot. 66: 2359-2369, 2015. Go to original source...
  4. Belimov, A.A., Malkov, N.V., Puhalsky, J.V., Safronova, V.I., Tikhonovich, I.A.: High specificity in response of pea mutant SGECdt to toxic metals: growth and element composition. - Environ. exp. Bot. 128: 91-98, 2016. Go to original source...
  5. Belimov, A.A., Malkov, N.V., Puhalsky, J.V., Tsyganov, V.E., Bodyagina, K.B., Safronova, V.I., Dietz, K.-J., Tikhonovich, I.A.: The crucial role of roots in increased Cd-tolerance and Cd-accumulation in the pea (Pisum sativum L.) mutant SGECdt. - Biol. Plant. 62: 543-550, 2018. Go to original source...
  6. Boödi, B., Oravecz, A.R., Lehoczki, E.: Effect of cadmium on organization and photoreduction of protochlorophyllide in dark-grown leaves and etioplasts of inner membrane preparations of wheat. - Photosynthetica 31: 411-420, 1995.
  7. Brand, J.J., Becker, D.W.: Evidence for direct roles of calcium in photosynthesis. - J. Bioenerg. Biomembr. 16: 239-249, 1984. Go to original source...
  8. Cakmak, I.: Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. - New Phytol. 146: 185-205, 2000. Go to original source...
  9. Chen, J., Huang, J.W.: Increased lead accumulation in a single gene mutant of pea (Pisum sativum L.). - Bull. Environ. Contam. Toxicol. 79: 25-28, 2007. Go to original source...
  10. Cho, M., Chardonnens, A.N., Dietz, K.J.: Differential heavy metal tolerance of Arabidopsis halleri and Arabidopsis thaliana: a leaf slice test. - New Phytol. 158: 287-293, 2003. Go to original source...
  11. Cobbett, C.S., May, M.J., Howden, R., Rolls, B.: The glutathione-deficient, cadmium sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. - Plant J. 16: 73-78, 1998. Go to original source...
  12. Dietz, K.-J., Schramm, M., Betz, M., Busch, H., Zink, C., Martinoia, E.: Characterization of the epidermis of barley primary leaves. 1. Isolation of epidermal protoplasts. - Planta 187: 425-430, 1992. Go to original source...
  13. Drazkiewicz, M., Tukendorf, A., Baszynski, T.: Age-dependent response of maize leaf segments to cadmium treatment: effect on chlorophyll fluorescence and phytochelatin accumulation. - J. Plant Physiol. 160: 247-254, 2003. Go to original source...
  14. Guinel, F.C., LaRue, T.A.: Excessive aluminium accumulation in pea mutant E107 (brz). - Plant Soil 157: 75-82, 1993. Go to original source...
  15. Haag-Kerwer, A., Schafer, H.J., Heiss, S., Walter, C., Rausch, T.: Cadmium exposure in Brassica juncea causes a decline in transpiration rate and leaf expansion without effect on photosynthesis. - J. exp. Bot. 50: 1827-1835, 1999.
  16. Ha, S.B., Smith, A.P., Howden, R., Dietrich, W.M., Bugg, S., O'Connell, M.J., Goldsbrough, P.B., Cobbett, C.S.: Phytohelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. - Plant Cell 11: 1153-1164, 1999. Go to original source...
  17. Hasan, S.A., Fariduddin, Q., Ali, B., Hayat, S., Ahmad, A.: Cadmium: toxicity and tolerance in plants. - J. environ. Biol. 30: 165-174, 2009.
  18. He, J.Y., Zhu, C., Ren, Y.F., Jiang, D.A., Sun, Z.X.: Root morphology and cadmium uptake kinetics of the cadmium-sensitive rice mutant. - Biol. Plant. 51: 791-794, 2007. Go to original source...
  19. Hochmal, A.K., Schulze, S., Trompelt, K., Hippler, M.: Calcium-dependent regulation of photosynthesis. - BBA Bioenergetics 1847: 993-1003, 2015.
  20. Horvath, G., Droppa, M., Oravecz, A., Raskin, V.I., Marder J.B.: Formation of the photosynthetic apparatus during greening of cadmium-poisoned barley leaves. - Planta 199: 238-243, 1996. Go to original source...
  21. Howden, R., Goldsbrough, P.B., Andersen, C.R. ,Cobbett, C.S.: Cadmium-sensitive cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. - Plant Physiol. 107: 1059-1066, 1995. Go to original source...
  22. Huang, D., Gong, X., Liu, Y., Zeng, G., Lai, C., Bashir, H., Zhou, L., Wang, D., Xu, P., Cnen, M.,Wan, J.: Effects of calcium at toxic concentrations of cadmium in plants. - Planta 245: 863-873, 2017. Go to original source...
  23. Kalstyan, A..Robertazzi,A., Knapp, E.W.: Oxygen-evolving Mn cluster in photosystem II: the protonation pattern and oxidation state in the high-resolution crystal structure. - J. amer. chem. Soc. 134: 7442-7449, 2012. Go to original source...
  24. Kevrešan S., Ćirin-Novta, V., Kuhajda, K., Kandrač, J., Petrović, N., Grbović, L., Kevrešan, Ž.: Alleviation of cadmium toxicity by naphthenate treatment. - Biol. Plant. 48: 453-455, 2004. Go to original source...
  25. Kimber, M.S., Pai, E.F.: The active site architecture of Pisum sativum beta-carbonic anhydrase is a mirror image of that of alpha-carbonic anhydrases. - EMBO J. 19: 1407-1418, 2000. Go to original source...
  26. Krupa, Z.: Cadmium against higher plant photosynthesis - a variety of effects and where do they possibly come from? - Z. Naturforsch. C. 54: 723-729, 1999. Go to original source...
  27. Krupa, Z., Baszyriski, T.: Some aspects of heavy metal toxicity towards photosynthetic apparatus - direct and indirect effects on light and dark reactions. - Acta Physiol. Plant. 17: 177-190, 1995.
  28. Krupa, Z., Oquist, G., Huner, N.P.A.: The effects of cadmium on photosynthesis of Phaseolus vulgaris - a fluorescence analysis. - Physiol. Plant. 88: 626-630, 1993. Go to original source...
  29. Küpper, H., Šetlík, I., Spiller, M., Küpper, F.C., Prášil, O.: Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. - J. Phycol. 38: 429-441, 2002. Go to original source...
  30. Lin, Y.F., Aarts, G.M.: The molecular mechanism of zinc and cadmium stress response in plants. - Cell Mol. Life Sci. 69: 3187-3206, 2012. Go to original source...
  31. Metwally, A., Safronova, V.I., Belimov, A.A., Dietz K.J.: Genotypic variation of the response to cadmium toxicity in Pisum sativum L. - J. exp. Bot. 56: 167-178, 2005.
  32. Ouzounidou, G., Moustakas, M.,Eleftheriou, E.P.: Physiological and ultrastructural effects of cadmium on wheat (Triticum aestivum L.) leaves. - Arch. Environ. Contam. Toxicol. 32: 154-160, 1997. Go to original source...
  33. Pietrini, F., Iannelli, M.A., Pasqualini S., Massacci A.: Interaction of cadmium with glutathione and photosynthesis in developing leaves and chloroplasts of Phragmites australis (Cav.) Trin. ex Steudel. - Plant Physiol. 133: 829-837, 2003. Go to original source...
  34. Sandalio, L.M., Dalurzo, H.C., Gomez, M., Romero-Puertas, M.C., Del Rio, L.A.: Cadmium-induced changes in the growth and oxidative metabolism of pea plants. - J. exp. Bot. 52: 2115-2126, 2001. Go to original source...
  35. Sanita di Toppi, L., Gabrielli, R.: Response to cadmium in higher plants. - Environ. exp. Bot. 41: 105-130, 1999. Go to original source...
  36. Schulman, R.N., Salt, D.E., Raskin, I.: Isolation and partial characterization of lead-accumulating Brassica juncea mutant. - Theor. appl. Genet. 99: 398-404, 1999. Go to original source...
  37. Shaul, O.: Magnesium transport and function in plants: the tip on the iceberg. - BioMetals 15: 309-323, 2002. Go to original source...
  38. Shen, G.M., Zhu, C., Shangguan, L.-N., Du, Q.Z.: The Cd-tolerant rice mutant cadH-5 is a high Cd accumulator and shows enhanced antioxidant activity. - J. Plant Nutr. Soil Sci. 175: 309-318, 2012. Go to original source...
  39. Siedlecka, A., Samuelsson, G., Gardeström, P., Kleczkowski, L.A., Krupa, Z.: The "activatory model" of plant response to moderate cadmium stress - relationship between carbonic anhydrase and Rubisco. - In: Garab, G. (ed.): Photosynthesis: Mechanisms and Effects. Pp. 2677-2680. Kluwer Academic Publishers, Dordrecht - Boston - London 1998.
  40. Tsyganov, V.E., Belimov, A.A., Borisov, A.Y., Safronova, V.I., Georgi, M., Dietz, K.-J., Tikhonovich, I.A.: A chemically induced new pea (Pisum sativum L.) mutant SGECdt with increased tolerance to and accumulation of cadmium. - Ann. Bot. 99: 227-237, 2007. Go to original source...
  41. Van Vliet, C., Anderson, C.R., Cobbet, C.S.: Copper-sensitive mutant of Arabidopsis thaliana. - Plant Physiol. 109: 871-878, 1995. Go to original source...
  42. Wang, Q., Yang, S., Wan, S., Li, X.: The significance of calcium in photosynthesis. - Int. J. mol. Sci. 20: 1353, 2019. Go to original source...
  43. Wang, Y., Zong, K., Jiang, L., Sun, J., Ren, Y., Sun, Z., Wen, C., Chen, X., Cao, S.: Characterization of an Arabidopsis cadmium-resistant mutant cdr3-1D reveals a link between heavy metal resistance as well as seed development and flowering. - Planta 233: 697-706, 2011. Go to original source...
  44. Watanabe, A., Ito, H., Chiba, M., Ito, A., Shimizu, H., Fuji, S., Nakamura, S., Hattori, H., Chino, M., Satoh-Nagasawa, N., Takahashi, H., Sakurai, K., Akagi, H.: Isolation of novel types of Arabidopsis mutants with altered reactions to cadmium: cadmium-gradient agar plates are an effective screen for the heavy metal-related mutants. - Planta 232: 825-836, 2010. Go to original source...
  45. Welch, R.M., LaRue, T.A.: Physiological characteristics of Fe accumulation in the 'Bronze' mutant of Pisum sativum L. cv 'Sparkle' E107 (brz brz). - Plant Physiol. 93: 723-729, 1990. Go to original source...
  46. Yruela, I.: Transition metals in plant photosynthesis. - Metallomics 5: 1090, 2013. Go to original source...
  47. Zhou, W., Qiu, B.: Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). - Plant Sci. 169: 737-745, 2005. Go to original source...