Abstract
Excessive cadmium (Cd) content in soil leads to a number of phytotoxic effects and challenges agricultural production. Aim of this study was to investigate different responses of two maize inbreds and their hybrid to an elevated Cd content in soil by measuring photosynthetic and biochemical activity and to identify a Cd tolerance mechanism. Antioxidant statusrelated parameters varied significantly between inbreds and treatments. Dry mass increased in both inbreds, but remained unchanged in hybrid. After the Cd treatment, parameters of chlorophyll a fluorescence varied between inbreds and hybrid performance was similar to inbred B84. We concluded that inbred B84 is Cd-sensitive compared to Os6-2, which did not appear to be negatively affected by Cd treatment at this growth stage studied. We suspect that due to a dilution effect in the hybrid, there was no or very weak Cd stress detected by biochemical parameters, although stress was detected by chlorophyll a fluorescence.
Similar content being viewed by others
Abbreviations
- ABS/RC:
-
absorption per active reaction centre
- APX:
-
ascorbate peroxidase
- Car:
-
carotenoids
- CAT:
-
catalase
- Chl:
-
chlorophyll
- CK:
-
control
- DIo/RC:
-
dissipation per active reaction centre
- DM:
-
dry mass
- FM:
-
fresh mass
- ET:
-
electron transport
- ETo/ABS:
-
quantum yield for electron transport
- ETo/RC:
-
electron transport per active reaction centre
- ETo/TRo :
-
efficiency/probability for electron transport
- ETo (TRo-ETo):
-
electron transport beyond xxxx
- F0 :
-
minimal fluorescence yield of the dark-adapted state
- Fm :
-
maximal fluorescence yield of the dark-adapted state
- Fv :
-
variable fluorescence
- Fv/Fm :
-
maximal quantum yield of PSII photochemistry
- Mo:
-
approximated initial slope (ms–1) of the fluorescence transient normalised on the maximal variable fluorescence Fv
- PIABS :
-
performance index (potential) for energy conservation from exciton to the reduction of intersystem electron acceptors
- POD:
-
peroxidase
- RC/ABS:
-
density of reaction centres on chlorophyll a basis
- RC/CSo :
-
density of reaction centres per excited cross section
- ROS:
-
reactive oxygen species
- Sm :
-
normalised total complementary area above the transient curve
- TBARS:
-
thiobarbituric acid-reactive substances
- tmax :
-
time (in ms) to reach the maximal fluorescence intensity Fm
- TRo/ABS:
-
maximum quantum yield for primary photochemistry
- TRo/DIo :
-
flux ratio trapping per dissipation
- TRo/RC:
-
trapping per active reaction centre
- VJ :
-
relative variable fluorescence at J step.
References
Aebi H.: Catalase in vitro. — Methods Enzymol. 105: 121–126, 1984.
Aghaz M., Bandehagh A.: Phytotoxic effects of cadmium on photosynthesis pigments in dill (Anethum graveolens). — Int. J. Farm. Alli. Sci. 2: 544–548, 2013.
Anjum S.A., Tanveer M., Hussain S. et al.: Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. — Environ. Sci. Pollut. R. 22: 17022–17030, 2015.
Asada K.: Ascorbate peroxidase. — a hydrogen peroxide-scavenging enzyme in plants. — Physiol. Plantarum 85: 235–241, 1992.
Begović L., Mlilnarić S., Antunović Dunić J. et al.: Response of Lemna minor L. to short-term cobalt exposure: The effect on photosynthetic electron transport chain and induction of oxidative damage. — Aquat. Toxicol. 175: 117–126, 2016.
Brkić I., Šimić D., Zdunić Z. et al.: Combining abilities of cornbelt inbred lines of maize for mineral content in grain. — Maydica 48: 293–297, 2003.
Burzyński M., Żurek A.: Effects of copper and cadmium on photosynthesis in cucumber cotyledons. — Photosynthetica 45: 239–244, 2007.
Cakmak I., Štrbac D., Marchner H.: Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. — J. Exp. Bot. 44: 127–132, 1993.
Chaneva G., Parvanova P., Tzvetkova N., Uzunova A.: Photosynthetic response of maize plants against cadmium and paraquat impact. — Water Air Soil Pollut. 208: 287–293, 2010.
Chaoui A., Mazhoudi S., Habib Ghorbal M., El Ferjani E.: Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). — Plant Sci. 127: 139–147, 1997.
Chaudhary S., Sharma Y.K.: Interactive studies of potassium and copper with cadmium on seed germination and early seedling growth in maize (Zea mays L.). — J. Environ. Biol. 30: 427–432, 2009.
Chien S.H., Menon R.G.: Dilution effect of plant biomass on plant cadmium concentration ad induced by application of phosphate fertilizers. — In: Rodriguez-Barrueco C. (ed.): Fertilizers and Environment. — Development in Plant and Soil Sciences. Pp. 437–442. Kluwer Academic Publishers, Dordrecht 1996.
Cho U.H., Seo N.H.: Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. — Plant Sci. 168: 113–120, 2005.
Christen D., Schönmann S., Jermini M. et al.: Characterization and early detection of grapevine (Vitis vinifera) stress responses to esca disease by in situ chlorophyll fluorescence and comparison with drought stress. — Environ. Exp. Bot. 60: 504–514, 2007.
Ci D., Jiang D., Dai T. et al.: Effects of cadmium on plant growth and physiological traits in contrast wheat recombinant inbred lines differing in cadmium tolerance. — Chemosphere 77: 1620–1625, 2009.
Da Silva A.J., Nascimento C.W.A., Gouveia-Neto A.S., da Silva-Jr E.A.: LED induced chlorophyll fluorescence spectral analysis for the early detection and monitoring of cadmium toxicity in maize plants. — Water Air Soil Pollut. 223: 3527–3533, 2012.
Das P., Samantaray S., Rout R.: Studies on cadmium toxicity in plants: a review. — Environ. Pollut. 98: 29–36, 1998.
De Gara L., Paciolla C., De Tullio M. et al.: Ascorbate-dependent hydrogen peroxide detoxification and ascorbate regeneration during germination of a highly productive maize hybrid: Evidence of an improved detoxification mechanism against reactive oxygen species. — Physiol. Plantarum 109: 7–13, 2000.
Di Cagno R., Guidi L., Stefani A., Soldatini G.F.: Effects of cadmium on growth of Heliantus annus seedlings: physiological aspects. — New Phytol. 144: 65–71, 1999.
Di Toppi L.S., Gabbrielli R.: Response to cadmium in higher plants. — Environ. Exp. Bot. 41: 105–130, 1999.
Drążkiewicz M., Tukendorf A., Baszyński 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.
Ekmekçi Y., Tanyolaç D., Ayhan B.: Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. — J. Plant Physiol. 165: 600–611, 2008
Florijn P.J., van Beusichem M.L.: Uptake and distribution of cadmium in maize inbred lines. — Plant Soil 150: 25–32, 1993.
Franić M., Sorić R., Lončarić Z. et al.: Genotype variations in maize on cadmium contaminated soil. — In: Jug I., Đurđević B. (ed.): Proceedings of 6th Conference Agriculture in Nature and Environment Protection. Pp. 113–117. Glas Slavonije d.d., Osijek 2013.
Gallego S.M., Pena L.B., Barcia R.A. et al.: Unraveling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. — Environ. Exp. Bot. 83: 33–46, 2012.
Grant C.A., Buckley W.T., Bailey L.D., Selles F.: Cadmium accumulation in crops. — Can. J. Plant Sci. 78: 1–17, 1998.
Havaux M., Strasser R.J.: Dynamics of electron transfer within and between PS II reaction center complexes indicated by the light-saturation curve of in vivo variable chlorophyll fluorescence emission. — Photosynth. Res. 31: 149–156, 1992.
Jiang H.-X., Chen L.-S., Zheng J.-G. et al.: Aluminium-induced effects on photosystem II photochemistry in citrus leaves assessed by chlorophyll a fluorescence transient. — Tree Physiol. 28: 1863–1871.
Krall J.P., Edwards G.E.: Relationship between photosystem II activity and CO2 fixation in leaves. — Physiol. Plantarum 86: 180–187, 1992.
Kalaji H.M.; Loboda T.: Photosystem II of barley seedlings under cadmium and lead stress. — Plant Soil Environ. 53: 511–516, 2007.
Kalaji H M, Oukarroum A, Alexandrov V et al.: Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. — Plant. Physiol. Bioch. 81: 16–25, 2014.
Kalaji H.M., Schansker G., Breštić M. et al.: Frequently asked questions about chlorophyll fluorescence, the sequel. — Photosynth. Res.: doi: 10.1007/s11120-016-0318-y, 2016.
Krantev A., Yordanova R., Janda T. et al.: Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. — J. Plant Physiol. 165: 920–931, 2008.
Krinsky N.: Antioxidant functions of carotenoids. — Free Radical Bio. Med. 7: 617–635, 1989.
Küpper H., Küpper F., Spiller M.: Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. — J. Exp. Bot. 47: 259–266, 1996.
Larsson E.H., Bornman J.F., Asp H.: Influence of UV-B radiation and Cd2+ on chlorophyll fluorescence, growth and nutrient content in Brassica napus. — J. Exp. Bot. 49: 1031–1039, 1998
Lee E.A., Tracy W. F.: Modern maize breeding. — In: Bennetzen J., Hake, S. (ed.): Handbook of Maize: Genetics and Genomics. Pp. 141–160. Springer, New York 2009.
Lichtenthaler H.K., Kuhn G., Prenzel U. et al.: Adaptation of chloroplast-ultrastructure and of chlorophyll-protein levels to high-light and low-light growth conditions. — Z. Naturforsch. 37: 464–475, 1982.
Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Methods Enzymol. 148: 350–382, 1987.
Mallick N., Mohn F.H.: Use of chlorophyll fluorescence in metal-stress research: a case study with green microalga Scenedesmus. — Ecotox. Environ. Safe. 55: 64–69, 2003.
Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate. — specific peroxidase in spinach chloroplasts. — Plant Cell. Physiol. 22: 867–880, 1981.
Pagliano C., Raviolo M., Dalla Vecchia F. et al.: Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). — J. Photoch. Photobio. B 84: 70–78, 2006.
Procházková D., Sairam R.K., Srivastava G.C., Singh D.V.: Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. — Plant Sci. 161: 765–771, 2001.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051-07-0, URL http://www.Rproject. org/, 2012.
Ralph P.J., Burchett M.D.: Photosynthetic response of Halophila ovalis to heavy metal stress. — Environ. Pollut. 103: 91–101, 1998.
Rodríguez-Serrano M., Romero-Puertas M.C., Pazmiño D.M. et al.: Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. — Plant Physiol. 150: 229–243, 2009.
Romero-Puertas M.C., Palm, J.M., Gómez M. et al.: Cadmium causes the oxidative modification of proteins in pea plants. — Plant Cell Environ. 25: 677–686, 2002.
Sandalio L.M., Dalurzo H.C., Gómez M. et al.: Cadmiuminduced changes in the growth and oxidative metabolism of pea plants. — J. Exp. Bot. 52: 2115–2126, 2001.
Schützendübel A., Polle A.: Plant responses to abiotic stresses: heavy metal induced oxidative stress and protection by mycorrhisation. — J. Exp. Bot. 53: 1351–1365, 2002.
Siegel B.Z., Galston A.W.: The isoperoxidases of Pisum sativum. — Plant Physiol. 42: 221–226, 1967.
Šimić D., Mladenović Drinić S., Zdunić Z. et al.: Quantitative trait loci for biofortification in maize grain. — J. Hered. 103: 47–54, 2012
Sorić R., Ledenčan T., Zdunić Z. et al.: Quantitative trait loci for metal accumulation in maize leaf. — Maydica 56: 323–329, 2011.
Sorić R., Lončarić Z., Kovačević V. et al.: A major gene for leaf cadmium accumulation in maize (Zea mays L.). — In: The Proceedings of the International Plant Nutrition Colloquium XVI. http://escholarship. org/uc/item/1q48v6cf. UC Davis, 2009.
STAR, version 2.0.1. Biometrics and Breeding Informatics, PBGB Division, International Rice Research Institute. Los Baños, Laguna 2014.
Stirbet A, Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. — J. Photoch. Photobio. B. 104: 236–257, 2011.
Strasser R.J., Srivastava A., Govindjee: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. — Photochem. Photobiol. 61: 32–42, 1995.
Strasser R.J., Srivastava A., Tsimilli-Michael M.: Analysis of chlorophyll a fluorescence transient. — In: Papageorgiou G.C., Govindjee (ed.): Advances in Photosynthesis and Respiration. Pp. 321–362. Springer, Dodrecht 2004.
Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluorescent transient as a tool to characterize and screen photosynthetic samples. — In: Yunus M., Pathre, U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445–483. Taylor and Francis, London 2000.
Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V.: Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. — Biochim. Biophys. Acta 1797: 1313–1326, 2010.
Tuba Z., Saxena D.K., Srivastava K., Kalaji M.H.: Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) biomapping. — Curr. Sci. 98: 1505–1508, 2010.
Turnau K., Anielska T., Ryszka P. et al. Establishment of arbuscular mycorrhizal plants originating from xerothermic grasslands on heavy metal rich industrial wastes. — new solution for waste revegetation. — Plant Soil 305: 267–280, 2008.
Velikova V., Yordanov I., Edreva A.: Oxidative stress and some antioxidant systems in acid-rain treated bean plants. Protective role of exogenous polyamines. — Plant Sci. 151: 59–66, 2000
Verbruggen N., Hermans C., Schat H.: Mechanisms to cope with arsenic or cadmium excess in plants. — Curr. Opin. Plant Biol. 12: 364–372, 2009.
Verma S., Dubey R.S.: Leads toxicity induces lipid peroxidation and alters the activities of antioxidant enzxmes in growing rice plants. — Plant Sci. 164: 645–655, 2003.
Weigel H.J.: Inhibition of photosynthetic reactions of isolated intact chloroplasts by cadmium. — J. Plant Physiol. 119: 179–189, 1985.
Zhang Z., Jin F., Wang C.: Differences between Pb and Cd accumulation in 19 elite maize inbred lines and application prospects. — J. Biomed. Biotechnol. 2012: 271485, 2012.
Zhou W., Qiu B.: Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). — Plant Sci. 169: 737–745, 2005.
Żurek G., Rybka K., Pogrzeba M. et al.: Chlorophyll a fluorescence in evaluation of the effect of heavy metal soil contamination on perennial grasses. — PLOS ONE 9: e91475, 2014.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: This research was funded by the Croatian Science Foundation (project No. 5707: „Genetics and physiology of multiple stress tolerance in maize“).
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Franić, M., Galić, V., Mazur, M. et al. Effects of excess cadmium in soil on JIP-test parameters, hydrogen peroxide content and antioxidant activity in two maize inbreds and their hybrid. Photosynthetica 56, 660–669 (2018). https://doi.org/10.1007/s11099-017-0710-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-017-0710-7