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Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea

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Abstract

We evaluated the effect of TiO2 nanoparticles (NPs) on metabolic and molecular traits involved in photosynthesis of two chickpea (Cicer arietinum L.) genotypes (Sel96Th11439, cold tolerant genotype, and ILC533, cold susceptible one) during cold stress (4°C). The data analysis showed that hydrogen peroxide (H2O2) content increased more extremely under cold in susceptible plants than in tolerant ones. TiO2 NPs caused a significant decrease in H2O2 content so that tolerant plants showed lower H2O2 content than susceptible ones. This decrease often was accompanied with higher metabolic potential for photosynthesis particularly in tolerant plants. Under thermal treatments, TiO2 NPs significantly increased the activity of Rubisco compared to control plants although its activity decreased significantly under cold comparison with optimum temperature. Along with a decreasing in H2O2 content, more photosynthetic activity at the transcription levels of CaLRubisco, CaSRubisco and Cachlorophyll a/b-binding protein genes in a simultaneous manner particularly in plants treated with TiO2 NPs ensure the acclimation of plants to survival or recovery. Under such status, phosphoenolpyruvate carboxylase (PEPC) activity increased particularly in tolerant plants compared to susceptible ones as well as in plants treated with TiO2 NPs compared to control plants, indicating probably an increase in energy efficiency through different mechanisms like malate. Thus, chickpea tolerance responses to cold stress may occur after TiO2 NPs application on plants through managing the pressure of temperature decline damage and altered metabolism for plant growth.

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Abbreviations

Chl:

chlorophyll

NPs:

nanoparticles

PEPC:

phosphoenolpyruvate carboxylase

References

  1. Castiglione, M.R., Giorgetti, L., Cremonini, R., Bottega, S., and Spanò, C., Impact of TiO2 nanoparticles on Vicia narbonensis L.: potential toxicity effects, Protoplasma, 2014, vol. 251, pp. 1471–1479.

    Article  Google Scholar 

  2. Mohammadi, R., Maali-Amiri, R., and Abbasi, A., Effect of TiO2 nanoparticles on chickpea response to cold stress, Biol. Trace Elem. Res., 2013, vol. 152, pp. 403–410.

    Article  CAS  PubMed  Google Scholar 

  3. Mohammadi, R., Maali-Amiri, R., and Mantri, N., Effect of TiO2 nanoparticles on oxidative damage and antioxidant defense systems in chickpea seedlings during cold stress, Russ. J. Plant Physiol., 2014, vol. 61, pp. 768–775.

    Article  CAS  Google Scholar 

  4. Zhou, B., Sanz-Sáes, Á., Elazab, A., Shen, T., Sánchez-Bragado, R., Bort, J., Serret, M.D., and Araus, J.L., Physiological traits contributed to the recent increase in yield potential of winter wheat from Henan province, China, J. Integr. Plant Biol., 2014, vol. 56, pp. 492–504.

    Article  PubMed  Google Scholar 

  5. Parry, M.A.J., Reynolds, M., Salvucci, M.E., Raines, C., Andralojc, P.J., Zhu, X.G., Price, G.D., Condon, A.G., and Furbank, R.T., Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency, J. Exp. Bot., 2011, vol. 62, pp. 453–467.

    Article  CAS  PubMed  Google Scholar 

  6. Galmés, J., Perdomo, J.A., Flexas, J., and Whitney, S.M., Photosynthetic characterization of Rubisco transplantomic lines reveals alterations on photochemistry and mesophyll conductance, Photosynth. Res., 2013, vol. 115, pp. 153–166.

    Article  PubMed  Google Scholar 

  7. Flexas, J., Bota, J., Loreto, F., Cornic, G., and Sharkey, T., Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants, Plant Biol., 2004, vol. 6, pp. 269–279.

    Article  CAS  PubMed  Google Scholar 

  8. Kazemi-Shahandashti, S.S., Maali-Amiri, R., Zeinali, H., Khazaei, M., Talei, A., and Ramezanpour, S.S., Effect of short-term cold stress on oxidative damage and transcript accumulation of defense-related genes in chickpea seedlings, J. Plant Physiol., 2014, vol. 171, pp. 1106–1116.

    Article  CAS  PubMed  Google Scholar 

  9. Kramer, D.M. and Evans, J.R., The importance of energy balance in improving photosynthetic productivity, Plant Physiol., 2011, vol. 155, pp. 70–78.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Xuming, W., Fengqing, G., Linglan, M., Jie, L., Sitao, Y., Ping, Y., and Fashui, H., Effects of nanoanatase on ribulose-1,5-bisphosphate carboxylase/oxygenase mRNA expression in spinach, Biol. Trace Elem. Res., 2008, vol. 126, pp. 280–289.

    Article  PubMed  Google Scholar 

  11. Singh, D., Kumar, S., Singh, S.C., Lal, B., and Singh, N.B., Applications of liquid assisted pulsed laser ablation synthesized TiO2 nanoparticles on germination, growth and biochemical parameters of Brassica oleracea var. capitata, Sci. Adv. Mather., 2012, vol. 4, pp. 522–531.

    Article  CAS  Google Scholar 

  12. Ghosh, M., Bandyopadhyay, M., and Mukherjee, A., Genotoxicity of titanium dioxide (TiO2) nanoparticle at two trophic levels: plant and human lymphocytes, Chemosphere, 2010, vol. 81, pp. 1253–1262.

    Article  CAS  PubMed  Google Scholar 

  13. Lilley, R.M. and Walker, D.A., An improved spectrophotometric assay for ribulosebisphosphate carboxilase, Biochem. Biophys. Acta, 1974, vol. 385, pp. 226–229.

    Google Scholar 

  14. Sayre, R.T. and Kennedy, R.A., Photosynthetic enzyme activities and localization in Mollugo veticillata populations differing in the levels of C3 and C4 cycle operation, Plant Physiol., 1979, vol. 64, pp. 293–299.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Nazari, M.R., Habibpour F., Mehraban, F., Maali Amiri, R., and Zeinali H., Haneghah, H. Change in antioxidant responses against oxidative damage in black chickpea following cold acclimation, Russ. J. Plant Physiol., 2012, vol. 59, pp. 183–189.

    Article  CAS  Google Scholar 

  16. Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–CT method, Methods, 2001, vol. 25, pp. 402–408.

    Article  CAS  PubMed  Google Scholar 

  17. Lei, Z., Mingyu, S., Xiao, W., Chao, L., Chunxiang, Q., Liang, C., Hao, H., Xiaoqing, L., and Fashui, H., Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation, Biol. Trace Elem. Res., 2008, vol. 121, pp. 69–79.

    Article  PubMed  Google Scholar 

  18. Backhausen, J.E., Kitzmann, C., Horton, P., and Scheibe, R., Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent overreduction and competition for electrons, Photosynth. Res., 2000, vol. 64, pp. 1–13.

    Article  CAS  PubMed  Google Scholar 

  19. He, Y., Yu, C., Zhou, L., Chen, Y., Liu, A., Jin, J., Hong, J., Qi, Y., and Jiang, D., Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max) under salt stress, Plant Physiol. Biochem., 2014, vol. 74, pp. 118–124.

    Article  CAS  PubMed  Google Scholar 

  20. Flexas, J., Ribas-Carbó, V., Bota, J., Galméj M., Henkle, M., Martinez-Cañellas s., and Medrano, H., Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration, New Phytol., 2006, vol. 172, pp. 73–82.

    Article  CAS  PubMed  Google Scholar 

  21. Parry, M.A.J., Madgwick, P.J., Carvalho, J.F.C., and Andralojc, P.J., Prospects for increasing photosynthesis by overcoming the limitations of Rubisco, J. Agric. Sci., 2007, vol. 145, pp. 31–43.

    Article  CAS  Google Scholar 

  22. Parry, M.A.J., Keys, A.J., Madgwick, P.J., CarmoSilva, A.E., and Andralojc, P.J., Rubisco regulation: a role for inhibitors, J. Exp. Bot., 2008, vol. 59, pp. 1569–1580.

    Article  CAS  PubMed  Google Scholar 

  23. Gao, F., Liu, C., Qu, C., Zheng, L., Yang, F., Su, M., and Hong, F., Was improvement of spinach growth by nano-TiO2 treatment related to the changes of Rubisco activase? Biometals, 2008, vol. 21, pp. 211–217.

    Article  CAS  PubMed  Google Scholar 

  24. Suzuki, Y. and Makino, A., Translational down-regulation of RBCL is operative in the coordinated expression of Rubisco genes in senescent leaves in rice, J. Exp. Bot., 2013, vol. 64, pp. 1145–1152.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Liu, H.M., Fang, L., Che, Y.S., Wu, F.Z., and Yang, C.P., Protein expression patterns in two Spiraea species in response to cold treatment, Mol. Biol. Rep., 2014, vol. 41, pp. 4533–4547.

    Article  CAS  PubMed  Google Scholar 

  26. Hahn, M. and Walbot, V., Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves, Plant Physiol., 1989, vol. 91, pp. 930–938.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Xia, Y., Ning, Z., Bai, G., Li, R., Yan, G., Siddique, K.H., Baum, M., and Guo, P., Allelic variations of a light harvesting chlorophyll a/b-binding protein gene (Lhcb1) associated with agronomic traits in barley, PLoS One, 2012, vol. 7: e37573.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. González, M.C., Sánchez, R., and Cejudo, F.J., Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings, Planta, 2003, vol. 216, pp. 985–992.

    PubMed  Google Scholar 

  29. Ermolayev, V., Weschke, W., and Manteuffel, R., Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars, J. Exp. Bot., 2003, vol. 54, pp. 2745–2756.

    Article  CAS  PubMed  Google Scholar 

  30. Soussi, M., Lluch, C., Ocana, A., and Norero, A., Comparative study of nitrogen fixation and carbon metabolism in two chickpea (Cicer arietinum L.) cultivars under salt stress, J. Exp. Bot., 1999, vol. 50, pp. 1701–1708.

    Article  CAS  Google Scholar 

  31. Chia, D.W., Yoder, T.J., Reiter, W.D., and Gibson, S.I., Fumaric acid: an overlooked form of fixed carbon in Arabidopsis and other plant species, Planta, 2000, vol. 211, pp. 743–751.

    Article  CAS  PubMed  Google Scholar 

  32. Ryšlavá, H., Müller, K., Semorádová, Š., Synková, H., and Čeřovská, N., Photosynthesis and activity of phosphoenolpyruvate carboxylase in Nicotiana tabacum L. leaves infected by potato virus A and potato virus Y, Photosynthetica, 2003, vol. 41, pp. 357–363.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Agronomy and Plant Breeding, University College of Agriculture and Natural Resources, University of Tehran, Karaj, 31587-77871, Iran

    H. Hasanpour, R. Maali-Amir & H. Zeinali

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  1. H. Hasanpour
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  2. R. Maali-Amir
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  3. H. Zeinali
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Correspondence to R. Maali-Amir.

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Hasanpour, H., Maali-Amir, R. & Zeinali, H. Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea. Russ J Plant Physiol 62, 779–787 (2015). https://doi.org/10.1134/S1021443715060096

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  • DOI: https://doi.org/10.1134/S1021443715060096

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