Russian Journal of Plant Physiology

, Volume 66, Issue 4, pp 597–608 | Cite as

Combined Treatment with Cadmium and Zinc Enhances Lateral Root Development by Regulating Auxin Redistribution and Cell-Cycle Gene Expression in Rice Seedlings

  • F. Y. Zhao
  • X. L. HanEmail author
  • S. Y. Zhang


Enhanced lateral root (LR) development is of critical importance for rice plants adapting to heavy-metal-stress conditions. LR development is affected by heavy metals, such as aluminium (Al), copper (Cu), lead (Pb), zinc (Zn), chromium (Cr) and cadmium (Cd), or metals in combination, such as Cd and As. However, it has not been reported yet whether the combination of Cd and Zn affect LR growth in rice. Here, we studied the associations between LR growth, auxin signaling, and the cell cycle in the combination of Cd and Zn-treated rice (Oryza sativa L. cv. Zhonghua no. 11). Combined treatment with Cd and Zn significantly enhances LR development in rice seedlings. Cd levels decreased and Zn levels increased in the lateral root development regions (LRDRs) with the treatment of (Cd + Zn) compared to the treatment of Cd alone. Zn counteracted over-accumulation of auxin caused by Cd- and (Cd + Zn)-treatment significantly promoted LR growth by maintaining appropriate auxin distribution in the roots. Experiments using TIBA (2,3,5‑triiodobenzoic acid, an inhibitor of polar auxin transport), BFA (brefeldin A, a protein transport inhibitor), IBA (indole-3-butyric acid), MG132 (a protein degradation inhibitor) and DR5-GUS staining revealed that (Cd + Zn)-treatment influences the distribution of auxin through polar auxin transport and protein transport/degradation pathways. By evaluating expression levels of some key auxin-signaling genes and cell-cycle-related genes in roots treated with (Cd + Zn) or Cd alone, we found that (Cd + Zn)-treatment affects specific genes involved in auxin signaling and the cell cycle compared with Cd alone, and the treatment duration of 7 and 9 days showed different regulated manner. Our findings should help to elucidate how the effects of (Cd + Zn)-treatment on auxin signaling and the cell cycle influence LR growth.


Oryza sativa auxin redistribution auxin signaling combined cadmium and zinc cell cycle 



This work was financially supported by the National Natural Science Foundation of China (project no. 30671126), the National Natural Science Foundation of Shandong province (project no. ZR2015CL009). We are grateful to Dr. Xu for kindly help in HPLC analysis.


The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Supplementary material

11183_2019_8065_MOESM1_ESM.pdf (257 kb)


  1. 1.
    Ronzan, M., Piacentini, D., and Fattorini, L., Della Rovere, F., Eiche, E., Riemann, M., Altamura, M.M., and Falasca, G., Cadmium and arsenic affect root development in Oryza sativa L. negatively interacting with auxin, Environ. Exp. Bot., 2018, vol. 151, pp. 64–75.CrossRefGoogle Scholar
  2. 2.
    Bokor, B., Vaculík, M., Slováková, L., Masarovič, D., and Lux, A., Silicon does not always mitigate zinc toxicity in maize, Acta Physiol. Plant., 2014, vol. 36, pp. 733–743.CrossRefGoogle Scholar
  3. 3.
    Wang, Y., Wang, X., Wang, C., Peng, F., Wang, R., Xiao, X., Zeng, J., Kang, H., Fan, X., Sha, L., Zhang, H., and Zhou, Y., Transcriptomic profiles reveal the interactions of Cd/Zn in dwarf polish wheat (Triticum polonicum L.) roots, Front. Physiol., 2017, vol. 8: 168.Google Scholar
  4. 4.
    Lee, S., Kim, Y.Y., Lee, Y., and An, G., Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein, Plant Physiol., 2007, vol. 145, pp. 831–842.CrossRefGoogle Scholar
  5. 5.
    Ishimaru, Y., Suzuki, M., Kobayashi, T., Takahashi, M., Nakanishi, H., Mori, S., and Nishizawa, N.K., OsZIP4, a novel zinc-regulated zinc transporter in rice, J. Exp. Bot., 2005, vol. 56, pp. 3207–3214.CrossRefGoogle Scholar
  6. 6.
    Sun, J., Xu, Y., Ye, S., Jiang, H., Chen, Q., Liu, F., Zhou, W., Chen, R., Li, X., Tietz, O., Wu, X., Cohen, J.D., Palme, K., and Li, C., Arabidopsis ASA1Is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation, Plant Cell, 2009, vol. 21, pp. 1495–1511.CrossRefGoogle Scholar
  7. 7.
    Yang, Z.Y., Chen, F.H., Yuan, J.G., Zheng, Z.W., and Wong, M.H., Responses of Sesbania rostrata and S. cannabina to Pb, Zn, Cu and Cd toxicities, J. Environ. Sci. (China), 2004, vol. 16, pp. 670–673.Google Scholar
  8. 8.
    Potters, G., Pasternak, T.P., Guisez, Y., Palme, K.J., and Jansen, M.A.K., Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci., 2007, vol. 12, pp. 98–105.CrossRefGoogle Scholar
  9. 9.
    Sofo, A., Vitti, A., Nuzzaci, M., Tataranni, G., Scopa, A., Vangronsveld, J., Remans, T., Falasca, G., Altamura, M.M., Degola, F., and Toppi, L.S., Correlation between hormonal homeostasis and morphogenic responses in Arabidopsis thaliana seedlings growing in a Cd/Cu/Zn multi-pollution context, Physiol. Plant., 2013, vol. 149, pp. 487–498.CrossRefGoogle Scholar
  10. 10.
    Doncheva, S., Amenós, M., Poschenrieder, C., and Barceló, J., Root cell patterning: a primary target for aluminium toxicity in maize, J. Exp. Bot., 2005, vol. 56, pp. 1213–1220.CrossRefGoogle Scholar
  11. 11.
    Lequeux, H., Hermans, C., Lutts, S., and Verbruggen, N., Response to copper excess in Arabidopsis thaliana: impact on the root system architecture, hormone distribution, lignin accumulation and mineral profile, Plant Physiol. Biochem., 2010, vol. 48, pp. 673–682.CrossRefGoogle Scholar
  12. 12.
    Péret, B., Rybel, B.D., Casimiro, I., Benková, E., Swarup, R., Laplaze, L., Beeckman, T., and Bennett, M.J., Arabidopsis lateral root development: an emerging story, Trends Plant Sci., 2009, vol. 14, pp. 1–10.Google Scholar
  13. 13.
    Liu, Q., Zhou, G.Q., Xu, F., Yan, X.L., Liao, H., and Wang, J.X., The involvement of auxin in root architecture plasticity in Arabidopsis induced by heterogeneous phosphorus availability, Biol. Plant., 2013, vol. 57, pp. 739–748.CrossRefGoogle Scholar
  14. 14.
    Sreevidya, V.S., Hernandez-Oane, R.J., Gyaneshwar, P., Lara-Flores, M., Ladha, J.K., and Reddy, P.M., Changes in auxin distribution patterns during lateral root development in rice, Plant Sci., 2010, vol. 178, pp. 531–538.CrossRefGoogle Scholar
  15. 15.
    Sun, P., Tian, Q.Y., Chen, J., and Zhang, W.H., Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin, J. Exp. Bot., 2010, vol. 61, pp. 347–356.CrossRefGoogle Scholar
  16. 16.
    De Veylder, L., Engler, J.A., Burssens, S., Manevski, A., Lescure, B., Montagu, M.V., Engler, G., and Inzé, D., A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation, Planta, 1999, vol. 208, pp. 453–462.CrossRefGoogle Scholar
  17. 17.
    Stals, H. and Inzé, D., When plant cells decide to divide, Trends Plant Sci., 2001, vol. 6, pp. 359–364.CrossRefGoogle Scholar
  18. 18.
    Bücker-Neto, L., Paiva, A.L.S., Machado, R.D., Arenhart, R.A., and Margis-Pinheiro, M., Interactions between plant hormones and heavy metals responses, Genet. Mol. Biol., 2017, vol. 40, pp. 373–386.Google Scholar
  19. 19.
    Fattorini, L., Ronzan, M., Piacentini, D., Della Rovere, F., De Virgilio, C., Sofo, A., Altamura, M.M., and Falasca, G., Cadmium and arsenic affect quiescent centre formation and maintenance in Arabidopsis thaliana post-embryonic roots disrupting auxin biosynthesis and transport, Environ. Exp. Bot., 2017, vol. 144, pp. 37–48.CrossRefGoogle Scholar
  20. 20.
    Cherif, J., Mediouni, C., Ben Ammar, W., and Jemal, F., Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solanum lycopersicum), J. Environ. Sci. (China), 2011, vol. 23, pp. 837–844.CrossRefGoogle Scholar
  21. 21.
    Zhao, F.Y., Han, M.M., Zhang, S.Y., Ren, J., Hu, F., and Wang, X., MAPKs as a cross point in H2O2 and auxin signaling under combined cadmium and zinc stress in rice roots, Russ. J. Plant Physiol., 2014, vol. 61, pp. 608–618.CrossRefGoogle Scholar
  22. 22.
    Zhao, F.Y., Han, M.M., Zhang, S.Y., Wang, K., Zhang, C.R., Liu, T., and Liu, W., Hydrogen peroxide-mediated growth of the root system occurs via auxin signaling modification and variations in the expression of cell-cycle genes in rice seedlings exposed to cadmium stress, J. Integr. Plant Biol., 2012, vol. 54, pp. 991–1006.CrossRefGoogle Scholar
  23. 23.
    Sofo, A., Scopa, A., Manfra, M., De Nisco, M., Tenore, G., Troisi, J., Di Fiori, R., and Novellino, E., Trichoderma harzianum strain T-22 induces changes in phytohormone levels in cherry rootstocks (Prunus ce-rasus × P. canescens), Plant Growth Regul., 2011, vol. 65, pp. 421–425.CrossRefGoogle Scholar
  24. 24.
    Rock, C.D. and Sun, X., Crosstalk between ABA and auxin signaling pathways in roots of Arabidopsis thaliana (L.) Heynh., Planta, 2005, vol. 222, pp. 98–106.CrossRefGoogle Scholar
  25. 25.
    Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.CrossRefGoogle Scholar
  26. 26.
    Lux, A., Martinka, M., Vaculik, M., and White, P.J., Root responses to cadmium in the rhizosphere: a review, J. Exp. Bot., 2011, vol. 62, pp. 21–37.CrossRefGoogle Scholar
  27. 27.
    Guo, J., Song, J., Wang, F., and Zhang, X.S., Genome-wide identification and expression analysis of rice cell cycle genes, Plant Mol. Biol., 2007, vol. 64, pp. 349–360.CrossRefGoogle Scholar
  28. 28.
    Liedschulte, V., Laparra, H., Battey, J.N., Schwaar, J.D., Broye, H., Mark, R., Klein, M., Goepfert, S., and Bovet, L., Impairing both HMA4 homeologs is required for cadmium reduction in tobacco, Plant Cell Environ., 2017, vol. 40, pp. 364–377.CrossRefGoogle Scholar
  29. 29.
    Sharma, S.S. and Dietz, K.-J., The relationship between metal toxicity and cellular redox imbalance, Trends Plant Sci., 2009, vol. 14, pp. 43–50.CrossRefGoogle Scholar
  30. 30.
    Kim, Y.H., Khan, A.L., Kim, D.H., Lee, S.Y., Kim, K.M., Waqas, M., Jung, H.Y., Shin, J.H., Kim, J.G., and Lee, I.J., Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones, BMC Plant Biol., 2014, vol. 14: 13.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.College of Life Sciences, Shandong University of TechnologyZiboChina
  2. 2.Shandong Rice Research InstituteJiningChina

Personalised recommendations