Russian Journal of Plant Physiology

, Volume 66, Issue 3, pp 450–460 | Cite as

Heat Shock-Induced Salt Stress Tolerance in Lentil (Lens culinaris Medik.)

  • M. S. Hossain
  • M. Hasanuzzaman
  • A. Rahman
  • K. Nahar
  • J. A. Mahmud
  • M. FujitaEmail author


Soil salinity is a major constraint in crop production. Of the different strategies to cope with salt stress, a cross-tolerance strategy is inexpensive and easy to adopt. In this study, we investigated heat shock-induced salinity tolerance mechanism in lentil (Lens culinaris Medik cv. BARI Lentil-7). Six-day-old seedlings were exposed to 100 mM NaCl with or without 4-h heat shock (HS) (40 ± 1°C) for three days. The results showed that 100 mM NaCl reduced chlorophyll content, caused severe oxidative damage by reducing antioxidants, increased the toxic methylglyoxal (MG) content and disrupted ion homeostasis by increasing Na+ in the shoots and decreasing K+ in the roots. Heat shock pre-treatment improved the chlorophyll content and reduced oxidative damage by improving reduced ascorbate content, the GSH/GSSG ratio, catalase and ascorbate peroxidase activity under salt stress. Moreover, heat shock reduced the toxic MG content by upregulating glyoxalase system. Heat shock inhibited Na+ accumulation in the shoots and K+ efflux from the roots, as a result, the Na+/K+ ratio reduced both in the roots and shoots under salt stress. We further investigated the HS-induced changes in H2O2 and MG content. We assumed that the dynamics of H2O2 and MG at 1 h intervals during heat shock play a signaling role in activating antioxidant defense and glyoxalase pathway, as a result, plant showed tolerance to salt stress.


Lens culinaris cross-tolerance heat shock NaCl methylglyoxal H2O2 



This research was funded by the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan. We thank Mr. M.H.M. Borhannuddin Bhuyan, Ms. Khursheda Parvin and Mr. Sayed Mohammad Mohsin, Md. Shahadat Hossen, Abdul Awal Choudhury Masud, Faculty of Agriculture, Kagawa University, Japan for a critical review and editing of the manuscript. We also thank Dr. Md. Motiar Rohman, Bangladesh Agricultural Research Institute, Gazipur, Bangladesh for providing lentil seeds.


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.


  1. 1.
    Qadir, M., Tubeileh, A., Akhtar, J., Larbi, A., Minhas, P., and Khan, M., Productivity enhancement of salt-affected environments through crop diversification, Land Degrad. Dev., 2008, vol. 19, pp. 429–453.CrossRefGoogle Scholar
  2. 2.
    Horie, T., Karahara, I., and Katsuhara, M., Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants, Rice, 2012, vol. 5: 11.CrossRefGoogle Scholar
  3. 3.
    Munns, R. and Tester, M., Mechanism of salinity tolerance, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 651–681.CrossRefGoogle Scholar
  4. 4.
    Bose, J., Rodrigo-Moreno, A., and Shabala, S., ROS homeostasis in halophytes in the context of salinity stress tolerance, J. Exp. Bot., 2014, vol. 65, pp. 1241–1257.CrossRefGoogle Scholar
  5. 5.
    Gill, S.S. and Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 2010, vol. 48, pp. 909–930.CrossRefGoogle Scholar
  6. 6.
    Zhang, Y., Li, Z., Peng, Y., Wang, X., Peng, D., Li, Y., He, X., Zhang, X., Ma, X., Huang, L., and Yan, Y., Clones of FeSOD, MDHAR, DHAR genes from white clover and gene expression analysis of ROS-scavenging enzymes during abiotic stress and hormone treatments, Molecules, 2015, vol. 20, pp. 20939–20954.CrossRefGoogle Scholar
  7. 7.
    Hasanuzzaman, M., Nahar, K., Hossain, M.S., Mahmud, J.A., Rahman, A., Inafuku, M., Oku, H., and Fujita, M., Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants, Int. J. Mol. Sci., 2017, vol. 18: 200.CrossRefGoogle Scholar
  8. 8.
    Sankaranarayanan, S., Jamshed, M., and Samuel, M.A., Degradation of glyoxalase I in Brassica napus stigma leads to self-incompatibility response, Nat. Plants, 2015, vol. 1: 15185.CrossRefGoogle Scholar
  9. 9.
    Kaur, C., Kushwaha, H.R., Mustafiz, A., Pareek, A., Sopory, S.K., and Singla-Pareek, S.L., Analysis of global gene expression profile of rice in response to methylglyoxal indicates its possible role as a stress signal molecule, Front. Plant Sci., 2015, vol. 6: 682.Google Scholar
  10. 10.
    Atkinson, N.J. and Urwin, P.E., The interaction of plant biotic and abiotic stresses: from genes to field, J. Exp. Bot., 2012, vol. 63, pp. 3523–3544.CrossRefGoogle Scholar
  11. 11.
    Foyer, C.H., Rasool, B., Davey, J.W., and Hancock, R.D., Cross-tolerance to biotic and abiotic stresses in plants: a focus on resistance to aphid infestation, J. Exp. Bot., 2016, vol. 67, pp. 2025–2037.CrossRefGoogle Scholar
  12. 12.
    Hsu, Y.T. and Kao, C.H., Heat shock-mediated H2O2 accumulation and protection against Cd toxicity in rice seedlings, Plant Soil, 2007, vol. 300, pp. 137–147.CrossRefGoogle Scholar
  13. 13.
    Chao, Y.Y. and Kao, C.H., Heat shock-induced ascorbic acid accumulation in leaves increases cadmium tolerance of rice (Oryza sativa L.) seedlings, Plant Soil, 2010, vol. 336, pp. 39–48.CrossRefGoogle Scholar
  14. 14.
    Hossain, M.A., Mostofa, M.G., and Fujita, M., Heat-shock positively modulates oxidative protection of salt and drought-stressed mustard (Brassica campestris L.) seedlings, J. Plant Sci. Mol. Breed., 2013, vol. 2: 2.CrossRefGoogle Scholar
  15. 15.
    Afzal, F., Khan, T., Khan, A., Khan, S., Raza, H., Ihsan Ahanger, M.A., and Kazi, A.G., Nutrient deficiencies under stress in legumes, in Legumes under Environmental Stress: Yield, Improvement and Adaptations, Azooz, M.M. and Ahmad, P., Eds., Hoboken: Wiley, 2014, pp. 53–65.Google Scholar
  16. 16.
    Golezani, K.G. and Yengabad, F.M., Physiological responses of lentil (Lens culinaris Medik.) to salinity, Int. J. Agric. Crop Sci., 2012, vol. 4, pp. 1531–1535.Google Scholar
  17. 17.
    Hossain, M.S., Alam, M.U., Rahman, A., Hasanuzzaman, M., Nahar, K., Al Mahmud, J., and Fujita, M., Use of iso-osmotic solution to understand salt stress responses in lentil (Lens culinaris Medik.), S. Afr. J. Bot., 2017, vol. 113, pp. 346–354.CrossRefGoogle Scholar
  18. 18.
    Arnon, D.T., Copper enzymes in isolated chloroplasts polyphenol oxidase in Beta vulgaris, Plant Physiol., 1949, vol. 24, pp. 1–15.CrossRefGoogle Scholar
  19. 19.
    Bates, L.S., Waldren, R.P., and Teari, D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, pp. 205–207.CrossRefGoogle Scholar
  20. 20.
    Heath, R.L. and Packer, L., Photo peroxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation, Arch. Biochem. Biophys., 1968, vol. 125, pp. 189–198.CrossRefGoogle Scholar
  21. 21.
    Yu, C.W., Murphy, T.M., and Lin, C.H., Hydrogen peroxide-induces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation, Funct. Plant Biol., 2003, vol. 30, pp. 955–963.CrossRefGoogle Scholar
  22. 22.
    Nahar, K., Hasanuzzaman, M., Rahman, A., Alam, M.M., Mahmud, J.A., Suzuki, T., and Fujita, M., Polyamines confer salt tolerance in mung bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems, Front. Plant Sci., 2016, vol. 7: 1104.CrossRefGoogle Scholar
  23. 23.
    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
  24. 24.
    Santos, C.V., Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves, Sci. Hortic., 2004, vol. 103, pp. 93–99.CrossRefGoogle Scholar
  25. 25.
    Nahar, K., Hasanuzzaman, M., and Fujita, M., Roles of osmolytes in plant adaptation to drought and salinity, in Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies, Iqbal, N., Nazar, R.A., and Khan, N., Eds., New Delhi: Springer, 2016, pp. 37–68.Google Scholar
  26. 26.
    Li, Z.G., Duan, X.Q., Min, X., and Zhou, Z.H., Methylglyoxal as a novel signal molecule induces the salt tolerance of wheat by regulating the glyoxalase system, the antioxidant system, and osmolytes, Protoplasma, 2017, vol. 9, pp. 1–12.Google Scholar
  27. 27.
    Chao, Y.Y., Hsu, Y.T., and Kao, C.H., Involvement of glutathione in heat shock- and hydrogen peroxide-induced cadmium tolerance of rice (Oryza sativa L.) seedlings, Plant Soil, 2009, vol. 318: 37.CrossRefGoogle Scholar
  28. 28.
    Shabala, S. and Pottosin, I., Regulation of potassium transport in plants under hostile conditions: implication for abiotic and biotic stress tolerance, Physiol. Plant., 2014, vol. 151, pp. 257–279.CrossRefGoogle Scholar
  29. 29.
    Anschütz, U., Becker, D., and Shabala, S., Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment, J. Plant Physiol., 2014, vol. 171, pp. 670–687.Google Scholar
  30. 30.
    Demidchik, V., Straltsova, D., Medvedev, S.S., Pozhvanov, G.A., Sokolik, A., and Yurin, V., Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment, J. Exp. Bot., 2014, vol. 65, pp. 1259–1270.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • M. S. Hossain
    • 1
  • M. Hasanuzzaman
    • 2
  • A. Rahman
    • 2
  • K. Nahar
    • 3
  • J. A. Mahmud
    • 4
  • M. Fujita
    • 1
    Email author
  1. 1.Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa UniversityMiki-choJapan
  2. 2.Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural UniversityDhakaBangladesh
  3. 3.Department of Agricultural Botany, Faculty of Agriculture, Sher-e-Bangla Agricultural UniversityDhakaBangladesh
  4. 4.Department of Agroforestry and Environmental Science, Faculty of Agriculture, Sher-e-Bangla Agricultural UniversityDhakaBangladesh

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