biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 59:537-546, 2015 | DOI: 10.1007/s10535-015-0518-x

Effects of heat shock and salinity on barley growth and stress-related gene transcription

M. Faralli1, C. Lektemur2, D. Rosellini3, F. Gürel1,*
1 Department of Crop and Environment Sciences, Harper Adams University, Newport, UK
2 Department of Molecular Biology and Genetics, Faculty of Science, Istanbul University, Istanbul, Turkey
3 Department of Agricultural, Food and Environmental Sciences, University of Perugia, Perugia, Italy

The effects of a short (30 min) heat shock (HS) on plants subsequently grown under a salinity stress (SS, 200 mM NaCl) for 10 d were investigated in barley (Hordeum vulgare L.) cv. Tokak 157/37. The maximum temperature for HS allowing plant survival was 45 °C. The root length was significantly decreased by SS, whereas HS alone did not affect root growth. Interestingly, HS stimulated root elongation under SS. An osmotic adjustment was promoted in leaves by SS. On the contrary, HS increased the osmotic potential in leaves in the absence of SS, and partly counteracted the effect of SS in the HS+SS treatment. Cu/Zn-SOD, HvAPX, HvCAT2, HSP17, HSP18, and HSP90 were transcribed in leaves of HS-treated plants, but not in control plants. The HSP70 was constitutively transcribed in both the SS and control plants, but after HS, a shorter amplicon was also observed. The genes coding antioxidants, Cu/Zn-SOD, HvCAT2 and HvAPX, were differentially influenced by SS or HS+SS in the roots and leaves. In the roots, the mRNA content of BAS1, HvDRF1, HvMT2, and HvNHX1 increased after the HS treatment. In a recovery experiment in which plants were grown to maturity after HS and HS+SS stress exposure, the plant height increased and the time to maturity was reduced in comparison with SS. Our results show that HS could stimulate plant growth and reduce some of the negative effects of SS, and that it affected the transcription of several stress-related genes.

Keywords: antioxidants; Hordeum vulgare; osmotic adjustment; RT-qPCR; RWC
Subjects: temperature - high; heat shock; salinity; electrolyte leakage; relative water content; osmotic potential; gene expression; barley

Received: September 2, 2014; Revised: February 15, 2015; Accepted: February 16, 2015; Published: September 1, 2015  Show citation

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Faralli, M., Lektemur, C., Rosellini, D., & Gürel, F. (2015). Effects of heat shock and salinity on barley growth and stress-related gene transcription. Biologia plantarum59(3), 537-546. doi: 10.1007/s10535-015-0518-x
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References

  1. Acar, O., Türkan, I., Özdemir, F.: Superoxide dismutase and peroxidase activities in drought sensitive and resistant barley (Hordeum vulgare L.) varieties. - Acta Physiol. Plant. 23: 351-356, 2001. Go to original source...
  2. Almeselmani, M., Deshmukh, P.S., Sairam, R.K., Kushwaha, S.R., Singh, T.P.: Protective role of antioxidant enzymes under high temperature stress. - Plant Sci. 171: 382-388, 2006. Go to original source...
  3. Alscher, R.G., Erturk, N., Heat, L.S.: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. - J. exp. Bot. 53: 1331-1334, 2002. Go to original source...
  4. Arora, R., Pitchay, D.S., Bearce, B.C.: Water-stress-induced heat tolerance in geranium leaf tissues: a possible linkage through stress proteins? - Physiol. Plant. 103: 24-34, 1998. Go to original source...
  5. Babu, N.R., Devraj, V.R.: High temperature and salt stress response in French bean (Phaseolus vulgaris). - Aust. J. Crop. Sci. 2: 40-48, 2008.
  6. Bagatta, M., Pacifico D., Mandolino, G.: Evaluation of the osmotic adjustment response within the genus Beta. - J. Sugar Beet Res. 45: 119-133, 2008. Go to original source...
  7. Barrs, H.D., Weatherley, P.E.: A re-examination of the relative turgidity technique for estimation water deficit in leaves. - Aust. J. biol. Sci. 15: 413-428, 1962. Go to original source...
  8. Bassil, E., Coku, A., Blumwald, E.: Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. - J. exp. Bot. 63: 5727-5740, 2012. Go to original source...
  9. Borisova, T.A., Bugaje, S.M., Meshkova, N.V., Vlasov, P.V.: Heat shock increases the tolerance of plants to UV-B radiation: 1. Growth, development, and water supply to tissues. - Russ. J. Plant Physiol. 48: 507-513, 2001. Go to original source...
  10. Boston, R.S., Viitanen, P.V., Vierling, E.: Molecular chaperones and protein folding in plants. - Plant mol. Biol. 32: 191-222, 1996. Go to original source...
  11. Bowler, C., Fluhr, R.: The role of calcium and activated oxygen as signals for controlling cross-tolerance. - Trends Plant. Sci. 5: 241-246, 2000. Go to original source...
  12. Chen, W., Chao, G., Singh, K.B.: The promoter of a H2O2- inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. - Plant. J. 10: 955-966, 1996. Go to original source...
  13. Cramer, G.R.: Differential effects of salinity on leaf elongation kinetics of three grass species. - Plant Soil 253: 233-244, 2003. Go to original source...
  14. Delane, R., Greenway, H., Munns, R., Gibbs, J.: Ion concentration and carbohydrate status of the elongating leaf tissue of Hordeum vulgare growing at high external NaCl. I. Relationship between solute concentration and growth. - J. exp. Bot. 33: 557-573, 1982. Go to original source...
  15. Fedina, I.S., Nedeva, D., Çiçek, N.: Pre-treatment with H2O2 induces salt tolerance in barley seedlings. - Biol. Plant. 53: 321-24, 2009. Go to original source...
  16. Fricke, W., Akhiyarova, G., Wei, W., Alexandersson, E., Miller, A., Kjellbom, P.O., Richardson, A., Wojciechowski, T., Schreiber, L., Veselov, D., Kudoyarova, G., Volkov., V.: The short-term growth response to salt of the developing barley leaf. - J. exp. Bot. 57: 1079-1095, 2006. Go to original source...
  17. Fricke, W., Peters, W.S.: The biophysics of leaf growth in salt-stressed barley. A study at the cell level. - Plant Physiol. 129: 374-88, 2002. Go to original source...
  18. Gechev, T.S., Hille, J.: Hydrogen peroxide as a signal controlling plant programmed cell death. - J. cell. Biol. 168: 17-20, 2005. Go to original source...
  19. Griffin, J.J., Ranney, T.G., Pharr, D.M.: Heat and drought influence photosynthesis, water relation and soluble carbohydrates of two ecotype of redbud (Cercis canadensis). - J. amer. Soc. hort. Sci. 129: 497-502, 2004. Go to original source...
  20. Guo, P., Baum, M., Grando, S., Ceccarelli, S., Bai, G., Li, R., Von Korff, M., Varshney, R.K., Graner, A., Valkoun, J.: Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. - J. exp. Bot. 60: 3531-3544, 2009. Go to original source...
  21. Harrington, H.M., Alm, D.M.: Interaction of heat and salt shock in cultured tobacco cells. - Plant Physiol. 88: 618-625, 1988. Go to original source...
  22. Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R., Fujita, M.: Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. - Int. J. mol. Sci. 14: 9643-9684, 2013. Go to original source...
  23. Hopf, N., Plesofsky-Vig, N., Brambl, R.: The heat shock response of pollen and other tissues of maize. - Plant mol. Biol. 19: 623-630, 1992. Go to original source...
  24. Jia, W., Wand, Y., Zhang, S., Zhang, J.: Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. - J. exp. Bot. 378: 2201-2206, 2002. Go to original source...
  25. Jiang, Q., Hu, Z., Zhang, H., Ma, Y.: Overexpression of GmDREB1 improves salt tolerance in transgenic wheat and leaf protein response to high salinity. - Crop J. 2: 120-131, 2014. Go to original source...
  26. Jiang, Y., Huang, B.: Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. - J. exp. Bot. 52: 341-9, 2001. Go to original source...
  27. Koh, M., Kim, H.J.: The effect of metallothionein on the activity of enzymes involved in removal of reactive oxygen species. - Bull. korean chem. Soc. 22: 362-366, 2001.
  28. Kruse, E., Liu, Z., Kloppstech, K.: Expression of heat shock proteins during development of barley. - Plant mol. Biol. 23: 111-122, 1993. Go to original source...
  29. Lafuente, M.T., Belver, A., Guye, M.G., Saltveit, M.E.: Effect of temperature conditioning on chilling injury of cucumber cotyledons. - Plant Physiol. 95: 443-449, 1991. Go to original source...
  30. Lewis, J.G., Learmonth, R.P., Watson, K.: Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. - Microbiology 141: 687-694, 1995. Go to original source...
  31. Ma, L. J., Yu, C. M., Li, X. M., Li, Y. Y., Wang, L. L., Ma, C. Y., Tao, S. Y., Bu, N.: Pretreatment with NaCl induces tolerance of rice seedlings to subsequent Cd or Cd + NaCl stress. - Biol. Plant. 57: 567-570, 2013. Go to original source...
  32. Maestri, E., Klueva, N., Perrotta, C., Gulli, M., Nguyen, H.T., Marmiroli, N.: Molecular genetics of heat tolerance and heat shock proteins in cereals. - Plant mol. Biol. 48: 667-681, 2002. Go to original source...
  33. Miller, G., Suzuki, N., Ciftci-Ylmaz, S., Mittler, R.: Reactive oxygen species homeostasis and signalling during drought and salinity stresses. - Plant Cell Environ. 33: 453-467, 2010. Go to original source...
  34. Mirouze, M., Paszkowski, J.: Epigenetic contribution to stress adaptation in plants. - Curr. Opin. Plant Biol. 14: 267-274, 2011. Go to original source...
  35. Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K.: AP2/ERF family transcription factors in plant abiotic stress responses. - Biochim. biophys. Acta 1819: 86-96, 2012. Go to original source...
  36. Munns, R.: Comparative physiology of salt and water stress. - Plant Cell Environ. 25: 239-250, 2002. Go to original source...
  37. Munns, R., Passioura, J.B., Guo, J., Chazen, O., Cramer, G.R.: Water relations and leaf expansion: importance of time scale. - J. exp. Bot. 51: 1495-1504, 2000. Go to original source...
  38. Munns, R., Tester, M.: Mechanisms of salinity tolerance. - Annu. Rev. Plant Biol. 59:651-81, 2008. Go to original source...
  39. Natarajan, S., Kuehny, J.S.: Morphological, physiological, and anatomical characteristics associated with heat preconditioning and heat tolerance in Salvia splendens. - J. amer. Soc. hort. Sci. 133: 527-534, 2008. Go to original source...
  40. Ogawa, K., Kanematsu, S., Asada, K.: Intra- and extra-cellular localization of "cytosolic" CuZn superoxide dismutase in spinach leaf and hypocotyl. - Plant Cell Physiol. 37: 790-799, 1996. Go to original source...
  41. Öztürk, Z.N., Talame, V., Deyholos, M., Michalowski, C.B., Galbrait, W., Gözükirmizi, N., Tuberosa, R., Bohnert, H.J.: Monitoning large-scale changes in transcript abundance in drought and salt-stressed barley. - Plant mol. Biol. 48: 551-573, 2002. Go to original source...
  42. Passioura, J.B., Munns, R.: Rapid environmental changes that affect leaf water status induce transient surges or pauses in leaf expansion rate. - Aust. J. Plant Physiol. 7: 941-948, 2000. Go to original source...
  43. Patel, D., Franklin, K.A.: Temperature-regulation of plant architecture. - Plant Signal. Behav. 4: 577-579, 2009. Go to original source...
  44. Petrov, V.D., Van Breusegem, F.: Hydrogen peroxide - a central hub for information flow in plant cell. - AoB Plants 2012: pls014, 2012. Go to original source...
  45. Pitman, M.G., Lauchli, A.: Global impact of salinity and agricultural ecosystems. - In: Lauchli A, Luttge U. (ed.): Salinity: Environment-Plants-Molecules. Pp. 3-20. Kluwer Academic Press, Dordrecht 2002. Go to original source...
  46. Rollins, J.A., Habte, E., Templer, S.E., Colby, T., Schmidt, J., Von Korff, M.: Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). - J. exp. Bot. 64: 3201-3212, 2013. Go to original source...
  47. Roslyakova, T.V., Molchan, O.V., Vasekina, A.V., Lazareva, E.M., Sokolik, A.I., Yurin, V.M., De Boer, A.H., Babakov, A.V.: Salt tolerance of barley: relations between expression of isoforms of vacuolar Na+/H+-antiporter and 22Na+ accumulation. - Russ. J. Plant Physiol. 58: 24-35, 2011. Go to original source...
  48. Scafaro, A.P., Haynes, P.A., Atwell, B.J.: Physiological and molecular changes in Oryza meridionalis Ng., a heattolerant species of wild rice. - J. exp. Bot. 61: 191-202, 2010. Go to original source...
  49. Scandalios, J.G., Guan, L., Polidoros, A.N.: Catalases in plants: gene structure, properties, regulation and expression. - In: Scandalios, J.G. (ed.): Oxidative Stress and the Molecular Biology of Antioxidant Defenses. Pp. 343-406. Cold Spring Harbor Laboratory Press, New York 1997.
  50. Senthil-Kumar, M., Srikanthbabu, V., Mohanraju, B., Kumar, G., Shivaprakash, N., Udayakumar, M.: Screening of inbred lines to develop a thermotolerant sunflower hybrid using the temperature induction response (TIR) technique: a novel approach by exploiting residual variability. - J. exp. Bot. 54: 2569-2578, 2003. Go to original source...
  51. Serrano, R., Mulet, J.M., Rios, G., Marquez, J.A., De Larrinoa, I.F., Leube, M.P., Mendizabal, I, Pascual-Ahuir, A., Proft, M., Ros, R., Montesinos, C.: A glimpse of the mechanisms of ion homeostasis during salt stress. - J. exp. Bot. 50: 1023-1036, 1999. Go to original source...
  52. Shinozaki, K., Yamaguchi-Shinozaki, K.: Molecular responses to dehydration and low temperature: differences and crosstalk between two stress signalling pathways. - Curr. Opin. Plant Biol. 3: 217-223, 2000. Go to original source...
  53. Süle, A., Vanrobaeys, F., Hajòs, G., Van Beeumen, J., Devreese, B.: Proteomic analysis of small heat shock protein isoforms in barley shoots. - Phytochemistry 65: 1853-1863, 2004. Go to original source...
  54. Tan, W., Meng, Q.W., Brestic, M., Olsovska, K., Yang, X.: Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. - J. Plant Physiol. 168: 2063-2071, 2011. Go to original source...
  55. Tsaftaris, A.S., Bosabalidis, A.M., Scandalios, J.G.: Cell-typespecific gene expression and a catalasemic peroxisomes in a null Cat2 catalase mutant of maize. - Proc. nat. Acad. Sci. USA 80: 4455-4459, 1983. Go to original source...
  56. Vieira dos Santos, C., Rey, P.: Plant thioredoxins are key actors in oxidative stress response. - Trends Plant Sci. 11: 329-334, 2006.
  57. Vysotskaya, L., Hedley, P.E., Sharipova, G., Veselov, D., Kudoyarova, G., Morris, J., Jones, H.G.: Effect of salinity on water relations of wild barley plants differing in salt tolerance. - AoB Plants 2010: plq006, 2010. Go to original source...
  58. Wang, W.X., Vinocur, B., Arie, A.: Plants responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. - Planta 218: 1-14, 2003. Go to original source...
  59. Wang, W., Vinocur, B., Shoseyov, O., Altman, A.: Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. - Trends Plant Sci. 9: 244-252, 2004. Go to original source...
  60. Xue, G.P., Loverridge, C.W.: HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. - Plant J. 37: 326-339, 2004. Go to original source...
  61. Zhu, J.K.: Plant salt tolerance. - Trends Plant Sci. 6: 66-71, 2001. Go to original source...