Abstract
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.
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Abbreviations
- ABA:
-
abscisic acid
- APX:
-
ascorbate peroxidase
- α-TUB:
-
α-tubuline
- BAS1:
-
2-cis-peroxiredoxin 1
- CAT:
-
catalase
- Cu/Zn-SOD:
-
copper-zinc superoxide dismutase
- DRF1:
-
dehydration responsive factor-1
- GST:
-
glutathione-S-transferase
- HS:
-
heat shock
- MT2:
-
methallothionein-like protein type 2
- NHX1:
-
Na+/H+ antiporter 1
- SS:
-
salt stress
References
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.
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.
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.
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.
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.
Bagatta, M., Pacifico D., Mandolino, G.: Evaluation of the osmotic adjustment response within the genus Beta. — J. Sugar Beet Res. 45: 119–133, 2008.
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.
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.
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.
Boston, R.S., Viitanen, P.V., Vierling, E.: Molecular chaperones and protein folding in plants. — Plant mol. Biol. 32: 191–222, 1996.
Bowler, C., Fluhr, R.: The role of calcium and activated oxygen as signals for controlling cross-tolerance. — Trends Plant. Sci. 5: 241–246, 2000.
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.
Cramer, G.R.: Differential effects of salinity on leaf elongation kinetics of three grass species. — Plant Soil 253: 233–244, 2003.
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.
Fedina, I.S., Nedeva, D., Çiçek, N.: Pre-treatment with H2O2 induces salt tolerance in barley seedlings. — Biol. Plant. 53: 321–24, 2009.
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.
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.
Gechev, T.S., Hille, J.: Hydrogen peroxide as a signal controlling plant programmed cell death. — J. cell. Biol. 168: 17–20, 2005.
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.
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.
Harrington, H.M., Alm, D.M.: Interaction of heat and salt shock in cultured tobacco cells. — Plant Physiol. 88: 618–625, 1988.
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.
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.
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.
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.
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.
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.
Kruse, E., Liu, Z., Kloppstech, K.: Expression of heat shock proteins during development of barley. — Plant mol. Biol. 23: 111–122, 1993.
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.
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.
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.
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.
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.
Mirouze, M., Paszkowski, J.: Epigenetic contribution to stress adaptation in plants. — Curr. Opin. Plant Biol. 14: 267–274, 2011.
Mizoi, J., Shinozaki, K., Yamaguchi-Shinozaki, K.: AP2/ERF family transcription factors in plant abiotic stress responses. — Biochim. biophys. Acta 1819: 86–96, 2012.
Munns, R.: Comparative physiology of salt and water stress. — Plant Cell Environ. 25: 239–250, 2002.
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.
Munns, R., Tester, M.: Mechanisms of salinity tolerance. — Annu. Rev. Plant Biol. 59:651–81, 2008.
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.
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.
Öztürk, Z.N., Talame, V., Deyholos, M., Michalowski, C.B., Galbrait, W., Gözükırmızı, 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.
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.
Patel, D., Franklin, K.A.: Temperature-regulation of plant architecture. — Plant Signal. Behav. 4: 577–579, 2009.
Petrov, V.D., Van Breusegem, F.: Hydrogen peroxide — a central hub for information flow in plant cell. — AoB Plants 2012: pls014, 2012.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Vieira dos Santos, C., Rey, P.: Plant thioredoxins are key actors in oxidative stress response. — Trends Plant Sci. 11: 329–334, 2006.
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.
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.
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.
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.
Zhu, J.K.: Plant salt tolerance. — Trends Plant Sci. 6: 66–71, 2001.
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Acknowledgements. The authors thank Nazaret Poyraz for technical assistance. This work was supported by the Scientific Research Projects Coordination Unit of the Istanbul University (No. BAP 4712) and the Erasmus Exchange Program to M.F.
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Faralli, M., Lektemur, C., Rosellini, D. et al. Effects of heat shock and salinity on barley growth and stress-related gene transcription. Biol Plant 59, 537–546 (2015). https://doi.org/10.1007/s10535-015-0518-x
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DOI: https://doi.org/10.1007/s10535-015-0518-x