THE RELATIONSHIP BETWEEN NITRIC OXIDE AND PLANT HORMONES IN SNP ADMINISTRATED SUNFLOWER PLANTS UNDER SALT STRESS CONDITION
Fusun Yurekli
Inonu University, Arts & Science Faculty, Department of Botany 44280 Malatya-TurkeyOguz Ayhan Kirecci
Bitlis Eren University, Vocational School of Hizan, Bitlis-TurkeyAbstract
Nitric oxide (NO) and sodium nitro prusside (SNP) are striking molecules and play important roles in animals and plants. SNP serves as nitric oxide donor in both
group. NO can act free radical and impaires important biomolecules functions beside this it has beneficial effect recovery from salinity, drought etc. NO and SNP are beneficial and protectant molecules in cope with stressfull conditions. In plants these molecules are very important, and regulate many physiological events. In the present study, endogen abscisic acid (ABA), indole acetic acid (IAA), gibberellic acid (GA3) and NO levels were investigated in NaCl, SNP and plant growth regulators treated sunflower plant (Helianthus annuus L.) leaves and roots. The content of NO was higher in GA3 + SNP treated plant leaves at 72 h. The highest IAA level was determined in IAA + SNP treated plant roots at 72 h. In NaCl + ABA treated plant leaves ABA was higher at 72 and GA3 levels were equal or less than the control group. Our results showed that coadministration of SNP and plant growth regulators cope with salinity stress via elevated internal hormone and NO level versus salinity.
Keywords:
nitric oxide, sodium nitroprusside, salinity, sunflowerReferences
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Arasimowicz, M., Floryszak-Wieczorek, J., (2007). Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Sci., 172, 876–887.
Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J., Harberd, N.P. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science, 311, 91–93.
Bethke, P.C., Libourel, I.G.L., Jones, R.L. (2006). Nitricoxide reduces seed dormancy in Arabidopsis. J. Exp. Bot., 57, 517–526.
Bethke, P.C., Libourel, I.G.L., Aoyama, N., Chung, Y.Y., Still, D.W., Jones, R.L. (2007). The Arabidopsis aleurone layer responds to nitricoxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol., 143, 1173–1188.
Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., Neill, S.J. (2006). ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J., 45, 113–122.
Cramer, G.R., Nowak, R.S. (1992). Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stressed barley. Physiol. Plant., 84(4), 600–605.
Colebrook, E.H., Stephen, G., Thomas, A.L., Phillips, P.H. (2014). The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol., 217, 67–75.
Correa-Aragunde, N., Graziano, M., Lamattina, L. (2004). Nitric oxide plays a central role in determining lateral root development in tomato. Planta, 218, 900–905.
Davies, W.J., Jones, H.G. (1991). Abscisic acid: physiology, biochemistry. BIOS. Scientific Publishers Ltd., Cambridge, UK.
Davies, P.J. (1995). The plant hormone concept: concentration, sensitivity and transport. In: Plant hormones: physiology, biochemistry and molecular biology, Davies, P.J. (ed.). Kluwer Academic Press, Dordrecht, The Netherlands.
Desikan, R., Cheung, M.K., Bright, J., Henson, D., Hancock, J.T., Neill, S.J. (2004). ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cell. J. Exp. Bot., 395, 205–212.
Dong, T.T., Tong, H., Xiao, L.T., Cheng, H.Y., Song, S. (2012). Nitrate, abscisic acid and gibberellin interactions on the thermo inhibition of lettuce seed germination. Plant Grow. Reg., 66, 191–202.
Durner, J., Klessig, D.F. (1999). Nitric oxide as a signal in plants. Curr. Opin. Plant Biol., 2, 369–374.
Fernández-Marcos, M., Sanz, L., Lewis, D.R., Muday, G.K., Lorenzo, O. (2011). Nitricoxide causes root apical meristem defects and growth inhibition while reducing PINFORMED1(PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. USA, 108, 18506–18511.
Fernández-Marcos, M., Sanz, L., Lorenzo, O. (2012). Nitricoxide: an emerging regulator of cell elongation during primary root growth. Plant Sign. Behav., 7, 196–200.
Flowers, T.J. (2004). Improving crop salt tolerance. J. Exp. Bot., 55(396), 307–319.
Freschi, L. (2013). Nitric oxide and phytohormone interactions: current status and perspectives. Front. Plant Sci., 4, 398, 2013.
García-Mata, C., Lamattina, L. (2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol., 126, 1196–1204.
Hancock, J.T., Neill, S.J., Wilson, I.D. (2011). Nitric oxide and ABA in the control of plant function. Plant Sci., 181, 555–559.
He, H., Le, H., Gu, M. (2012). Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Sign. Behav., 7(4), 469–471.
Hu, X.Y., Neill, S.J., Tang, Z.C., Cai, W.M. (2005). Nitricoxide mediates gravitropic bending in soybean roots. Plant Physiol., 137, 663–670.
Kolbert, Z., Bartha, B., Erdei, L. (2005). Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselinum crispum plants under osmotic and drought stress. Proceedings of the 8th Hungarian Congress on Plant Physiologyand the 6th Hungarian Conference on Photosynthesis.
Lanteri, M.L., Pagnussat, G.C., Lamattina, L. (2006). Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J. Exp. Bot., 57, 1341–1351.
Leon, J., Lozano-Juste, J. (2011). Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol., 156, 1410–1423.
Lombardo, M.C., Graziano, M., Polacco, J.C., Lamattina, L. (2006). Nitricoxide functions as a positive regulator of root hair development. Plant Sign. Behav., 1, 28– 33.
Lozano-Juste, J., Leon, J. (2010 a). Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR-and AtNOA1-dependent nitricoxide biosynthesis in Arabidopsis. Plant Physiol. 152, 891–903.
Lozano-Juste, J., Leon, J. (2010 b). Nitric oxide modulates sensitivity to ABA. Plant Sign. Behav., 5, 314–316.
Mahajan, S., Tuteja, N. (2005). Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys., 444, 139–158.
Marrs, K.A. (1996). The functions and regulation of glutathione S-Transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 47, 127–158.
Martinez-Ferri, E., Manrique, E., Valladares, F., Balaguer, L. (2004). Winter photoinhibition in the field involves different processes in four co-occurring Mediterranean tree species. Tree Physiol., 24, 981–990.
Miransari, M., Smith, D.L. (2014). Plant hormones and seed germination. Environ. Exp. Bot., 99, 110– 121.
Moore, T.C. (1989). Biochemistry and physiology of plant hormones, 2nd edn. Springer-Verlag, New York U.S.A,
Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell. Environ., 25(2), 239–250.
Neill, S.J., Horgan, R. (1985). Abscisic acid production and water relations in wilty tomato mutants subjected to water deficiency. J. Exp. Bot. 36, 1222–1231.
Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J. (2008 a). Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot, 59, 165–176.
Ötvös, K., Pasternak, T.P., Miskolczi, P., Domoki, M., Dorjgotov, D., Szucs, A. (2005). Nitricoxide is required for, and promotes auxin-mediated activation of cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J. 43, 849–860.
Pagnussat, G.C., Lanteri, M.L., Lombardo, M.C., Lamattina, L. (2004). Nitricoxide mediates the indole acetic acid induction activation of a mitogen-activated proteinkinase cascade involved in adventitious root development. Plant Physiol., 135, 279–286.
Parida, A.K., Das, A.B. (2005). Salt tolerance and salinity effects on plants: A review. Ecotoxicol. Environ. Saf., 60(3), 324–349.
Pii, Y., Crimi, M., Cremonese, G., Spena, A., Pandolfini, T. (2007). Auxin and nitric oxide control in determinate nodule formation. BMC Plant Biol., 8,7–21.
Porcel, R., Aroca, R., Ruiz-Lozano, J.M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev., 32, 181–200.
Popko, J., Hänsch, R., Mendel, R., Polle, A., Teichmann, A. (2010). The role of abscisic acid and auxin in the response of poplar to abiotic stress. Plant Biol., 12, 242–258.
Radhakrishnan, R., Lee, I.J. (2013). Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. J. Plant Growth Reg., 32, 22–30.
Sarath, G., Bethke, P.C., Jones, R., Baird, L.M, Hou, G., Mitchell, R.B. (2006). Nitric oxide accelerates seed germination in warm-season grasses. Planta, 223, 1154–1164.
Sripinyowanich, S., Klomsakul, P., Boonburapong, B., Bangyeekhun, T., Asami, T., Gu, H., Buaboocha, T., Chadchawan, S. (2013). Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): The role os OsP5CS1 and OsP5CR gene expression during salt stress. Environ. Exp. Bot., 86, 94–105.
Szepsi, A., Csiszar, J., Gemes, K., Horvarth, E., Horvath, F., Simon, L.M., Tari, I. (2009). Salicylic acid improves the acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ contents of the leaves without toxicity symptoms in Solanum lycopersicum L. J. Plant Physiol., 166, 914–925.
Tossi, V., Lamattina, L., Cassia, R. (2009). An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol., 181, 871–879.
Tun, N.N., Holk, A., Scherer, G.F.E. (2001). Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett., 509, 174–176.
Valladares, F., Pearcy, R.W. (2002). Drought can be more critical in the shade than in the sun: a field study of carbon gain and photo-inhibition in a Californian shrub during a dry El Nino year. Plant Cell Environ., 25, 749–759.
Weyers, J.D.B., Paterson, N.W. (2001). Plant hormones and the control of physiological processes. New Phytol., 152, 375–407.
Xiong, L., Schumaker, K.S., Zhu, J.K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell, 14, 165–183.
Xu, J., Wang, W.Y., Yin, H.X., Liu, X.J., Sun, H., Mi, Q. (2010). Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil., 326, 321–330.
Xue-Xuan, X., Hong-Bo, S., Yuan-Yuan, M., Gang, X., Jun-Na, S., Dong Gang, G., Cheng-Jiang, R. (2010). Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abioticstressed conditions. Crit. Rev. Biotech., 30, 222–230.
Yamaguchi-Shinozaki, K., Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and toletance to dehydration and cold stresses. Ann. Rev. Plant Biol., 57, 781–803.
Yarra, R., He, S.J., Abbagani, S., Ma, B., Bulle, M., Zhang, W.K. (2012). Overexpression of a wheat Na+/H+ antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tiss. Organ Cult., 111, 49–57.
Yordanov, I., Velikova, V., Tsonev, T. (2000). Plant responses to drought, acclimatation and stress tolerance. Photosynthetica, 38, 171–186.
Yu, J.N., Huang, J., Wang, Z.N., Zhang, J.S., Chen, S.Y. (2007). An Na+/H+ antiporter gene from wheat plays an important role in stress tolerance. J. Bio. Sci., 32(6), 1153–61.
Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., Zhang, W. (2006b). Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta, 224, 545–555.
Zhao, Q., Zhao, Y.J., Zhao, B.C., Ge, R.C., Li, M., Shen, Y.Z., Huang, Z.J. (2009). Cloning and functional analysis of wheat V-H+-ATPase subunit genes. Plant Mol. Biol., 69(1–2), 33–46.
Zhu, J.K., (2007). Plant salt stress. John Wiley & Sons, Ltd. Zhu, X.F., Jiang, T., Wang, Z.W., Lei, G.J., Shi, Y.Z., Li, G.X., Zheng, S.J. (2012). Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J. Hazard. Mat., 239–240, 302–307.
Zörb, C., Geilfus, C.M., Mühling, K.H., Ludwig-Müller, J. (2013). The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J. Plant Physiol., 170, 220–224.
Arasimowicz, M., Floryszak-Wieczorek, J., (2007). Nitric oxide as a bioactive signaling molecule in plant stress responses. Plant Sci., 172, 876–887.
Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J., Harberd, N.P. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science, 311, 91–93.
Bethke, P.C., Libourel, I.G.L., Jones, R.L. (2006). Nitricoxide reduces seed dormancy in Arabidopsis. J. Exp. Bot., 57, 517–526.
Bethke, P.C., Libourel, I.G.L., Aoyama, N., Chung, Y.Y., Still, D.W., Jones, R.L. (2007). The Arabidopsis aleurone layer responds to nitricoxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol., 143, 1173–1188.
Bright, J., Desikan, R., Hancock, J.T., Weir, I.S., Neill, S.J. (2006). ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J., 45, 113–122.
Cramer, G.R., Nowak, R.S. (1992). Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stressed barley. Physiol. Plant., 84(4), 600–605.
Colebrook, E.H., Stephen, G., Thomas, A.L., Phillips, P.H. (2014). The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol., 217, 67–75.
Correa-Aragunde, N., Graziano, M., Lamattina, L. (2004). Nitric oxide plays a central role in determining lateral root development in tomato. Planta, 218, 900–905.
Davies, W.J., Jones, H.G. (1991). Abscisic acid: physiology, biochemistry. BIOS. Scientific Publishers Ltd., Cambridge, UK.
Davies, P.J. (1995). The plant hormone concept: concentration, sensitivity and transport. In: Plant hormones: physiology, biochemistry and molecular biology, Davies, P.J. (ed.). Kluwer Academic Press, Dordrecht, The Netherlands.
Desikan, R., Cheung, M.K., Bright, J., Henson, D., Hancock, J.T., Neill, S.J. (2004). ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cell. J. Exp. Bot., 395, 205–212.
Dong, T.T., Tong, H., Xiao, L.T., Cheng, H.Y., Song, S. (2012). Nitrate, abscisic acid and gibberellin interactions on the thermo inhibition of lettuce seed germination. Plant Grow. Reg., 66, 191–202.
Durner, J., Klessig, D.F. (1999). Nitric oxide as a signal in plants. Curr. Opin. Plant Biol., 2, 369–374.
Fernández-Marcos, M., Sanz, L., Lewis, D.R., Muday, G.K., Lorenzo, O. (2011). Nitricoxide causes root apical meristem defects and growth inhibition while reducing PINFORMED1(PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. USA, 108, 18506–18511.
Fernández-Marcos, M., Sanz, L., Lorenzo, O. (2012). Nitricoxide: an emerging regulator of cell elongation during primary root growth. Plant Sign. Behav., 7, 196–200.
Flowers, T.J. (2004). Improving crop salt tolerance. J. Exp. Bot., 55(396), 307–319.
Freschi, L. (2013). Nitric oxide and phytohormone interactions: current status and perspectives. Front. Plant Sci., 4, 398, 2013.
García-Mata, C., Lamattina, L. (2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol., 126, 1196–1204.
Hancock, J.T., Neill, S.J., Wilson, I.D. (2011). Nitric oxide and ABA in the control of plant function. Plant Sci., 181, 555–559.
He, H., Le, H., Gu, M. (2012). Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Sign. Behav., 7(4), 469–471.
Hu, X.Y., Neill, S.J., Tang, Z.C., Cai, W.M. (2005). Nitricoxide mediates gravitropic bending in soybean roots. Plant Physiol., 137, 663–670.
Kolbert, Z., Bartha, B., Erdei, L. (2005). Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselinum crispum plants under osmotic and drought stress. Proceedings of the 8th Hungarian Congress on Plant Physiologyand the 6th Hungarian Conference on Photosynthesis.
Lanteri, M.L., Pagnussat, G.C., Lamattina, L. (2006). Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J. Exp. Bot., 57, 1341–1351.
Leon, J., Lozano-Juste, J. (2011). Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol., 156, 1410–1423.
Lombardo, M.C., Graziano, M., Polacco, J.C., Lamattina, L. (2006). Nitricoxide functions as a positive regulator of root hair development. Plant Sign. Behav., 1, 28– 33.
Lozano-Juste, J., Leon, J. (2010 a). Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR-and AtNOA1-dependent nitricoxide biosynthesis in Arabidopsis. Plant Physiol. 152, 891–903.
Lozano-Juste, J., Leon, J. (2010 b). Nitric oxide modulates sensitivity to ABA. Plant Sign. Behav., 5, 314–316.
Mahajan, S., Tuteja, N. (2005). Cold, salinity and drought stresses: An overview. Arch. Biochem. Biophys., 444, 139–158.
Marrs, K.A. (1996). The functions and regulation of glutathione S-Transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 47, 127–158.
Martinez-Ferri, E., Manrique, E., Valladares, F., Balaguer, L. (2004). Winter photoinhibition in the field involves different processes in four co-occurring Mediterranean tree species. Tree Physiol., 24, 981–990.
Miransari, M., Smith, D.L. (2014). Plant hormones and seed germination. Environ. Exp. Bot., 99, 110– 121.
Moore, T.C. (1989). Biochemistry and physiology of plant hormones, 2nd edn. Springer-Verlag, New York U.S.A,
Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell. Environ., 25(2), 239–250.
Neill, S.J., Horgan, R. (1985). Abscisic acid production and water relations in wilty tomato mutants subjected to water deficiency. J. Exp. Bot. 36, 1222–1231.
Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J. (2008 a). Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot, 59, 165–176.
Ötvös, K., Pasternak, T.P., Miskolczi, P., Domoki, M., Dorjgotov, D., Szucs, A. (2005). Nitricoxide is required for, and promotes auxin-mediated activation of cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J. 43, 849–860.
Pagnussat, G.C., Lanteri, M.L., Lombardo, M.C., Lamattina, L. (2004). Nitricoxide mediates the indole acetic acid induction activation of a mitogen-activated proteinkinase cascade involved in adventitious root development. Plant Physiol., 135, 279–286.
Parida, A.K., Das, A.B. (2005). Salt tolerance and salinity effects on plants: A review. Ecotoxicol. Environ. Saf., 60(3), 324–349.
Pii, Y., Crimi, M., Cremonese, G., Spena, A., Pandolfini, T. (2007). Auxin and nitric oxide control in determinate nodule formation. BMC Plant Biol., 8,7–21.
Porcel, R., Aroca, R., Ruiz-Lozano, J.M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sustain. Dev., 32, 181–200.
Popko, J., Hänsch, R., Mendel, R., Polle, A., Teichmann, A. (2010). The role of abscisic acid and auxin in the response of poplar to abiotic stress. Plant Biol., 12, 242–258.
Radhakrishnan, R., Lee, I.J. (2013). Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. J. Plant Growth Reg., 32, 22–30.
Sarath, G., Bethke, P.C., Jones, R., Baird, L.M, Hou, G., Mitchell, R.B. (2006). Nitric oxide accelerates seed germination in warm-season grasses. Planta, 223, 1154–1164.
Sripinyowanich, S., Klomsakul, P., Boonburapong, B., Bangyeekhun, T., Asami, T., Gu, H., Buaboocha, T., Chadchawan, S. (2013). Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): The role os OsP5CS1 and OsP5CR gene expression during salt stress. Environ. Exp. Bot., 86, 94–105.
Szepsi, A., Csiszar, J., Gemes, K., Horvarth, E., Horvath, F., Simon, L.M., Tari, I. (2009). Salicylic acid improves the acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ contents of the leaves without toxicity symptoms in Solanum lycopersicum L. J. Plant Physiol., 166, 914–925.
Tossi, V., Lamattina, L., Cassia, R. (2009). An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol., 181, 871–879.
Tun, N.N., Holk, A., Scherer, G.F.E. (2001). Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett., 509, 174–176.
Valladares, F., Pearcy, R.W. (2002). Drought can be more critical in the shade than in the sun: a field study of carbon gain and photo-inhibition in a Californian shrub during a dry El Nino year. Plant Cell Environ., 25, 749–759.
Weyers, J.D.B., Paterson, N.W. (2001). Plant hormones and the control of physiological processes. New Phytol., 152, 375–407.
Xiong, L., Schumaker, K.S., Zhu, J.K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell, 14, 165–183.
Xu, J., Wang, W.Y., Yin, H.X., Liu, X.J., Sun, H., Mi, Q. (2010). Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil., 326, 321–330.
Xue-Xuan, X., Hong-Bo, S., Yuan-Yuan, M., Gang, X., Jun-Na, S., Dong Gang, G., Cheng-Jiang, R. (2010). Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abioticstressed conditions. Crit. Rev. Biotech., 30, 222–230.
Yamaguchi-Shinozaki, K., Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and toletance to dehydration and cold stresses. Ann. Rev. Plant Biol., 57, 781–803.
Yarra, R., He, S.J., Abbagani, S., Ma, B., Bulle, M., Zhang, W.K. (2012). Overexpression of a wheat Na+/H+ antiporter gene (TaNHX2) enhances tolerance to salt stress in transgenic tomato plants (Solanum lycopersicum L.). Plant Cell Tiss. Organ Cult., 111, 49–57.
Yordanov, I., Velikova, V., Tsonev, T. (2000). Plant responses to drought, acclimatation and stress tolerance. Photosynthetica, 38, 171–186.
Yu, J.N., Huang, J., Wang, Z.N., Zhang, J.S., Chen, S.Y. (2007). An Na+/H+ antiporter gene from wheat plays an important role in stress tolerance. J. Bio. Sci., 32(6), 1153–61.
Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., Zhang, W. (2006b). Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta, 224, 545–555.
Zhao, Q., Zhao, Y.J., Zhao, B.C., Ge, R.C., Li, M., Shen, Y.Z., Huang, Z.J. (2009). Cloning and functional analysis of wheat V-H+-ATPase subunit genes. Plant Mol. Biol., 69(1–2), 33–46.
Zhu, J.K., (2007). Plant salt stress. John Wiley & Sons, Ltd. Zhu, X.F., Jiang, T., Wang, Z.W., Lei, G.J., Shi, Y.Z., Li, G.X., Zheng, S.J. (2012). Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J. Hazard. Mat., 239–240, 302–307.
Zörb, C., Geilfus, C.M., Mühling, K.H., Ludwig-Müller, J. (2013). The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J. Plant Physiol., 170, 220–224.
Fusun Yurekli
Inonu University, Arts & Science Faculty, Department of Botany 44280 Malatya-Turkey
Inonu University, Arts & Science Faculty, Department of Botany 44280 Malatya-Turkey
Oguz Ayhan Kirecci
Bitlis Eren University, Vocational School of Hizan, Bitlis-Turkey
Bitlis Eren University, Vocational School of Hizan, Bitlis-Turkey
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