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Evidence for the involvement of nitric oxide and reactive oxygen species in osmotic stress tolerance of wheat seedlings: Inverse correlation between leaf abscisic acid accumulation and leaf water loss

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Abstract

Nitric oxide (NO) and reactive oxygen species (ROS) play important roles in both abscisic acid (ABA) signaling and stress-induced ABA accumulation. However, little is known about their physiological roles in the whole plant. In this study, the effects of NO and ROS on leaf water control and the roles of ABA were determined using wheat (Triticum aestivum L.) seedlings. As compared with the control, osmotic stress reduced leaf water loss (LWL) while it increased leaf ABA content. The effects of osmotic stress on LWL and ABA contents were partially reversed by NO scavengers or NO synthase (NOS) inhibitors. Furthermore, sodium nitroprusside (SNP) at concentrations between 0.01 and 10 mM all reduced LWL efficiently and induced ABA accumulation in a dose-dependent manner. When ABA synthesis was inhibited by fluridone or actidione, the effects of SNP on LWL were partially reversed. These results suggest that NO is involved in leaf water maintenance of wheat seedlings under osmotic stress, and one of the possible mechanisms is by stimulating ABA synthesis. The ROS scavengers used in our experiments had no effects on either LWL or ABA accumulation induced by osmotic stress. However, all ROS induced LWL reduction and ABA accumulation significantly. Hydrogen peroxide had the same effects as SNP on LWL and induced ABA accumulation in a dose-dependent manner but had a maximal effect at 1 mM. Fluridone reversed the effects of H2O2 on both LWL reduction and ABA accumulation, while actidione had no effect. These results suggest that ROS are also involved in leaf water maintenance of wheat seedlings by stimulating ABA biosynthesis, but with a different mechanism to that of NO. The ABA-independent mechanism in NO/ROS regulation of leaf water balance is discussed, in relation to our results.

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References

  • Asada D. 1992. Production and scavenging of active oxygen in chloroplasts. In: Scandalios J.G. (ed.), Molecular Biology of Free Radical Scavenging Systems, Cold Spring Harbor Laboratory Press, New York, pp. 173–192.

    Google Scholar 

  • Beligni M.V. and Lamattina L. 2000. Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210: 215–221.

    Google Scholar 

  • Beligni M.V. and Lamattina L. 2001. Nitric oxide: A nontraditional regulator of plant growth. Trends Plant Sci. 6: 508–509.

    Google Scholar 

  • Chen Z., Silva H. and Klessig D.F. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883–1886.

    Google Scholar 

  • Dean J.V. and Harper J.E. 1986. Nitric oxide and nitrous oxide production by soybean and winged bean during the in vivo nitrate reductase assay. Plant Physiol. 82: 718–723.

    Google Scholar 

  • Delledonne M., Xia Y.J., Dixon R.A. and Lamb C. 1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585–588.

    Google Scholar 

  • Desikan R., Griffiths R., Hancock J. and Neill S. 2002. A new role for an old enzyme: Nitrate reductase mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 99: 16314–16348.

    Google Scholar 

  • Durner J. and Klessig D. 1999. Nitric oxide as a signal in plants. Curr. Opin. Plant Biol. 2: 369–374.

    Google Scholar 

  • Durner J., Wendehenne D. and Klessig D.F. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl Acad. Sci. USA 95: 10328–10333.

    Google Scholar 

  • García-Mata C. and Lammattina L. 2001. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126: 1196–1204.

    Google Scholar 

  • García-Mata C. and Lammattina L. 2002. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128: 790–792.

    Google Scholar 

  • Gogorcena Y., Iturbe-Ormaetxe I., Escuredo P.R. and Becana M. 1995. Antioxidant defenses against activated oxygen in pea nodules subjected to water stress. Plant Physiol. 108: 753–759.

    Google Scholar 

  • Gouvêa C.M.C.P., Souza J.F., Magalhães A.C.N. and Martins I.S. 1997. NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regul. 21: 183–187.

    Google Scholar 

  • Guan L.M., Zhao J. and Scandalios J.G. 2000. Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J. 22: 87–95.

    Google Scholar 

  • Iturbe-Ormaetxe I., Escuredo P.R., Arrese-Igor C. and Becana M. 1998. Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol. 116: 173–181.

    Google Scholar 

  • Jabs T., Dietrich R.A. and Dangl J. 1996. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273: 1853–1856.

    Google Scholar 

  • Jia W. and Zhang J. 2000. Water stress-induced abscisic acid accumulation in relation to reducing agents and sulfhydryl modifiers in maize plant. Plant Cell Environ. 23: 1389–1395.

    Google Scholar 

  • Leung J. and Giraudat J. 1998. Abscisic acid signal transduction. Ann. Rev. Plant Physiol. Plant Mol. Biol. 49: 199–222.

    Google Scholar 

  • Magalhaes J.R., Monte D.C. and Durzan D. 2000. Nitric oxide and ethylene emission in Arabidopsis thaliana. Physiol. Mol. Biol. Plant. 6: 117–127.

    Google Scholar 

  • Moran J.F., Becana M., Iturbe-Ormaetxe I., Frechilla S., Klucas R.V. and Aparicio-Tejo P. 1994. Drought induces oxidative stress in pea plants. Planta 194: 346–352.

    Google Scholar 

  • Ninnemann H. and Maier J. 1996. Indications for occurrence of nitric oxide synthases in fungi and plants and involvement in photoconidiation of Neurospora crassa. Photochem. Photobiol. 64: 393–398.

    Google Scholar 

  • Pagnussat G.C., Simontacchi M., Puntarulo S. and Lamattina L. 2002. Nitric oxide is required for root organogenesis. Plant Physiol. 129: 954–956.

    Google Scholar 

  • Pei Z.M., Murata Y., Benning G., Thomine S., Klüsener B., Allen G.J., Grill E. and Schroeder J.I. 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–734.

    Google Scholar 

  • Price A.H., Atherton N.M. and Hendry G.A.F. 1989. Plants under drought-stress generate activated oxygen. Free Rad. Res. Comm. 8: 61–66.

    Google Scholar 

  • Smirnoff N. 1993. The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol. 125: 27–58.

    Google Scholar 

  • Yamasaki H., Sakihama Y. and Takahashi S. 1999. An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 4: 128–129.

    Google Scholar 

  • Takahashi S. and Yamasaki H. 2002. Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide. FEBS Lett. 512: 145–148.

    Google Scholar 

  • Wang H.L. and Zhang C.L. 1995. Seasonal changes of endogenous ABA and cytokinins in environmental adaptation of different ecotypes of reed plants. J. Environ. Sci. 7: 449–454.

    Google Scholar 

  • Wang X.Q., Ullah H., Jones A.M. and Assmann S.M. 2001. G proteins regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292: 2070–2072.

    Google Scholar 

  • Wu Y., Kuzma J., Maréchal E., Graeff R., Lee H.C., Foster R. and Chua N.H. 1997. Abscisic acid signaling through cyclic ADP-ribose in plants. Science 278: 2126–2130.

    Google Scholar 

  • Yamasaki H. and Sakihama Y. 2000. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett. 468: 89–92.

    Google Scholar 

  • Zeevaart J.A.D. and Creelman R.A. 1988. Metabolism and physiology of abscisic acid. Ann. Rev. Plant Physiol. Plant Mol. Biol. 39: 439–473.

    Google Scholar 

  • Zhang J. and Davies W.J. 1989. Abscisic acid produced in dehydrating roots may enable the plant to measure the water status of the soil. Plant Cell Environ. 12: 73–81.

    Google Scholar 

  • Zhang X., Zhang L., Dong F., Gao J., Galbraith D.W. and Song C.P. 2001. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 126: 1438–1448.

    Google Scholar 

  • Zhao Z., Chen G. and Zhang C. 2001. Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Aust. J. Plant Physiol. 28: 1055–1061.

    Google Scholar 

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Correspondence to Zhiguang Zhao.

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Xing, H., Tan, L., An, L. et al. Evidence for the involvement of nitric oxide and reactive oxygen species in osmotic stress tolerance of wheat seedlings: Inverse correlation between leaf abscisic acid accumulation and leaf water loss. Plant Growth Regulation 42, 61–68 (2004). https://doi.org/10.1023/B:GROW.0000014894.48683.1b

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  • DOI: https://doi.org/10.1023/B:GROW.0000014894.48683.1b

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