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Nitric oxide acts downstream of abscisic acid in molybdenum-induced oxidative tolerance in wheat

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Abstract

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Our study first reveals that Mo mediates oxidative tolerance through ABA signaling. Moreover, NO acts downstream of ABA signaling in Mo-induced oxidative tolerance in wheat under drought stress.

Abstract

Nitric oxide (NO) is related to the improvement of molybdenum (Mo)-induced oxidative tolerance. While the function of Mo in abscisic acid (ABA) synthesis and in mediating oxidative tolerance by the interaction of ABA and NO remain to be studied. The –Mo and +Mo treatment-cultivated wheat was separated and subsequently was pretreated with AO inhibitor, ABA synthesis inhibitor, exogenous ABA, NO scavenger, NO donor or their combinations under polyethylene glycol 6000 (PEG)-stimulated drought stress (PSD). The AO activity and ABA content were increased by Mo in wheat under PSD, however, AO inhibitor decreased AO activity, correspondingly reduced ABA accumulation, suggesting that AO involves in the regulation of Mo-induced ABA synthesis. Mo enhanced activities and expressions of antioxidant enzyme, while these effects of Mo were reversed by AO inhibitor and ABA synthesis inhibitor due to the decrease of ABA content, but regained by exogenous ABA, indicating that Mo induces oxidative tolerance through ABA. Moreover, NO scavenger inhibited activities of antioxidant enzyme caused by Mo and exogenous ABA, but the inhibitions were eliminated by NO donor, indicating that NO is involved in ABA pathway in the regulation of Mo-induced oxidative tolerance in wheat under PSD. Finally, we proposed a scheme for the mechanism of Mo-induced oxidative tolerance.

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References

  • Arc E, Galland M, Godin B, Cueff G, Rajjou L (2013a) Nitric oxide implication in the control of seed dormancy and germination. Front Plant Sci 4:346. https://doi.org/10.3389/fpls.2013.00346

    PubMed  PubMed Central  Google Scholar 

  • Arc E, Sechet J, Corbineau F, Rajjou L, Marionpoll A (2013b) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63. https://doi.org/10.3389/fpls.2013.00063

    PubMed  PubMed Central  Google Scholar 

  • Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5:28. https://doi.org/10.3389/fpls.2014.00028

    Article  PubMed  PubMed Central  Google Scholar 

  • Daszkowskagolec A, Szarejko I (2013) Open or close the gate-stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138. https://doi.org/10.3389/fpls.2013.00138

    Google Scholar 

  • Ding Y, Cao J, Ni L, Zhu Y, Zhang A, Tan M, Jiang M (2012) ZmCPK11 is involved in abscisic acid-induced antioxidant defence and functions upstream of ZmMPK5 in abscisic acid signalling in maize. J Exp Bot 64:871–884

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding L, Gao C, Li YR, Li Y, Zhu Y, Xu GH, Shen QR, Kaldenhoff R, Kai L, Guo SW (2015) The enhanced drought tolerance of rice plants under ammonium is related to aquaporin (AQP). Plant Sci 234:14–21

    Article  CAS  PubMed  Google Scholar 

  • Gayatri G, Agurla S, Raghavendra AS (2013) Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front Plant Sci 4:425. https://doi.org/10.3389/fpls.2013.00425

    Article  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  Google Scholar 

  • Leon J, Castillo MC, Coego A, Lozanojuste J, Mir R (2014) Diverse functional interactions between nitric oxide and abscisic acid in plant development and responses to stress. J Exp Bot 65:907–921

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zhang J, Zhang J, Hao L, Hua J, Duan L, Zhang M, Li Z (2013) Expression of an Arabidopsis molybdenum cofactor sulphurase gene in soybean enhances drought tolerance and increases yield under field conditions. Plant Biotechnol J 11:747–758

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Zhuo C, Wang X, Guo Z (2014) Nitrate reductase (NR)-dependent NO production mediates ABA- and H2O2 -induced antioxidant enzymes. Plant Physiol Bioch 74:9–15

    Article  CAS  Google Scholar 

  • Ma F, Lu R, Liu H, Shi B, Zhang J, Tan M, Zhang A, Jiang M (2012) Nitric oxide-activated calcium/calmodulin-dependent protein kinase regulates the abscisic acid-induced antioxidant defence in maize. J Exp Bot 63:4835–4847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendel RR (2013) Metabolism of molybdenum. In: Banci L (ed) Metallomics and the cell, metal ions in life sciences, 12. Springer, Dordrecht, pp 503–528

    Google Scholar 

  • Nagamune K, Hicks LM, Fux B, Brossier F, Chini EN, Sibley LD (2008) Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451:207–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54

    Article  CAS  Google Scholar 

  • Osakabe Y, Yamaguchishinozaki K, Shinozaki K, Tran LS (2014a) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202:35–49

    Article  PubMed  Google Scholar 

  • Osakabe Y, Osakabe K, Shinozaki K, Tran LS (2014b) Response of plants to water stress. Front Plant Sci 5:86. https://doi.org/10.3389/fpls.2014.00086

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. https://doi.org/10.1093/nar/29.9.e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Planchet E, Verdu I, Delahaie J, Cukier C, Girard C, Paven MM, Limami AM (2014) Abscisic acid-induced nitric oxide and proline accumulation in independent pathways under water-deficit stress during seedling establishment in Medicago truncatula. J Exp Bot 65:2161–2170

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro DM, Desikan RBJ, Confraria A, Harrison J, Hancock JT, Barros RS, Neill SJ, Wilson ID (2009) Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ 32:46–57

    Article  CAS  PubMed  Google Scholar 

  • Seo M, Peeters AJM, Koiwai H, Oritani T, Marionpoll A, Zeevaart JAD, Koornneef M, Kamiya Y, Koshiba T (2000) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. P Nati Acad Sci USA 97:12908–12913

    Article  CAS  Google Scholar 

  • Shu S, Gao P, Li L, Yuan Y, Sun J, Guo S (2016) Abscisic acid-induced H2O2 accumulation enhances antioxidant capacity in pumpkin-grafted cucumber leaves under Ca(NO3)2 tress. Front Plant Sci 7:1489. https://doi.org/10.3389/fpls.2016.01489

    PubMed  PubMed Central  Google Scholar 

  • Sun XC, Hu CX, Tan QL (2006) Effects of molybdenum on antioxidative defense system and membrane lipid peroxidation in winter wheat under low temperature stress. J Plant Physiol Mol Biol 32:175–182

    CAS  Google Scholar 

  • Sun XC, Hu CX, Tan QL, Liu JS, Liu HE (2009) Effects of molybdenum on expression of cold-responsive genes in abscisic acid (ABA)-dependent and ABA-independent pathways in winter wheat under low-temperature stress. Ann Bot-London 104:345–356

    Article  CAS  Google Scholar 

  • Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:12449. https://doi.org/10.1038/srep12449

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang PC, Du YY, Hou YJ, Zhao Y, Hsu C, Yuan FJ, Zhu XF, Tao WA, Song CP, Zhu JK (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. P Nati Acad Sci USA 112:613–618

    Article  CAS  Google Scholar 

  • Wu SW, Hu CX, Tan QL, Nie ZJ, Sun XC (2014) Effects of molybdenum on water utilization, antioxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum) under drought stress. Plant Physiol Bioch 83:365–374

    Article  CAS  Google Scholar 

  • Wu SW, Hu CX, Tan QL, Lu L, Shi KL, Yong Z, Sun XC (2015) Drought stress tolerance mediated by zinc-induced antioxidative defense and osmotic adjustment in cotton (Gossypium Hirsutum). Acta Physiol Plant 37:1–9

    Article  Google Scholar 

  • Wu SW, Hu CX, Tan QL, Xu SJ, Sun XC (2017) Nitric oxide mediates molybdenum-induced antioxidant defense in wheat under drought stress. Front Plant Sci 8:1085. https://doi.org/10.3389/fpls.2017.01085

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiong LM, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress and osmotic Stress responsive gene expression. Plant Cell 13:2063–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zdunek-Zastocka E (2008) Molecular cloning, characterization and expression analysis of three aldehyde oxidase genes from Pisum sativum L. Plant Physiol Bioch 46:19–28

    Article  CAS  Google Scholar 

  • Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50

    Article  CAS  PubMed  Google Scholar 

  • Zhang YM, Tan JL, Guo ZF, Lu SY, He SJ, Wei S, Zhou BY (2009) Increased abscisic acid levels in transgenic tobacco over-expressing 9 cis -epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant Cell Environ 32:509–519

    Article  PubMed  Google Scholar 

  • Zhang A, Zhang J, Zhang J, Ye N, Zhang H, Tan M, Jiang M (2011) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol 52:181–192

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Hu CX, Zhao XH, Tan QL, Sun XC, Cao AY, Cui M, Zhang Y (2012) Molybdenum improves antioxidant and osmotic-adjustment ability against salt stress in Chinese cabbage (Brassica campestris L. ssp. Pekinensis). Plant Soil 355:375–383

    Article  CAS  Google Scholar 

  • Zhang H, Liu Y, Wen F, Yao D, Wang L, Guo J, Ni L, Zhang A, Tan M, Jiang M (2014) A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defence and oxidative stress tolerance in rice. J Exp Bot 65:5795–5809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Yu HY, Zhang YS, Wang YB, Li MY, Zhang JC, Duan LS, Zhang MC, Li ZH (2016) Increased abscisic acid levels in transgenic maize overexpressing AtLOS5 mediated root ion fluxes and leaf water status under salt stress. J Exp Bot 67:1339–1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou BY, Guo ZF, Xing JP, Huang BR (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot 56:3223–3228

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Zuo M, Liang Y, Jiang M, Zhang J, Scheller HV, Tan M, Zhang A (2013) MAP65–1a positively regulates H2O2 amplification and enhances brassinosteroid-induced antioxidant defence in maize. J Exp Bot 64:3787–3802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Key Research and Development program of China (2016YFD0200108), the Fundamental National Key Project of Science and Technology (2014BAD14B02), the 948 Project from the Ministry of Agriculture of China (2016-X41) and the National Natural Science Foundation of China (Program No. 41771329).

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XS, CH and SW conceived the experiment. SW, SX and YX performed the experiment. SW, QT and XZ analyzed the data. SW and XS wrote the manuscript.

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Correspondence to Xuecheng Sun.

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The authors declare that they have no conflict of interest.

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Communicated by Qiaochun Wang.

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Wu, S., Hu, C., Tan, Q. et al. Nitric oxide acts downstream of abscisic acid in molybdenum-induced oxidative tolerance in wheat. Plant Cell Rep 37, 599–610 (2018). https://doi.org/10.1007/s00299-018-2254-0

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  • DOI: https://doi.org/10.1007/s00299-018-2254-0

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