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Molybdenum Application Regulates Oxidative Stress Tolerance in Winter Wheat Under Different Nitrogen Sources

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Abstract

Molybdenum (Mo), an essential microelement, may enhance the oxidative stress tolerance in plants. However, the efficacy of Mo might be variable with different forms of nitrogen (N) fertilizer. The present study was conducted to investigate the role of Mo application in regulating oxidative stress tolerance in winter wheat under different N sources. A hydroponic study was carried out comprising of two winter wheat cultivars ‘97003’ and ‘97014’ as Mo efficient and Mo inefficient, respectively, under two Mo levels (0 and 1 μM) and three different N sources (NO3̶, NH4NO3, or NH4+). Winter wheat plants supplied with different N sources accumulated superoxide anions (O2), and malonaldehyde (MDA) contents in the order of NH4+ > NO3̶ > NH4NO3, suggesting that sole application of either N sources, especially sole NH4+ source, may induce oxidative stress in winter wheat. However, Mo application decreased the MDA contents by 20.02%, 15.11%, and 25.89% in Mo-efficient cultivar and 30.75%, 23.79%, and 37.76% in Mo-inefficient cultivar under NO3̶, NH4NO3, and NH4+ sources, respectively, while increased antioxidant enzyme activities and carotenoids and abscisic acid (ABA) contents up-regulated the expressions of TaAO and TaAba3 genes. Mo application regulated oxidative stress tolerance in winter wheat under different N sources through enhancing ABA production and ROS-scavenging enzymes. Mo-efficient ‘97003’ winter wheat cultivar possesses a wider range of adaptability to withstand Mo-deficient conditions than Mo-inefficient ‘97014’ cultivar.

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References

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141(2):391–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5(2):28

    PubMed  PubMed Central  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159(6):567–584

    CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2013) Ecological significance and complexity of N-source preference in plants. Ann Bot 112(6):957–963

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125(1):61–64

    CAS  PubMed  PubMed Central  Google Scholar 

  • Downton W, Loveys B, Grant W (1988) Non-uniform stomatal closure induced by water stress causes putative non-stomatal inhibition of photosynthesis. New Phytol 110(4):503–509

    Google Scholar 

  • Drath M, Kloft N, Batschauer A, Marin K, Novak J, Forchhammer K (2008) Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 147(1):206–215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2010) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28(8):1056–1071

    Google Scholar 

  • Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24(16):1695–1708

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain S, Khan F, Cao W, Wu L, Geng M (2016) Seed priming alters the production and detoxification of reactive oxygen intermediates in rice seedlings grown under sub-optimal temperature and nutrient supply. Front Plant Sci 7(116)

  • Hussain S, Khaliq A, Noor MA, Tanveer M, Hussain HA, Hussain S, Shah T, Mehmood T (2020) Metal toxicity and nitrogen metabolism in plants: an overview. In: Carbon and Nitrogen Cycling in Soil. Springer, pp 221–248

  • Imran M, Hu C, Hussain S, Rana MS, Riaz M, Afzal J, Aziz O, Elyamine AM, Ismael MAF, Sun X (2019a) Molybdenum-induced effects on photosynthetic efficacy of winter wheat (Triticum aestivum L.) under different nitrogen sources are associated with nitrogen assimilation. Plant Physiol Biochem 141:154–163

    CAS  PubMed  Google Scholar 

  • Imran M, Sun X, Hussain S, Ali U, Rana MS, Rasul F, Saleem MH, Moussa MG, Bhantana P, Afzal J (2019b) Molybdenum-induced effects on nitrogen metabolism enzymes and elemental profile of winter wheat (Triticum aestivum L.) under different nitrogen sources. Int J Mol Sci 20(12):3009

    CAS  PubMed Central  Google Scholar 

  • Kovács B, Puskás-Preszner A, Huzsvai L, Lévai L, Bódi É (2015) Effect of molybdenum treatment on molybdenum concentration and nitrate reduction in maize seedlings. Plant Physiol Biochem 96:38–44

    PubMed  Google Scholar 

  • Li B, Li Q, Xiong L, Kronzucker HJ, Krämer U, Shi W (2012) Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress. Plant Physiol 160(4):2040–2051

    CAS  PubMed  PubMed Central  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 Biotech J 11(6):747–758

    CAS  Google Scholar 

  • Li B, Li G, Kronzucker HJ, Baluška F, Shi W (2014) Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends Plant Sci 19(2):107–114

    CAS  PubMed  Google Scholar 

  • Liu L, Xiao W, Li L, Li D-M, Gao D-S, Zhu C-y FX-L (2017) Effect of exogenously applied molybdenum on its absorption and nitrate metabolism in strawberry seedlings. Plant Physiol Biochem 115:200–211

    CAS  PubMed  Google Scholar 

  • Lu C, Zhang J (2000) Photosynthetic CO(2) assimilation, chlorophyll fluorescence and photoinhibition as affected by nitrogen deficiency in maize plants. Plant Sci 151(2):135–143

    CAS  PubMed  Google Scholar 

  • Marschner H (2012) Mineral nutrition of higher plants. J Ecol 76(4):1250

    Google Scholar 

  • Mccourt P, Creelman R (2008) The ABA receptors -- we report you decide. Curr Opin Plant Biol 11(5):474–478

    CAS  PubMed  Google Scholar 

  • Meng ZB, Chen LQ, Suo D, Li GX, Tang CX, Zheng SJ (2012) Nitric oxide is the shared signalling molecule in phosphorus- and iron-deficiency-induced formation of cluster roots in white lupin (Lupinus albus). Ann Bot 109(6):1055–1064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mohanty P (2004) Defense potentials to NaCl in a mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 161(5):531–542

    PubMed  Google Scholar 

  • Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radic Res Comm 28(6):659–671

    CAS  Google Scholar 

  • Müge O (2014) Reactive oxygen species: the good, the bad, and the enigma. Mol Cell Oncol 1(3)

  • Nie Z, Hu C, Tan Q, Sun X (2016) Gene expression related to molybdenum enzyme biosynthesis in response to molybdenum deficiency in winter wheat. J Soil Sci Plant Nutr 16(4):979–990

    CAS  Google Scholar 

  • Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ 33(9):1486–1501

    CAS  PubMed  PubMed Central  Google Scholar 

  • Podgórska A, Gieczewska K, Ł-K K, Rasmusson AG, Gardeström P, Szal B (2013) Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)(+) ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity. Plant Cell Environ 36(11):2034–2045

    PubMed  Google Scholar 

  • Polesskaya OG, Kashirina EI, Alekhina ND (2004) Changes in the activity of antioxidant enzymes in wheat leaves and roots as a function of nitrogen source and supply. Russ J Plant Physiol 51(5):615–620

    CAS  Google Scholar 

  • Raven JA (2010) Tansley review no. 2. Regulation of pH and generation of osmolarity in vascular plants: a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol 101(1):25–77

    Google Scholar 

  • Santos RL, Freire FJ, Oliveira ECA, Simões Neto DE, Medeiros MRFA, Bezerra PC, Moura MJA, Barbosa JA, Lopes NRC, Santos NL (2018) Productivity and technological quality of sugarcane under fertilization of nitrogen and molybdenum. J Soil Sci Plant Nutr 18(4):1002–1020

    Google Scholar 

  • Seo M, Peeters AJ, Koiwai H, Oritani T, Marion-Poll A, Zeevaart JA, 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. Proc Natl Acad Sci U S A 97(23):12908–12913

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su C-L, Zhang F-M, Sun K, Zhang W, Dai C-C (2019) Fungal endophyte Phomopsis liquidambari improves iron and molybdenum nutrition uptake of peanut in consecutive monoculture soil. J Soil Sci Plant Nutr 19(1):71–80

    CAS  Google Scholar 

  • Sun X, Hu C, Tan Q, Liu J, Liu H (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 104(2):345–356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Gao J, Tian Z, Liu Y, Abid M, Jiang D, Cao W, Dai T (2016) Adaptation to rhizosphere acidification is a necessary prerequisite for wheat (Triticum aestivum L.) seedling resistance to ammonium stress. Plant Physiol Biochem 108:447–455

    CAS  PubMed  Google Scholar 

  • Wang F, Gao J, Shi S, He X, Dai T (2018) Impaired electron transfer accounts for the photosynthesis inhibition in wheat seedlings (Triticum aestivum L.) subjected to ammonium stress. Physiol Plant 167(2):159–172

    PubMed  Google Scholar 

  • Wen X, Hu C, Sun X, Zhao X, Tan Q (2019) Research on the nitrogen transformation in rhizosphere of winter wheat (Triticum aestivum) under molybdenum addition. Environ Sci Pollut Res 26(3):2363–2374

    CAS  Google Scholar 

  • Wu S, Hu C, Tan Q, Nie Z, Sun X (2014) Effects of molybdenum on water utilization, antioxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum L.) under drought stress. Plant Physiol Biochem 83:365–374

    CAS  PubMed  Google Scholar 

  • Wu S, Hu C, Tan Q, Xu S, Sun X (2017) Nitric oxide mediates molybdenum-induced antioxidant defense in wheat under drought stress. Front Plant Sci 8:1085

    PubMed  PubMed Central  Google Scholar 

  • Wu S, Hu C, Tan Q, Zhao X, Xu S, Xia Y, Sun X (2018) Nitric oxide acts downstream of abscisic acid in molybdenum-induced oxidative tolerance in wheat. Plant Cell Rep 37(4):599–610

    CAS  PubMed  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu J-K (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress–and osmotic stress–responsive gene expression. Plant Cell 13(9):2063–2083

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(1):165–183

    Google Scholar 

  • Yang L, Sun J, Tian Z, Hakeem A, Feng W, Dong J, Cao W, Adkins SW, Dai T (2016) Physiological responses of wheat (Triticum aestivum L.) germination to elevated ammonium concentrations: reserve mobilization, sugar utilization, and antioxidant metabolism. Plant Growth Reg 81(2):1–12

    CAS  Google Scholar 

  • Zdunek-Zastocka E (2008) Molecular cloning, characterization and expression analysis of three aldehyde oxidase genes from Pisum sativum L. Plant Physiol Biochem 46(1):19–28

    CAS  PubMed  Google Scholar 

  • Zhang M, Hu C, Zhao X, Tan Q, Sun X, Cao A, 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(1–2):375–383

    CAS  Google Scholar 

  • Zou N, Li B, Dong G, Kronzucker HJ, Shi W (2012) Ammonium-induced loss of root gravitropism is related to auxin distribution and TRH1 function, and is uncoupled from the inhibition of root elongation in Arabidopsis. J Exp Bot 63(10):3777–3788

    CAS  PubMed  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (Program No. 41771329) and the 948 Project from the Ministry of Agriculture of China (2016-X41).

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Correspondence to Chengxiao Hu.

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Imran, M., Sun, X., Hussain, S. et al. Molybdenum Application Regulates Oxidative Stress Tolerance in Winter Wheat Under Different Nitrogen Sources. J Soil Sci Plant Nutr 20, 1827–1837 (2020). https://doi.org/10.1007/s42729-020-00254-6

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