Abstract
Drought is believed to cause many metabolic changes which affect plant growth and development. However, it might be mitigated by various inorganic substances, such as nitrogen. Thus, the study was carried out to investigate the effect of foliar-applied urea with or without urease inhibitor N-(n-butyl) thiophosphoric triamide (NBPT) on a maize cultivar under drought stress simulated by 15% (w/v) polyethylene glycol 6000. Foliar-applied urea resulted in a significant increase in plant dry weight, relative water content, and photosynthetic pigments under water stress condition. Furthermore, the activities of superoxide dismutase (SOD), peroxidase (POD), and hydrogen peroxidase (CAT), were enhanced with all spraying treatments under drought stress, which led to decreases in accumulation of hydrogen peroxide (H2O2), superoxide anion (\({\text{O}}_2^{ \cdot - }\)) and malondialdehyde (MDA). The contents of soluble protein and soluble sugar accumulated remarkably with urea-applied under drought stress condition. Moreover, a further enhancement in above metabolites was observed by spraying a mixture of urea and urease inhibitor as compared to urea sprayed only. Taken together, our findings show that foliar application of urea and a urease inhibitor could significantly enhance drought tolerance of maize through protecting photosynthetic apparatus, activating antioxidant defense system and improving osmoregulation.
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References
Abedi T, Pakniyat H (2010) Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech J Genet Plant Breed 46:27–34
Akram NA, Noreen S, Noreen T, Ashraf M (2015) Exogenous application of trehalose alters growth, physiology and nutrient composition in radish (Raphanus sativus L.) plants under water-deficit condition. Braz J Bot 38:431–439
Akram NA, Shafiq S, Ashraf M, Aisha R, Sajid MA (2016) Drought-induced anatomical changes in radish (Raphanus sativus L.) leaves supplied with trehalose through different modes. Arid Land Res Manag 30:412–420
Arjenaki FG, Jabbari R, Morshedi A (2012) Evaluation of drought stress on relative water content, chlorophyll content and mineral elements of wheat (Triticum aestivum L.) varieties. Int J Agric Crop Sci 4:726–729
Artola E, Cruchaga S, Ariz I, Moran JF, Garnica M, Houdusse F, Mina JMG, Irigoyen I, Lasa B, Aparicio-Tejo PM (2011) Effect of N-(n-butyl) thiophosphoric triamide on urea metabolism and the assimilation of ammonium by Triticum aestivum L. Plant Growth Regul 63:73–79
Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190
Blum A (2009) Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crop Res 112:119–123
Blum A (2016) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ. doi:10.1111/pce.12800
Bollard EG, Cook AR, Turner NA (1968) Urea as sole source of nitrogen for plant growth. Planta 83:1–12
Campos H, Cooper M, Habben JE, Edmeades GO, Schussler JR (2004) Improving drought tolerance in maize: a view from industry. Field Crop Res 90:19–34
Castillo FJ (1996) Antioxidative protection in the inducible CAM plant Sedum album L. following the imposition of severe water stress and recovery. Oecologia 107:469–477
Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29
Cohen DM (1996) Urea-inducible Egr-1 transcription in renal inner medullary collecting duct (mIMCD3) cells is mediated by extracellular signal-regulated kinase activation. Proc Natl Acad Sci USA 93:11242–11247
Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125:61–64
Croce R, Amerongen H (2014) Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10:492–501
Cruchaga S, Artola E, Lasa B, Ariz I, Irigoyen I, Moran JF, Aparicio-Tejo PM (2011) Short term physiological implications of NBPT application on the N metabolism of Pisum sativum and Spinacea oleracea. J Plant Physiol 168:329–336
Cunha JR, Neto MCL, Carvalho FE, Martins MO, Jardim-Messeder D, Margis-Pinheiro M, Silveira JA (2016) Salinity and osmotic stress trigger different antioxidant responses related to cytosolic ascorbate peroxidase knockdown in rice roots. Environ Exp Bot 131:58–67
Dawar KM (2010) The impacts of urease inhibitor and method of application on the bioavailability of urea fertilizer in ryegrass (Lolium perenne L.). PhD thesis. University of Canterbury, Christchurch, pp 49–71
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53–66
Del Amor FM, Cuadra-Crespo P (2011) Alleviation of salinity stress in broccoli using foliar urea or methyl-jasmonate: analysis of growth, gas exchange, and isotope composition. Plant Growth Regul 63:55–62
Demura T, Ye ZH (2010) Regulation of plant biomass production. Curr Opin Plant Biol 13:298–303
Doupis G, Bertaki M, Psarras G, Kasapakis I, Chartzoulakis K (2013) Water relations, physiological behavior and antioxidant defence mechanism of olive plants subjected to different irrigation regimes. Sci Hortic 153:150–156
Esmaeilpour A, Van Labeke MC, Van Damme P, Samson R (2014) Variation of relative water content, water use efficiency and stomatal density during drought stress and subsequent recovery in pistachio cultivars (Pistacia vera L.). XXIX Int Hortic Congr Hortic 1109:113–120
Ghobadi M, Taherabadi S, Ghobadi ME, Mohammadi GR, Jalali-Honarmand S (2013) Antioxidant capacity, photosynthetic characteristics and water relations of sunflower (Helianthus annuus L.) cultivars in response to drought stress. Ind Crop Prod 50:29–38
Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateshwarulu B, Shanker AK, Shanker C, Mandapaka M (eds) Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–315
Hasanuzzaman M, Nahar K, Gill SS, Fujita M (2013) Drought stress responses in plants, oxidative stress, and antioxidant defense. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley, Weinheim, pp 209–250
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:32
Houles V, Guerif M, Mary B (2007) Elaboration of a nitrogen nutrition indicator for winter wheat based on leaf area index and chlorophyll content for making nitrogen recommendations. Eur J Agron 27:1–11
Juan YH, Chen LJ, Wu ZJ, Wang R (2009) Kinetics of soil urease affected by urease inhibitors at contrasting moisture regimes. Rev Cienc Suelo Nutr 9:125–133
Kawakami EM, Oosterhuis DM, Snider JL (2013) Nitrogen assimilation and growth of cotton seedlings under NaCl salinity and in response to urea application with NBPT and DCD. J Agron Crop Sci 199:106–117
Kaya C, Higgs D (2003) Relationship between water use and urea application in salt-stressed pepper plants. J Plant Nutr 26:19–30
Kaya C, Ashraf M, Sönmez O, Tuna AL, Aydemir S (2015a) Exogenously applied nitric oxide confers tolerance to salinity-induced oxidative stress in two maizes (Zea mays L.) cultivars differing in salinity tolerance. Turk J Agric For 39:909–919
Kaya C, Sönmez O, Ashraf M, Polat T, Tuna L, Aydemir S (2015b) Exogenous application of nitric oxide and thiourea regulates on growth and some key physiological processes in maize (Zea mays L.) plants under saline stress. Soil Water J S:61–66
Ke D, Sun G, Wang Z (2007) Effects of superoxide radicals on ACC synthase activity in chilling-stressed etiolated mungbean seedlings. Plant Growth Regul 51:83–91
Kukreja S, Nandwal AS, Kumar N, Sharma SK, Unvi V, Sharma PK (2005) Plant water status, H2O2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biol Plant 49:305–308
Kumar GM, Knowles NR (1993) Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum) seed-tubers. Plant Physiol 102:115–124
Kumawat RN, Mahla HR (2015) Effect of foliar applied urea and planting pattern on the leaf pigments and yield of cluster bean (Cyamopsis tetragonoloba L.) grown in low rainfall areas of western India. Legum Res 38:96–100
Latif M, Akram NA, Ashraf M (2016) Regulation of some biochemical attributes in drought-stressed cauliflower (Brassica oleracea L.) by seed pre-treatment with ascorbic acid. J Hortic Sci Biotechnol 91:129–137
Levin NW, Folden T, Zhu F, Ronco C (2002) Dry weight determination. In: Hemodialysis technology, vol 137. Karger, Perugia, pp 272–278
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc T 11:591–592
Liu LH, Ludewig U, Frommer WB, von Wirén N (2003) AtDUR3 encodes a new type of high-affinity urea/H+ symporter in Arabidopsis. Plant Cell 15:790–800
Maleva M, Borisova G, Chukina N, Nekrasova G, Prasad MNV (2013) Influence of exogenous urea on photosynthetic pigments, 14CO2 uptake, and urease activity in Elodea densa-environmental implications. Environ Sci Pollut R 20:6172–6177
Maleva M, Borisova G, Chukina N, Prasad MNV (2015) Urea-induced oxidative damage in Elodea densa leaves. Environ Sci Pollut Res 22:13556–13563
McCue KF, Hanson AD (1990) Drought and salt tolerance: towards understanding and application. Trends Biotechnol 8:358–362
Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76
Menchyk N (2012) Foliar applied urea nitrogen metabolism in warm-season turfgrass under salinity stress. PhD thesis. Clemson University, Clemson
Meng Q, Hou P, Wu L, Chen X, Cui Z, Zhang F (2013) Understanding production potentials and yield gaps in intensive maize production in China. Field Crops Res 143:91–97
Mir MR, Khan NA, Bhat MA, Lone NA, Rather GH, Razivi SM, Bhat KA, Singh S, Payne WA (2010) Effect of ethrel spray and nitrogen on growth, photosynthesis, carboxylation efficiency and water use efficiency of mustard (Brassica juncea L.). Int J Curr Res 6:45–52
Mohammadkhani N, Heidari R (2007) Effects of drought stress on protective enzyme activities and lipid peroxidation in two maize cultivars. Pak J Biol Sci 10:3835–3840
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481
Muñoz-Muñoz, García-Molina JLF, García-Ruiz PA, Arribas E, Tudela J, García-Cánovas F, Rodriguez-Lopez JN (2009) Enzymatic and chemical oxidation of trihydroxylated phenols. Food Chem 113:435–444
Naylor AW (2012) Water deficits and nitrogen metabolism. In: Kozlowski TT (ed) Water deficits and plant growth. Academic Press, London, pp 241–254
Naz H, Akram NA, Ashraf M (2016) Impact of ascorbic acid on growth and physiology of cucumber (Cucumis sativus) plants under water-deficit condition. Pak J Bot 48:877–883
Padmavathi TA, Rao DM (2013) Differential accumulation of osmolytes in 4 cultivars of peanut (Arachis hypogaea L.) under drought stress. J Crop Sci Biotechnol 16:151–159
Pasqualini S, Cresti M, Del Casino C, Faleri C, Frenguelli G, Tedeschini E, Ederli L (2015) Roles for NO and ROS signaling in pollen germination and pollen-tube elongation in Cupressus arizonica. Biol Plant 59:735–744
Paździoch-Czochra M, Wideńska A (2002) Spectrofluorimetric determination of hydrogen peroxide scavenging activity. Anal Chim Acta 452:177–184
Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882
Quilot B, Génard M, Kervella J, Lescourret F (2004) Analysis of genotypic variation in fruit flesh total sugar content via an ecophysiological model applied to peach. Theor Appl Genet 109:440–449
Rajale GB, Prasad R (1974) Relative efficiency of urea, nitrification inhibitor treated urea and slow release nitrogen fertilizers for rice (Oryza sativa L.). J Agric Sci 83:303–308
Rajasekar M, Rabert GA, Manivannan P (2015) The effect of triazole induced photosynthetic pigments and biochemical constituents of Zea mays L. (maize) under drought stress. Appl Nano Sci 6:727–735
Rasheed R, Wahid A, Farooq M, Hussain I, Basra SM (2011) Role of proline and glycinebetaine pretreatments in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds. Plant Growth Regul 65:35–45
Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen relationships: interpretation of different patterns between Pseudotsugamen ziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiol 23:137–144
Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163:1037–1046
Shafiq S, Akram NA, Ashraf M (2015) Does exogenously-applied trehalose alter oxidative defense system in the edible part of radish (Raphanus sativus L.) under water-deficit conditions? Sci Hortic 185:68–75
Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–25
Shivay YS, Prasad R (2012) Zinc-coated urea improves productivity and quality of basmati rice (Oryza sativa L.) under zinc stress condition. J Plant Nutr 35:928–951
Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216
Stiegler JC, Richardson MD, Karcher DE (2011) Foliar nitrogen uptake following urea application to putting green turfgrass species. Crop Sci 51:1253–1260
Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486
Talbi S, Romero-Puertas MC, Hernández A, Terrón L, Ferchichi A, Sandalio LM (2015) Drought tolerance in a Saharian plant Oudneya africana: role of antioxidant defences. Environ Exp Bot 111:114–126
Tarighaleslami M, Zarghami R, Boojar MMA, Oveysi M (2012) Effects of drought stress and different nitrogen levels on morphological traits of proline in leaf and protein of corn seed (Zea mays L.). Am Eur J Agric Environ Sci 12:49–56
Von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1057
Wang CY (1995) Effect of temperature preconditioning on catalase, peroxidase, and superoxide dismutase in chilled zucchini squash. Postharvest Biol Technol 5:67–76
Wang WB, Kim YH, Lee HS, Kim KY, Deng XP, Kwak SS (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577
Watson CJ, Miller H (1996) Short-term effects of urea amended with the urease inhibitor N-(n-butyl) thiophosphoric triamide on perennial ryegrass. Plant Soil 184:33–45
Witte CP, Tiller SA, Taylor MA, Davies HV (2002) Leaf urea metabolism in potato. Urease activity profile and patterns of recovery and distribution of 15N after foliar urea application in wild-type and urease-antisense transgenics. Plant Physiol 128:1129–1136
Wu F, Bao W, Li F, Wu N (2008) Effects of drought stress and N supply on the growth, biomass partitioning and water-use efficiency of Sophora davidii seedlings. Environ Exp Bot 63:248–255
Xie J (2009) Addressing China’s water scarcity: recommendations for selected water resource management issues. World Bank, Washington
Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222
Yang F, Miao LF (2010) Adaptive responses to progressive drought stress in two poplar species originating from different altitudes. Silva Fenn 44:23–37
Yasmeen A, Basra S, Wahid A, Farooq M, Nouman W, Hussain N (2013) Improving drought resistance in wheat (Triticum aestivum) by exogenous application of growth enhancers. Int J Agric Biol 15:1307–1312
Younis ME, Hasaneen MN, Ahmed AR, El-Bialy DM (2009) Plant growth, metabolism and adaptation in relation to stress condition. XXI. Reversal of harmful NaCl-effects in lettuce plants by foliar application with urea. Aust J. Crop Sci 3:83–95
Yuan J, Li J, Zhao A, Cao G, Wang H, Liu H, Luo C (2013) Effects of different fertilities on the antioxidant enzyme activities and chlorophyll content of radix Pseudostellariae. Med Plant 4:37–40
Zaman M, Zaman S, Adhinarayanan C, Nguyen ML, Nawaz S, Dawar KM (2013) Effects of urease and nitrification inhibitors on the efficient use of urea for pastoral systems. Soil Sci Plant Nutr 59:649–659
Zanin L, Tomasi N, Zamboni A, Varanini Z, Pinton R (2015) The urease inhibitor NBPT negatively affects DUR3-mediated uptake and assimilation of urea in maize roots. Front Plant Sci 6:1007–1019
Zhang L, Li S, Liang Z, Li S (2009) Effect of foliar nitrogen application on nitrogen metabolism, water status, and plant growth in two maize cultivars under short-term moderate stress. J Plant Nutr 32:1861–1881
Zhang LX, Wang K, Zhao YG, Zhai YY, Gao M, An ZF, Liu JC, Hu JJ (2012a) Foliar urea application affects nitric oxide burst and glycinebetaine metabolism in two maize cultivars under drought. Pak J Bot 44:81–86
Zhang LX, Zhai YY, Li YF, Zhao YG, Lv LX, Gao M, Liu JC, Hu JJ (2012b) Effects of nitrogen forms and drought stress on growth, photosynthesis and some physico-chemical properties of stem juice of two maize cultivars (Zea mays L.) at elongation stage. Pak J Bot 44:1405–1412
Zhang LX, Zheng P, Ruan Z, Tian L, Ashraf M (2015) Nitric oxide accumulation and glycinebetaine metabolism in two osmotically stressed maize cultivars supplied with different nitrogen forms. Biol Plant 59:183–186
Zhao WY, Xu S, Li JL, Cui LJ, Chen YN, Wang JZ (2008) Effects of foliar application of nitrogen on the photosynthetic performance and growth of two fescue cultivars under heat stress. Biol Plant 52:113–116
Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159
Acknowledgements
This research was supported by the Foundation of State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau (A314021402-1514), China Postdoctoral Science Foundation (QN2009069) and Sci-tech Development Foundation of NWSUAF (A2990215264). WG, PFZ and LT contributed equally to this work.
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Gou, W., Zheng, P., Tian, L. et al. Exogenous application of urea and a urease inhibitor improves drought stress tolerance in maize (Zea mays L.). J Plant Res 130, 599–609 (2017). https://doi.org/10.1007/s10265-017-0933-5
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DOI: https://doi.org/10.1007/s10265-017-0933-5