Abstract
Abiotic stresses, including drought, detrimentally affect the growth and productivity of many economically important crop plants, leading to significant yield losses, which can result in food shortages and threaten the sustainability of agriculture. Balancing plant growth and stress responses is one of the most important functions of agricultural application to optimize plant production. In this study, we initially report that copper nanoparticle priming positively regulates drought stress responses in maize. The copper nanoparticle priming plants displayed enhanced drought tolerance indicated by their higher leaf water content and plant biomass under drought as compared with water-treated plants. Moreover, our data showed that the treatment of copper nanoparticle on plants increased anthocyanin, chlorophyll and carotenoid contents compared to water-treated plants under drought stress conditions. Additionally, histochemical analyses with nitro blue tetrazolium and 3,3′-diaminobenzidine revealed that reactive oxygen species accumulation of priming plants was decreased as a result of enhancement of reactive oxygen species scavenging enzyme activities under drought. Furthermore, our comparative yield analysis data indicated applying copper nanoparticles to the plant increased total seed number and grain yield under drought stress conditions. Our data suggest that copper nanoparticle regulates plant protective mechanisms associated with drought tolerance, which is a promising approach for the production of drought-tolerant crop plants.
References
Ambrosini VG et al (2018) High copper content in vineyard soils promotes modifications in photosynthetic parameters and morphological changes in the root system of ‘Red Niagara’ plantlets. Plant Physiol Biochem 128:89–98. https://doi.org/10.1016/j.plaphy.2018.05.011
Arora S, Sharma P, Kumar S, Nayan R, Khanna PK, Zaidi MGH (2012) Gold-nanoparticle induced enhancement in growth and seed yield of Brassica juncea. Plant Growth Regul 66:303–310. https://doi.org/10.1007/s10725-011-9649-z
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Burke DJ et al (2015) Iron oxide and titanium dioxide nanoparticle effects on plant performance and root associated microbes. Int J Mol Sci 16:23630–23650. https://doi.org/10.3390/ijms161023630
Casimiro A, Arrabaça MC (2015) Effect of copper deficiency on photosynthesis in wheat. In: Sybesma C (ed) Advances in photosynthesis research. Advances in agricultural biotechnology, vol 4. Springer, Dordrecht, pp 435–437. https://doi.org/10.1007/978-94-017-4971-8_95
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. https://doi.org/10.1111/tpj.13299
Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26. https://doi.org/10.1016/S1360-1385(96)80019-7
Din MI, Arshad F, Hussain Z, Mukhtar M (2017) Green adeptness in the synthesis and stabilization of copper nanoparticles: catalytic, antibacterial, cytotoxicity, and antioxidant activities. Nanoscale Res Lett 12:638. https://doi.org/10.1186/s11671-017-2399-8
Drazkiewicz M, Skorzynska-Polit E, Krupa Z (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. Biometals 17:379–387. https://doi.org/10.1023/B:BIOM.0000029417.18154.22
Emiliani J, D’Andrea L, Lorena Falcone Ferreyra M, Maulion E, Rodriguez E, Rodriguez-Concepcion M, Casati P (2018) A role for beta, beta-xanthophylls in Arabidopsis UV-B photoprotection. J Exp Bot 69:4921–4933. https://doi.org/10.1093/jxb/ery242
Farooq MA et al (2019) Acquiring control: the evolution of ROS-Induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol Biochem 141:353–369. https://doi.org/10.1016/j.plaphy.2019.04.039
Gong F, Yang L, Tai F, Hu X, Wang W (2014) “Omics” of maize stress response for sustainable food production: opportunities and challenges. Omics 18:714–732. https://doi.org/10.1089/omi.2014.0125
Gururani MA, Venkatesh J, Tran LS (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
Ha CV et al (2013a) The auxin response factor transcription factor family in soybean: genome-wide identification and expression analyses during development and water stress. DNA Res 20:511–524. https://doi.org/10.1093/dnares/dst027
Ha CV, Le DT, Nishiyama R, Watanabe Y, Tran UT, Dong NV, Tran LS (2013b) Characterization of the newly developed soybean cultivar DT2008 in relation to the model variety W82 reveals a new genetic resource for comparative and functional genomics for improved drought tolerance. Biomed Res Int 2013:759657. https://doi.org/10.1155/2013/759657
Ha CV et al (2014a) Genome-wide identification and expression analysis of the CaNAC family members in chickpea during development, dehydration and ABA treatments. PLoS One 9:e114107. https://doi.org/10.1371/journal.pone.0114107
Ha CV et al (2014b) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA 111:851–856. https://doi.org/10.1073/pnas.1322135111
Hoang SA, Nguyen LQ, Nguyen NH, Tran CQ, Nguyen DV, Vu QN, Phan CM (2019) Metal nanoparticles as effective promotors for Maize production. Sci Rep 9:13925. https://doi.org/10.1038/s41598-019-50265-2
Hossain MA et al (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420. https://doi.org/10.3389/fpls.2015.00420
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:800. https://doi.org/10.3389/fpls.2019.00800
Karamanos RE, Pomarenski Q, Goh TB, Flore NA (2004) The effect of foliar copper application on grain yield and quality of wheat. Can J Plant Sci 84:47–56. https://doi.org/10.4141/P03-090
Latowski D, Kuczynska P, Strzalka K (2011) Xanthophyll cycle—a mechanism protecting plants against oxidative stress. Redox Rep 16:78–90. https://doi.org/10.1179/174329211x13020951739938
Le VD (2019) Nanoparticles for the improved crop production. In: Panpatte DG, Jhala YK (eds) Nanotechnology for agriculture: crop production & protection. Springer Singapore, Singapore, pp 85–106. https://doi.org/10.1007/978-981-32-9374-8_5
Li P, Li YJ, Zhang FJ, Zhang GZ, Jiang XY, Yu HM, Hou BK (2017) The Arabidopsis UDP-glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J 89:85–103. https://doi.org/10.1111/tpj.13324
Liu Y, He C (2016) Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Rep 35:995–1007. https://doi.org/10.1007/s00299-016-1950-x
Luo P et al (2016) Overexpression of Rosa rugosa anthocyanidin reductase enhances tobacco tolerance to abiotic stress through increased ROS scavenging and modulation of ABA signaling. Plant Sci 245:35–49. https://doi.org/10.1016/j.plantsci.2016.01.007
Mallarino AP, Enderson TJ, Haq MU (2014) Corn and soybean yield response to micronutrients fertilization. Integrated Crop Management Conference, Iowa State University, pp 129–136
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
Mochida K, Ha CV, Sulieman S, Nguyen DV, Tran L (2015) Databases of transcription factors in legumes. In: de Bruijn FJ (ed) Biological nitrogen fixation. Wiley, New York, pp 817–822. https://doi.org/10.1002/9781119053095.ch81
Mostofa MG, Hossain MA, Fujita M, Tran LS (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433. https://doi.org/10.1038/srep11433
Myers SS et al (2017) Climate change and global food systems: potential impacts on food security and undernutrition. Annu Rev Public Health 38:259–277. https://doi.org/10.1146/annurev-publhealth-031816-044356
Nakabayashi R et al (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379. https://doi.org/10.1111/tpj.12388
Ngo BQ, Dao TT, Nguyen CH, Tran XT, Nguyen TV, Khuu TD, Huynh TH (2014) Effects of nanocrystalline powders (Fe, Co and Cu) on the germination, growth, crop yield and product quality of soybean (Vietnamese species DT-51). Adv Nat Sci Nanosci Nanotechnol 5:015016. https://doi.org/10.1088/2043-6262/5/1/015016
Nguyen KH et al (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci USA 113:3090–3095. https://doi.org/10.1073/pnas.1600399113
Nguyen HM et al (2017) Ethanol enhances high-salinity stress tolerance by detoxifying reactive oxygen species in Arabidopsis thaliana and rice. Front Plant Sci 8:1001. https://doi.org/10.3389/fpls.2017.01001
Nguyen HM et al (2018a) Transcriptomic analysis of Arabidopsis thaliana plants treated with the Ky-9 and Ky-72 histone deacetylase inhibitors. Plant Signal Behav 13:e1448333. https://doi.org/10.1080/15592324.2018.1448333
Nguyen KH et al (2018b) The soybean transcription factor GmNAC085 enhances drought tolerance in Arabidopsis. Environ Exp Bot 151:12–20. https://doi.org/10.1016/j.envexpbot.2018.03.017
Osakabe Y, Osakabe K, Shinozaki K, Tran LS (2014) Response of plants to water stress. Front Plant Sci 5:86. https://doi.org/10.3389/fpls.2014.00086
Pei ZM et al (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734. https://doi.org/10.1038/35021067
Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R (2009) Starch grain and phytolith evidence for early ninth millennium B.P. maize from the Central Balsas River Valley, Mexico. Proc Natl Acad Sci USA 106:5019–5024. https://doi.org/10.1073/pnas.0812525106
Printz B et al (2016) Combining -omics to unravel the impact of copper nutrition on Alfalfa (Medicago sativa) stem metabolism. Plant Cell Physiol 57:407–422. https://doi.org/10.1093/pcp/pcw001
Regier N, Cosio C, von Moos N, Slaveykova VI (2015) Effects of copper-oxide nanoparticles, dissolved copper and ultraviolet radiation on copper bioaccumulation, photosynthesis and oxidative stress in the aquatic macrophyte Elodea nuttallii. Chemosphere 128:56–61. https://doi.org/10.1016/j.chemosphere.2014.12.078
Salemi FE, Esfahani MN, Tran LS (2019) Mechanistic insights into enhanced tolerance of early growth of alfalfa (Medicago sativa L.) under low water potential by seed-priming with ascorbic acid or polyethylene glycol solution. Ind Crops Prod 137:436–445. https://doi.org/10.1016/j.indcrop.2019.05.049
Savvides A, Ali S, Tester M, Fotopoulos V (2016) Chemical priming of plants against multiple abiotic stresses: mission possible? Trends Plant Sci 21:329–340. https://doi.org/10.1016/j.tplants.2015.11.003
Singh A, Singh NB, Hussain I, Singh H (2017a) Effect of biologically synthesized copper oxide nanoparticles on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var. botrytis. J Biotechnol 262:11–27. https://doi.org/10.1016/j.jbiotec.2017.09.016
Singh T, Shukla S, Kumar P, Wahla V, Bajpai VK (2017b) Application of nanotechnology in food science: perception and overview. Front Microbiol 8:1501. https://doi.org/10.3389/fmicb.2017.01501
Stevanovic M et al (2016) The impact of high-end climate change on agricultural welfare. Sci Adv 2:e1501452. https://doi.org/10.1126/sciadv.1501452
Tamez C, Morelius EW, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey J (2019) Biochemical and physiological effects of copper compounds/nanoparticles on sugarcane (Saccharum officinarum). Sci Total Environ 649:554–562. https://doi.org/10.1016/j.scitotenv.2018.08.337
Thangavelu RM, Gunasekaran D, Jesse DMI, Riyaz SUM, Sundarajan D, Krishnan K (2018) Nanobiotechnology approach using plant rooting hormone synthesized silver nanoparticle as “nanobullets” for the dynamic applications in horticulture—an in vitro and ex vitro study. Arab J Chem 11:48–61. https://doi.org/10.1016/j.arabjc.2016.09.022
Tran ML et al (2020) Metal-based nanoparticles enhance drought tolerance in soybean. J Nanomater 2020:4056563. https://doi.org/10.1155/2020/4056563
Usman M et al (2020) Nanotechnology in agriculture: current status, challenges and future opportunities. Sci Total Environ 721:137778. https://doi.org/10.1016/j.scitotenv.2020.137778
Utsumi Y et al (2019) Acetic acid treatment enhances drought avoidance in cassava (Manihot esculenta Crantz). Front Plant Sci 10:521. https://doi.org/10.3389/fpls.2019.00521
Viera I, Perez-Galvez A, Roca M (2019) Green natural colorants. Molecules. https://doi.org/10.3390/molecules24010154
Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718. https://doi.org/10.1111/j.1469-8137.2008.02431.x
Wang Z et al (2018) Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves. Biol Open 7:bio035279. https://doi.org/10.1242/bio.035279
Webber H et al (2018) Diverging importance of drought stress for maize and winter wheat in Europe. Nat Commun 9:4249. https://doi.org/10.1038/s41467-018-06525-2
Wheeler T, von Braun J (2013) Climate change impacts on global food security. Science 341:508–513. https://doi.org/10.1126/science.1239402
Xie X, He Z, Chen N, Tang Z, Wang Q, Cai Y (2019) The roles of environmental factors in regulation of oxidative stress in plant. Biomed Res Int 2019:9732325. https://doi.org/10.1155/2019/9732325
Xue Y et al (2014) Zinc, iron, manganese and copper uptake requirement in response to nitrogen supply and the increased grain yield of summer maize. PLoS One 9:e93895. https://doi.org/10.1371/journal.pone.0093895
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
Yamauchi Y (2018) Integrated chemical control of abiotic stress tolerance using biostimulants. In: Andjelkovic V (ed) Plant abiotic stress and responses to climate change. IntechOPen, London, pp 133–143. https://doi.org/10.5772/intechopen.74214
Acknowledgements
This project was supported by grants from project coded KHCN-TB.10C/13-18 to SH under the program titled “Science and Technology for the Sustainable Development of the Northwest Region” of Vietnam National University, Hanoi, Vietnam. We thank Veronica Lee, University of Missouri, Columbia, USA for her English editing.
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DN and CH designed research; CH, HN, NL, KN, HN, HL, AN, and ND, performed research; DN and SH contributed research materials, reagents and analytic tools; CH, NL, and HN analyzed the data; and HN, CH and DN wrote the manuscript.
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Van Nguyen, D., Nguyen, H.M., Le, N.T. et al. Copper Nanoparticle Application Enhances Plant Growth and Grain Yield in Maize Under Drought Stress Conditions. J Plant Growth Regul 41, 364–375 (2022). https://doi.org/10.1007/s00344-021-10301-w
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DOI: https://doi.org/10.1007/s00344-021-10301-w