Maize (Zea mays L.) is one of the most widely grown cereals in the world. Its cultivation is affected by abiotic stress caused by climate change, in particular, drought. Zinc (Zn) supplied by foliar nutrition can increase plant resistance to water stress by enhancing physiological and enzymatic antioxidant defence mechanisms. One of the possibilities to reduce the effect of drought on plant production is also the utilization of trehalose. In order to confirm the effect of the foliar application of selected forms of Zn (0.1% w/v solution)-zinc oxide micro- (ZnO) and nanoparticles (ZnONP), zinc sulphate (ZnSO4) and zinc chelate (ZnEDTA)-a pot experiment in controlled conditions was conducted in combination with trehalose (1% w/v solution) on selected growth parameters of maize exposed to the drought stress. A significant effect of coapplication of Zn and trehalose on chlorophyll content, chlorophyll fluorescence parameters, root electrical capacity, weight of maize aboveground biomass (AGB) and Zn content in AGB was found. At the same time, the hypothesis of a positive effect of carbohydrates on increasing the uptake of foliar-applied Zn was confirmed, especially for the ZnEDTA and ZnSO4. This paper presents the first empirical evidence of the trehalose addition to sprays for zinc foliar fertilization of maize proving to be an effective way of increasing the resistance of maize grown under drought stress conditions.

Department of Agrochemistry Soil Science Microbiology and Plant Nutrition Faculty of AgriScience Mendel University in Brno Zemědělská 1 61300 Brno Czech Republic

Zobrazit více v PubMed

Cairns J.E., Sanchez C., Vargas M., Ordoñez R., Araus J.L. Dissecting Maize Productivity: Ideotypes Associated with Grain Yield under Drought Stress and Well-watered Conditions. J. Integr. Plant Biol. 2012;54:1007–1020. doi: 10.1111/j.1744-7909.2012.01156.x. PubMed DOI

Waraich E.A., Ahmad R., Saifullah, Ashraf M.Y. Ehsanullah Role of mineral nutrition in alleviation of drought stress in plants. Aust. J. Crop Sci. 2011;5:764–777. doi: 10.1007/BF00581171. DOI

Bista D.R., Heckathorn S.A., Jayawardena D.M., Mishra S., Boldt J.K. Effects of Drought on Nutrient Uptake and the Levels of Nutrient-Uptake Proteins in Roots of Drought-Sensitive and -Tolerant Grasses. Plants. 2018;7:28. doi: 10.3390/plants7020028. PubMed DOI PMC

Hassan M.U., Aamer M., Chattha M.U., Haiying T., Shahzad B., Barbanti L., Nawaz M., Rasheed A., Afzal A., Liu Y., et al. The Critical Role of Zinc in Plants Facing the Drought Stress. Agriculture. 2020;10:396. doi: 10.3390/agriculture10090396. DOI

Alloway B.J. Soil factors associated with zinc deficiency in crops and humans. Environ. Geochem. Health. 2009;31:537–548. doi: 10.1007/s10653-009-9255-4. PubMed DOI

Sadeghzadeh B. A review of zinc nutrition and plant breeding. J. Soil Sci. Plant Nutr. 2013;13:907–927. doi: 10.4067/S0718-95162013005000072. DOI

Noulas C., Tziouvalekas M., Karyotis T. Zinc in soils, water and food crops. J. Trace Elem. Med. Biol. 2018;49:252–260. doi: 10.1016/j.jtemb.2018.02.009. PubMed DOI

Singh B., Natesan S.K.A., Singh B.K., Usha K. Improving zinc efficiency of cereals under zinc deficiency. Curr. Sci. 2005;88:36–44.

Subbaiah L.V., Prasad T.N.V.K.V., Krishna T.G., Sudhakar P., Reddy B.R., Pradeep T. Novel Effects of Nanoparticulate Delivery of Zinc on Growth, Productivity, and Zinc Biofortification in Maize (Zea mays L.) J. Agric. Food Chem. 2016;64:3778–3788. doi: 10.1021/acs.jafc.6b00838. PubMed DOI

Ivanov K., Vasilev A., Mitkov A., Nguyen N., Tonev T. Application of Zn-containing foliar fertilisers for recovery of the grain productivity potential of Zn-deficient maize plants. Ital. J. Agron. 2021;16 doi: 10.4081/ija.2021.1759. DOI

Anees M.A., Ali A., Shakoor U., Ahmed F., Hasnain Z., Hussain A. Foliar applied potassium and zinc enhances growth and yield performance of maize under rainfed conditions. Int. J. Agric. Biol. 2016;18:1025–1032. doi: 10.17957/IJAB/15.0204. DOI

González-Caballo P., Barrón V., Torrent J., del Campillo M.C., Sánchez-Rodríguez A.R. Wheat and Maize Grown on Two Contrasting Zinc-deficient Calcareous Soils Respond Differently to Soil and Foliar Application of Zinc. J. Soil Sci. Plant Nutr. 2022;22:1718–1731. doi: 10.1007/s42729-022-00766-3. DOI

Imran M., Rehim A. Zinc fertilization approaches for agronomic biofortification and estimated human bioavailability of zinc in maize grain. Arch. Agron. Soil Sci. 2017;63:106–116. doi: 10.1080/03650340.2016.1185660. DOI

Umar W., Hameed M.K., Aziz T., Maqsood M.A., Bilal H.M., Rasheed N. Synthesis, characterization and application of ZnO nanoparticles for improved growth and Zn biofortification in maize. Arch. Agron. Soil Sci. 2020;67:1164–1176. doi: 10.1080/03650340.2020.1782893. DOI

Shao J., Wu W., Rasul F., Munir H., Huang K., Awan M.I., Albishi T.S., Arshad M., Hu Q., Huang G., et al. Trehalose induced drought tolerance in plants: Physiological and molecular responses. Not. Bot. Horti Agrobot. Cluj-Napoca. 2022;50:12584. doi: 10.15835/nbha50112584. DOI

Jain N.K., Roy I. Effect of trehalose on protein structure. Protein Sci. 2009;18:24–36. doi: 10.1002/pro.3. PubMed DOI PMC

Bianchi G., Gamba A., Limiroli R., Pozzi N., Elster R., Salamini F., Bartels D. The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol. Plant. 1993;87:223–226. doi: 10.1111/j.1399-3054.1993.tb00146.x. DOI

Lunn J.E., Delorge I., Figueroa C.M., Van Dijck P., Stitt M. Trehalose metabolism in plants. Plant J. 2014;79:544–567. doi: 10.1111/tpj.12509. PubMed DOI

Richards A.B., Krakowka S., Dexter L.B., Schmid H., Wolterbeek A.P.M., Waalkens-Berendsen D.H., Shigoyuki A., Kurimoto M. Trehalose: A review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem. Toxicol. 2002;40:871–898. doi: 10.1016/S0278-6915(02)00011-X. PubMed DOI

Crowe J.H. Trehalose as a “chemical chaperone”: Fact and fantasy. Mol. Asp. Stress Response Chaperones Membr. Netw. 2007;594:143–158. doi: 10.1007/978-0-387-39975-1. PubMed DOI

Pereira C.S., Lins R.D., Chandrasekhar I., Freitas L.C.G., Hünenberger P.H. Interaction of the Disaccharide Trehalose with a Phospholipid Bilayer: A Molecular Dynamics Study. Biophys. J. 2004;86:2273–2285. doi: 10.1016/S0006-3495(04)74285-X. PubMed DOI PMC

Crowe J.H., Carpenter J.F., Crowe L.M. The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 1998;60:73–103. doi: 10.1146/annurev.physiol.60.1.73. PubMed DOI

Akram N.A., Noreen S., Noreen T., Ashraf M. Exogenous application of trehalose alters growth, physiology and nutrient composition in radish (Raphanus sativus L.) plants under water-deficit conditions. Braz. J. Bot. 2015;38:431–439. doi: 10.1007/s40415-015-0149-7. DOI

Alam M.M., Nahar K., Hasanuzzaman M., Fujita M. Trehalose-induced drought stress tolerance: A comparative study among different Brassica species. Plant Omics. 2014;7:271–283.

Ali Q., Ashraf M. Induction of Drought Tolerance in Maize (Zea mays L.) due to Exogenous Application of Trehalose: Growth, Photosynthesis, Water Relations and Oxidative Defence Mechanism. J. Agron. Crop Sci. 2011;197:258–271. doi: 10.1111/j.1439-037X.2010.00463.x. DOI

Ibrahim H.A., Abdellatif Y.M.R. Effect of maltose and trehalose on growth, yield and some biochemical components of wheat plant under water stress. Ann. Agric. Sci. 2016;61:267–274. doi: 10.1016/j.aoas.2016.05.002. DOI

Shafiq S., Akram N.A., Ashraf M. Does exogenously-applied trehalose alter oxidative defense system in the edible part of radish (Raphanus sativus L.) under water-deficit conditions? Sci. Hortic. 2015;185:68–75. doi: 10.1016/j.scienta.2015.01.010. DOI

Zulfiqar F., Chen J., Finnegan P.M., Younis A., Nafees M., Zorrig W., Hamed K.B. Application of Trehalose and Salicylic Acid Mitigates Drought Stress in Sweet Basil and Improves Plant Growth. Plants. 2021;10:1078. doi: 10.3390/plants10061078. PubMed DOI PMC

Goltsev V.N., Kalaji H.M., Paunov M., Bąba W., Horaczek T., Mojski J., Kociel H., Allakhverdiev S.I. Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ. J. Plant Physiol. 2016;63:869–893. doi: 10.1134/S1021443716050058. DOI

Chloupek O., Dostál V., Středa T., Psota V., Dvořáčková O. Drought tolerance of barley varieties in relation to their root system size. Plant Breed. 2010;129:630–636. doi: 10.1111/j.1439-0523.2010.01801.x. DOI

Cseresnyés I., Vozáry E., Rajkai K. Does electrical capacitance represent roots in the soil? Acta Physiol. Plant. 2020;42:1–6. doi: 10.1007/s11738-020-03061-9. DOI

Cseresnyés I., Takács T., Végh K.R., Anton A., Rajkai K. Electrical impedance and capacitance method: A new approach for detection of functional aspects of arbuscular mycorrhizal colonization in maize. Eur. J. Soil Biol. 2013;54:25–31. doi: 10.1016/j.ejsobi.2012.11.001. DOI

Heitholt J.J., Sloan J.J., MacKown C.T. Copper, manganese, and zinc fertilization effects on growth of soybean on a calcareous soil. J. Plant Nutr. 2002;25:1727–1740. doi: 10.1081/PLN-120006054. DOI

Mosaad I. Influence of integrated in-soil zinc application and organic fertilization on yield, nitrogen uptake and nitrogen use efficiency of rice. Egypt. J. Soil Sci. 2019;59:241–250. doi: 10.21608/ejss.2019.13349.1277. DOI

Hesse H., Trachsel N., Suter M., Kopriva S., Von Ballmoos P., Rennenberg H., Brunold C. Effect of glucose on assimilatory sulphate reduction in Arabidopsis thaliana roots. J. Exp. Bot. 2003;54:1701–1709. doi: 10.1093/jxb/erg177. PubMed DOI

Smoleń S., Sady W. Effect of foliar application of urea, molybdenum, benzyladenine, sucrose and salicylic acid on yield, nitrogen metabolism of radish plants and quality of edible roots. J. Plant Nutr. 2012;35:1113–1129. doi: 10.1080/01904167.2012.676125. DOI

Kumar A.M., Schaub U., Söll D., Ujwal M.L. Glutamyl-transfer RNA: At the crossroad between chlorophyll and protein biosynthesis. Trends Plant Sci. 1996;1:371–376. doi: 10.1016/S1360-1385(96)80311-6. DOI

Sadak M.S. Mitigation of drought stress on Fenugreek plant by foliar application of trehalose. Int. J. ChemTech Res. 2016;9:147–155.

Zhou W., Liang X., Zhang Y., Dai P., Liang B., Li J., Sun C., Lin X. Role of sucrose in modulating the low-nitrogen-induced accumulation of phenolic compounds in lettuce (Lactuca sativa L.) J. Sci. Food Agric. 2020;100:5412–5421. doi: 10.1002/jsfa.10592. PubMed DOI

Alexander A., Hunsche M. Influence of formulation on the cuticular penetration and on spray deposit properties of manganese and zinc foliar fertilizers. Agronomy. 2016;6:39. doi: 10.3390/agronomy6030039. DOI

Fernandez V., Eichert T. Uptake of hydrophilic solutes through plant leaves: Current state of knowledge and perspectives of foliar fertilization. Crit. Rev. Plant Sci. 2009;28:36–68. doi: 10.1080/07352680902743069. DOI

Alloway B.J. Zinc in Soils and Crop Nutrition. 2nd ed. Springer; Brussels, Belgium: 2008.

Xia H., Xue Y., Liu D., Kong W., Xue Y., Tang Y., Li J., Li D., Mei P. Rational Application of Fertilizer Nitrogen to Soil in Combination with Foliar Zn Spraying Improved Zn Nutritional Quality of Wheat Grains. Front. Plant Sci. 2018;9:677. doi: 10.3389/fpls.2018.00677. PubMed DOI PMC

Zhao A.Q., Tian X.H., Cao Y.X., Lu X.C., Liu T. Comparison of soil and foliar zinc application for enhancing grain zinc content of wheat when grown on potentially zinc-deficient calcareous soils. J. Sci. Food Agric. 2014;94:2016–2022. doi: 10.1002/jsfa.6518. PubMed DOI

Fernández V., Bahamonde H.A., Peguero-Pina J.J., Gil-Pelegrín E., Sancho-Knapik D., Gil L., Goldbach H.E., Eichert T. Physico-chemical properties of plant cuticles and their functional and ecological significance. J. Exp. Bot. 2017;68:5293–5306. doi: 10.1093/jxb/erx302. PubMed DOI

Roosta H.R., Estaji A., Niknam F. Effect of iron, zinc and manganese shortage-induced change on photosynthetic pigments, some osmoregulators and chlorophyll fluorescence parameters in lettuce. Photosynthetica. 2018;56:606–615. doi: 10.1007/s11099-017-0696-1. DOI

Pilon-Smits E.A.H., Terry N., Sears T., Kim H., Zayed A., Hwang S., Van Dun K., Voogd E., Verwoerd T.C., Krutwagen R.W.H.H., et al. Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J. Plant Physiol. 1998;152:525–532. doi: 10.1016/S0176-1617(98)80273-3. DOI

Roger M.J.R., Weiss O. Fluorescence techniques. In: Roger M.J.R., editor. Handbook of Plant Ecophisiolgy Techniques. Kluwer Academic Publishers; Dordrecht, The Netherlands: 2001. pp. 155–171.

Cherif J., Derbel N., Nakkach M., von Bergmann H., Jemal F., Lakhdar Z.B. Analysis of in vivo chlorophyll fluorescence spectra to monitor physiological state of tomato plants growing under zinc stress. J. Photochem. Photobiol. B Biol. 2010;101:332–339. doi: 10.1016/j.jphotobiol.2010.08.005. PubMed DOI

Yusefi-Tanha E., Fallah S., Rostamnejadi A., Pokhrel L.R. Responses of soybean (Glycine max [L.] Merr.) to zinc oxide nanoparticles: Understanding changes in root system architecture, zinc tissue partitioning and soil characteristics. Sci. Total Environ. 2022;835:155348. doi: 10.1016/j.scitotenv.2022.155348. PubMed DOI

Moghaddasi S., Fotovat A., Khoshgoftarmanesh A.H., Karimzadeh F., Khazaei H.R., Khorassani R. Bioavailability of coated and uncoated ZnO nanoparticles to cucumber in soil with or without organic matter. Ecotoxicol. Environ. Saf. 2017;144:543–551. doi: 10.1016/j.ecoenv.2017.06.074. PubMed DOI

Doolette C.L., Read T.L., Li C., Scheckel K.G., Donner E., Kopittke P.M., Schjoerring J.K., Lombi E. Foliar application of zinc sulphate and zinc EDTA to wheat leaves: Differences in mobility, distribution, and speciation. J. Exp. Bot. 2018;69:4469–4481. doi: 10.1093/jxb/ery236. PubMed DOI PMC

Cakmak I., Kalayci M., Kaya Y., Torun A.A., Aydin N., Wang Y., Arisoy Z., Erdem H., Yazici A., Gokmen O., et al. Biofortification and Localization of Zinc in Wheat Grain. J. Agric. Food Chem. 2010;58:9092–9102. doi: 10.1021/jf101197h. PubMed DOI

Zhang Y.Q., Sun Y.X., Ye Y.L., Karim M.R., Xue Y.F., Yan P., Meng Q.F., Cui Z.L., Cakmak I., Zhang F.S., et al. Zinc biofortification of wheat through fertilizer applications in different locations of China. Field Crops Res. 2012;125:1–7. doi: 10.1016/j.fcr.2011.08.003. DOI

Wang J., Mao H., Zhao H., Huang D., Wang Z. Different increases in maize and wheat grain zinc concentrations caused by soil and foliar applications of zinc in Loess Plateau, China. Field Crops Res. 2012;135:89–96. doi: 10.1016/j.fcr.2012.07.010. DOI

Xia H., Kong W., Wang L., Xue Y., Liu W., Zhang C., Yang S., Li C. Foliar Zn Spraying Simultaneously Improved Concentrations and Bioavailability of Zn and Fe in Maize Grains Irrespective of Foliar Sucrose Supply. Agronomy. 2019;9:386. doi: 10.3390/agronomy9070386. DOI

Zbíral J. Determination of plant-available micronutrients by the Mehlich 3 soil extractant—A proposal of critical values. Plant Soil Environ. 2016;62:527–531. doi: 10.17221/564/2016-PSE. DOI

Zbíral J., Malý S., Váňa M., editors. Soil Analysis III. 3rd ed. Central Institute for Supervising and Testing in Agriculture; Brno, Czech Republic: 2011. pp. 18–52. (In Czech)

Schumacher B.A. Methods for the Determination of Total Organic Carbon (TOC) in Soils and Sediments. United States Environmental Protection Agency, Environmental Sciences Division National, Exposure Research Laboratory; Las Vegas, NV, USA: 2002.

Gee G.W., Bauder J.W. Particle-size analysis. In: Klute A., editor. Methods of Soil Analysis Part 1—Physical and Mineralogical Methods. SSSA; Madison, WI, USA: 1986. pp. 383–411. ASA.

Nachabe B.M.H. Refining the definition of field capacity in the literature. J. Irrig. Drain. Eng. 1998;124:230–232. doi: 10.1061/(ASCE)0733-9437(1998)124:4(230). DOI

Netto A.T., Campostrini E., De Oliveira J.G., Bressan-Smith R.E. Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Sci. Hortic. 2005;104:199–209. doi: 10.1016/j.scienta.2004.08.013. DOI

Ortuzar-Iragorri M.A., Alonso A., Castellón A., Besga G., Estavillo J.M., Aizpurua A. N-Tester use in soft winter wheat: Evaluation of nitrogen status and grain yield prediction. Agron. J. 2005;97:1380–1389. doi: 10.2134/agronj2004.0268. DOI

Strasser R.J., Srivastava A., Tsimilli-Michael M. The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M., Pathre U., Monathy P., editors. Probing Photosynthesis: Mechanism, Regulation & Adaptation. Taylor and Francis; London, UK: 2000. pp. 443–480.

Stirbet A., Govindjee G. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. J. Photochem. Photobiol. B Biol. 2011;104:236–257. doi: 10.1016/j.jphotobiol.2010.12.010. PubMed DOI

Kalaji H.M., Schansker G., Ladle R.J., Goltsev V., Bosa K., Allakhverdiev S.I., Brestic M., Bussotti F., Calatayud A., Dąbrowski P., et al. Frequently asked questions about in vivo chlorophyll fluorescence: Practical issues. Photosynth. Res. 2014;122:121–158. doi: 10.1007/s11120-014-0024-6. PubMed DOI PMC

Genty B., Briantais J.M., Baker N.R. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta—Gen. Subj. 1989;990:87–92. doi: 10.1016/S0304-4165(89)80016-9. DOI

StatSoft, Inc STATISTICA (Data Analysis Software System), Version 14. 2021. [(accessed on 10 July 2022)]. Available online: www.statsoft.com.

Influence of indole acetic acid and trehalose, with and without zinc oxide nanoparticles coated urea on tomato growth in nitrogen deficient soils