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24-Epibrassinolide and Spermine Combined Treatment Sustains Maize (Zea mays L.) Drought Tolerance by Improving Photosynthetic Efficiency and Altering Phytohormones Profile

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Abstract

24-Epibrassinolide (EBL) and/or spermine (Spm) applications regulate photosynthetic process and hormonal balance in drought-stressed plants. A pot experiment was conducted to investigate the potential effects of 25 mg l−1 EBL and/or 0.1 mg l−1 Spm applied to maize (Zea mays L.; hybrid Giza 129) exposed to water deficiency (50 and 75% field capacity). Plastic pots were planted with maize plants and designed in a complete randomized design with four replications. Drought significantly impaired photosynthetic pigments content, photochemical reactions of photosynthesis, net photosynthetic rate, transpiration rate, stomatal conductance, maximum quantum efficiency of PSII photochemistry, electron transport rate, actual photochemical efficiency of PSII, photochemical quenching coefficient, effective quantum yield of PSII photochemistry, activities of Rubisco, Rubisco activase, and carbonic anhydrase, seeds carbohydrate content as well as concentrations of auxins, cytokinins, and gibberellins. These changes were significantly modulated in drought-affected plants after EBL and Spm combined application. Moreover, this combined treatment under water shortage conditions inhibited the increased concentrations of intercellular CO2, non-photochemical quenching coefficients, and abscisic acid as well as diminished the enhanced activity of glycolate oxidase. These results reinforce the utility of this combined treatment not only in improving the photosynthetic capability but also in regulating the hormonal homeostasis as a powerful strategy to enhance the plant drought tolerance. Indeed, exogenous application of 25 mg l−1 Spm + 0.1 mg l−1 EBL can preserve the photosynthetic apparatus activity under water deficiency.

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References

  • Ahmed CB, Rouina BB, Sensoy S, Boukhris M, Abdallah FB (2009) Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes. Environ Exp Bot 67:345–352

    Google Scholar 

  • Anjum SA, Tanveer M, Ashraf U, Hussain S, Shahzad B, Khan I, Wang L (2016) Effect of progressive drought stress on growth, leaf gas exchange, and antioxidant production in two maize cultivars. Environ Sci Pollut Res 23:17132–17141

    CAS  Google Scholar 

  • Blasco B, Ríos JJ, Cervilla LM, Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Rosales MA, Ruiz JM, Romero L (2010) Photorespiration process and nitrogen metabolism in lettuce plants (Lactuca sativa L.): induced changes in response to iodine biofortification. J Plant Growth Regul 29:477–486

    CAS  Google Scholar 

  • Cerovic ZG, Plesnicar M (1984) An improved procedure for the isolation of intact chloroplasts of high photosynthetic activity. Biochem J 223:543–545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Wang XM, Zhou L, He Y, Wang D, Qi YH, Jiang DA (2015) Rubisco activase is also a multiple responder to abiotic stresses in rice. PLoS One 10(10):e0140934

    PubMed  PubMed Central  Google Scholar 

  • Chernyadev II (2009) The protective action of cytokinins on the photosynthetic machinery and productivity of plants under stress (review). Appl Biochem Microbiol 45:351–362

    CAS  Google Scholar 

  • Coombs J, Hall DO, Long SP, Scurlock JMO (1987) Techniques in bioproductivity and photosynthesis. Pergamon, Oxford

    Google Scholar 

  • Cottenie A, Verloo M, Kiekens L, Velghe G, Camerlynck R (1982) Chemical analysis of plants and soils. In: Laboratory of analytical and agrochemistry. State University, Ghent, pp 14–24

    Google Scholar 

  • Divi UK, Krishna P (2009) Brassinosteroids confer stress tolerance. In: Weinheim HH (ed) Plant stress biology: genomics goes systems biology. Wiley-VCH, Weinheim, pp 119–135

    Google Scholar 

  • Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151

    PubMed  PubMed Central  Google Scholar 

  • Dobrikova AG, Vladkova RS, Rashkov GD et al (2014) Effects of exogenous 24-epibrassinolide on the photosynthetic membranes under non-stress conditions. Plant Physiol Biochem 80:75–82

    CAS  PubMed  Google Scholar 

  • Dong Y, Wang W, Hu G, Chen W, Zhuge Y, Wang Z, He M (2017) Role of exogenous 24-epibrassinolide in enhancing the salt tolerance of wheat seedlings. J Soil Sci Plant Nutr 17(3):554–569

    CAS  Google Scholar 

  • Dubois M, Gills K, Hamilton JK, Robers PA, Smith F (1956) Colorimeter method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  • Dwivedi RS, Randhawa NS (1974) Evolution of a rapid test of the hidden hunger of zinc in plants. Plant Soil 40:445–451

    CAS  Google Scholar 

  • Fan WQ, Zhao MY, Li SL, Bai X, Li J, Meng H et al (2016) Contrasting transcriptional responses of PYR1/PYL/RCAR ABA receptors to ABA or dehydration stress between maize seedling leaves and roots. BMC Plant Biol 16:99

    PubMed  PubMed Central  Google Scholar 

  • Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol Plant 31:937–945

    CAS  Google Scholar 

  • Gill MB, Cai K, Zhang G, Zeng F (2017) Brassinolide alleviates the drought-induced adverse effects in barley by modulation of enzymatic antioxidants and ultrastructure. Plant Growth Regul 82:447–455

    CAS  Google Scholar 

  • Gleason SM, Wiggans DR, Bliss CA, Comas LH, Cooper M, DeJonge KC, Young JS, Zhang H (2017) Coordinated decline in photosynthesis and hydraulic conductance during drought stress in Zea mays. Flora 227:1–9

    Google Scholar 

  • Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320

    CAS  PubMed  Google Scholar 

  • Hamdani S, Yaakoubi H, Carpentier R (2011) Polyamines interaction with thylakoid proteins during stress. J Photochem Photobiol B 104:314–319

    CAS  PubMed  Google Scholar 

  • Hu W, Yan X, Xiao Y, Zeng J, Qi H, Ogweno J (2013) 24-Epibrassinosteroid alleviate drought-induced inhibition of photosynthesis in Capsicum annuum. Sci Hortic 150:232–237

    CAS  Google Scholar 

  • Huang X, Zhou G, Yang W, Wang A, Hu Z, Lin C, Chen X (2014) Drought-inhibited ribulose-1,5-bisphosphate carboxylase activity is mediated through increased release of ethylene and changes in the ratio of polyamines in pakchoi. J Plant Physiol 171:1392–1400

    CAS  PubMed  Google Scholar 

  • Irigoyen JJ, Emerich DW, Sanchez-Dıaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugar in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60

    CAS  Google Scholar 

  • Jiang YP, Cheng F, Zhou YH, Xia XJ, Mao WH, Shi K, Chen ZX, Yu JQ (2012) Cellular glutathione redox homeostasis plays an important role in the brassinosteroid-induced increase in CO2 assimilation in Cucumis sativus. New Phytol 194:932–943

    CAS  PubMed  Google Scholar 

  • Li Z, Zhang Y, Zhang X, Peng Y, Merewitz E, Ma X, Huang L, Yan Y (2016) The alterations of endogenous polyamines and phytohormones induced by exogenous application of spermidine regulate antioxidant metabolism, metallothionein and relevant genes conferring drought tolerance in white clover. Environ Exp Bot 124:22–38

    CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Lu CM, Qiu NW, Wang BS, Zhang JH (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54:851–860

    CAS  PubMed  Google Scholar 

  • Mehta P, Jajoo A, Mathur S, Bharti S (2010) Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves. Plant Physiol Biochem 48:16–20

    CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    CAS  PubMed  Google Scholar 

  • Nehela Y, Hijaz F, Elzaawely AA, El-Zahaby HM, Killiny N (2016) Phytohormone profiling of the sweet orange (Citrus sinensis L., Osbeck) leaves and roots using GC–MS-based method. J Plant Physiol 199:12–17

    CAS  PubMed  Google Scholar 

  • Osório ML, Osório J, Romano A (2013) Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaris major under high temperature and drought. Photosynthetica 51:75–84

    Google Scholar 

  • Pastenes C, Pimentel P, Lillo J (2005) Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot 56:425–433

    CAS  PubMed  Google Scholar 

  • Popovic RB, Kyle DJ, Cohen AS, Zalik S (1979) Stabilization of thylakoid membranes by spermine during stress induced senescence of barley leaf discs. Plant Physiol 64:721–726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qin G, Gu H, Ma L, Peng Y, Deng XW, Chen Z, Qu LJ (2007) Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll carotenoid, and gibberellin biosynthesis. Cell Res 17:471–482

    CAS  PubMed  Google Scholar 

  • Radhakrishnan R, Lee I (2013) Spermine promotes acclimation to osmotic stress by modifying antioxidant, abscisic acid, and jasmonic acid signals in soybean. J Plant Growth Regul 32:22–30

    CAS  Google Scholar 

  • Ramel F, Sulmon C, Gouesbet G, Couee I (2009) Natural variation reveals relationships between pre-stress carbohydrate nutritional status and subsequent responses to xenobiotic and oxidative stress in Arabidopsis thaliana. Ann Bot 104:1323–1337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ribaut JM, Betran J, Monneveux P, Setter T (2012) Drought tolerance in maize. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp 311–344

    Google Scholar 

  • Sapeta H, Costa JM, Lourenco T, Maroco J, van der Linde P, Oliveira MM (2013) Drought stress response in Jatropha curcas: growth and physiology. Environ Exp Bot 85:76–84

    CAS  Google Scholar 

  • Shakirova F, Allagulova C, Maslennikova D, Fedorova K, Yuldashev R, Lubyanova A, Bezrukova M, Avalbaev A (2016) Involvement of dehydrins in 24-epibrassinolide-induced protection of wheat plants against drought stress. Plant Physiol Biochem 108:539–548

    CAS  PubMed  Google Scholar 

  • Snedecor GW, Cochran WG (1980) Statistical methods, 7th edn. Iowa State Univ. Press, Ames

    Google Scholar 

  • Sun C, Gao X, Chen X, Fu J, Zhang Y (2016) Metabolic and growth responses of maize to successive drought and re-watering cycles. Agric Water Manag 172:62–73

    Google Scholar 

  • Talaat NB (2013) RNAi based simultaneous silencing of all forms of light-dependent NADPH:protochlorophyllide oxidoreductase genes result in the accumulation of protochlorophyllide in tobacco (Nicotiana tabacum). Plant Physiol Biochem 71:31–36

    CAS  PubMed  Google Scholar 

  • Talaat NB (2019a) Role of reactive oxygen species signaling in plant growth and development. In: Hasanuzzaman M, Fotopoulos V, Nahar K, Fujita M (eds) Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms. Wiley, Chichester, pp 225–266

    Google Scholar 

  • Talaat NB (2019b) Abiotic stresses-induced physiological alteration in wheat. In: Hasanuzzaman M, Nahar K, Hossain A (eds) Wheat production in changing environments—responses, adaptation and tolerance. Springer Nature Singapore Pte, Ltd, Singapore, pp 1–30

    Google Scholar 

  • Talaat NB, Shawky BT (2012) 24-Epibrassinolide ameliorates the saline stress and improves the productivity of wheat (Triticum aestivum L.). Environ Exp Bot 82:80–88

    CAS  Google Scholar 

  • Talaat NB, Shawky BT (2013) 24-Epibrassinolide alleviates salt-induced inhibition of productivity by increasing nutrients and compatible solutes accumulation and enhancing antioxidant system in wheat (Triticum aestivum L.). Acta Physiol Plant 35:729–740

    CAS  Google Scholar 

  • Talaat NB, Shawky BT (2016) Dual application of 24-epibrassinolide and spermine confers drought stress tolerance in maize (Zea mays L.) by modulating polyamine and protein metabolism. J Plant Growth Regul 35:518–533

    CAS  Google Scholar 

  • Talaat NB, Shawky BT, Ibrahim AS (2015) Alleviation of drought-induced oxidative stress in maize (Zea mays L.) plants by dual application of 24-epibrassinolide and spermine. Environ Exp Bot 113:47–58

    CAS  Google Scholar 

  • Tiwari BS, Bose A, Ghosh B (1997) Photosynthesis in rice under salt stress. Photosynthetica 34:303–306

    CAS  Google Scholar 

  • Todorova D, Talaat NB, Katerova Z, Alexieva V, Shawky BT (2016) Polyamines and brassinosteroids in drought stress responses and tolerance in plants. In: Ahmad P (ed) Water stress and crop plants: a sustainable approach, vol 2. Wiley, Chichester, pp 608–627

    Google Scholar 

  • Xia XJ, Huang LF, Zhou YH, Mao WH, Shi K, Wu JX, Asami T, Chen Z, Yu JQ (2009) Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. Planta 230:1185–1196

    CAS  PubMed  Google Scholar 

  • Yih RY, Clark HE (1965) Carbohydrate and protein content of boron deficient tomato root tips in relation to anatomy and growth. Plant Physiol 40:312–315

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang RH, Zhang XH, Camberato JJ, Xue JQ (2015) Photosynthetic performance of maize hybrids to drought stress. Russ J Plant Physiol 62:788–796

    CAS  Google Scholar 

  • Zhang W, Wang C, Dong M, Jin S, Li H (2018) Dynamics of soil fertility and maize growth with lower environment impacts depending on a combination of organic and mineral fertilizer. J Soil Sci Plant Nutr 18(2):556–575

    CAS  Google Scholar 

  • Zhao G, Xu H, Zhang P, Su X, Zhao H (2017) Effects of 24-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress. Plant Growth Regul 81:377–384

    CAS  Google Scholar 

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Talaat, N.B. 24-Epibrassinolide and Spermine Combined Treatment Sustains Maize (Zea mays L.) Drought Tolerance by Improving Photosynthetic Efficiency and Altering Phytohormones Profile. J Soil Sci Plant Nutr 20, 516–529 (2020). https://doi.org/10.1007/s42729-019-00138-4

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