Abstract
Sugarcane (Saccharum officinarum) is one of the main sources of sugar, energy renewable, and ethanol worldwide. Nitrogen (N) plays a plethora of structural and functional roles on sugarcane growth and development. Nickel (Ni) is a cofactor of urease enzyme, acting in N metabolism and antioxidant system in plants, potentially leading to enhanced use of absorbed N. This study aimed to evaluate Ni application on N metabolism, antioxidant system, and yield of two sugarcane cultivars (RB86 7515 RB96 6928). The experiment was composed by six Ni application rates (0; 0.25; 0.5; 1; 3; 9 mg kg−1) and two sugarcane cultivars. Application of Ni via soil increased photosynthetic pigments concentration, urease, and nitrate reductase activity, leading to an enhanced N metabolism in sugarcane plants. Fertilization with Ni also improved antioxidant system by increasing superoxide dismutase, ascorbate peroxidase, and catalase activity alleviating the stress caused by reactive oxygen species. The increased photosynthetic pigments and antioxidant systems led to a higher concentration of free amino acids and total sugars. The enhanced N metabolism and increased sugar accumulation were followed by an increase in leaf, root, stems dry weights, and tiller number. The application rate of 0.5 mg Ni kg−1 led to a higher yield in sugarcane cultivars. This study presents fundamental new insights regarding Ni effect on N metabolism and sugar concentration that can be helpful to increase the crop tolerance to abiotic stress, and this could potentially lead to increase sugarcane yield under field conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abou-Zeid H, Tammam A, Badr R, Bader A, Ibrahim Y (2020) Ultrastructural and physiological responses induced by nickel and ozone stress in rice (Oryza sativa) cultivars. Int J Agric Biol 23:15–24. https://doi.org/10.17957/IJAB/15.1253
Alexieva V, Sergiev S, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344. https://doi.org/10.1046/j.1365-3040.2001.00778.x
Arkoun M, Jannin L, Laîné P, Etienne P, Masclaux-Daubresse C, Citerne S, Garnica M, Garcia-Mina JM, Yvin JC, Ourry A (2013) A physiological and molecular study of the effects of nickel deficiency and phenylphosphorodiamidate (PPD) application on urea metabolism in oilseed rape (Brassica napus L.). Plant Soil 362:79–92. https://doi.org/10.1007/s11104-012-1227-2
Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to tranfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292. https://doi.org/10.1034/j.1399-3054.1998.1040217.x
Bahar NHA, Lo M, Sanjaya M, Van Vianen J, Alexander P, Ickowitz A, Sunderland T (2020) Meeting the food security challenge for nine billion people in 2050: what impact on forests? Glob Environ Change 62:102056. https://doi.org/10.1016/j.gloenvcha.2020.102056
Bai C, Reilly CC, Wood BW (2006) Nickel deficiency disrupts metabolism of ureides, amino acids, and organic acids of young pecan foliage. Plant Physiol 140:433–443. https://doi.org/10.1104/pp.105.072983
Barcelos JPQ, Reis HPG, Godoy CV, Gratão PL, Furlani Junior E, Putti FF, Reis AR (2018) Impact of foliar nickel application on urease activity, antioxidant metabolism and control of powdery mildew (Microsphaera diffusa) in soybean plants. Plant Pathol 67:1502–1513. https://doi.org/10.1111/ppa.12871
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
Campos JVL, Cunha LOM, Nascimentodo V, Figueiredode PAM, Ferrari S (2022) Can foliar application of nutrients increase the productive potential of peanuts? Gesunde Pflan 74:1–5. https://doi.org/10.1007/s10343-022-00739-7
Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80. https://doi.org/10.1080/00103627509366547
Cunha MLO, de Oliveira LCA, Silva VM, Montanha GS, dos Reis AR (2022) Selenium increases photosynthetic capacity, daidzein biosynthesis, nodulation and yield of peanuts plants (Arachis hypogaea L.). Plant Physiol Biochem 190:231–239. https://doi.org/10.1016/j.plaphy.2022.08.006
De Almeida Moreira BR, Cruz VH, Cunha MLO, da Silva VR (2021a) Full-scale production of high-quality wood pellets assisted by multivariate statistical process control. Biomass Bioenerg 151:106159. https://doi.org/10.1016/j.biombioe.2021.106159
De Almeida Moreira BR, Cruz VH, Cunha MLO, Lopes NP, Magalhães AC, Miasaki CT, da Silva VR (2021b) Valorization of semi-solid by-product from distillation of cellulosic ethanol into blends for heating and power. Waste Dispos Sustain Energy 3:49–61. https://doi.org/10.1007/s42768-020-00062-9
De Andrade Junior MAU, Valin H, Soterroni AC, Ramos FM, Halog A (2019) Exploring future scenarios of ethanol demand in Brazil and their land-use implications. Energy Policy 134:110958. https://doi.org/10.1016/j.enpol.2019.110958
Dixon NE, Gazzola C, Blakeley RL, Zerner B (1975) Jack bean urease (EC 3.5.1.5) a metalloenzyme: simple biological role for nickel. J Am Chem Soc 97:4131–4133
Dos Santos SG, da Silva RF, Da Fonseca CS, Pereira W, Santos LA, Reis VM (2017) Development and nitrate reductase activity of sugarcane inoculated with five diazotrophic strains. Arch Microbiol 199:863–873. https://doi.org/10.1007/s00203-017-1357-2
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Ferrari S, Cunha MLO, VallePolycarpo Gdo, Zied DC, de Oliveira LCA, Júnior EF (2022a) Genotypic variation in grain nutritional content and agronomic traits of upland rice: strategy to reduce hunger and malnutrition. Cereal Res Commun 50:1–9. https://doi.org/10.1007/s42976-022-00257-2
Ferrari S, Valle Polycarpo Gdo, Vargas PF, Fernandes AM, Cunha MLO, Pagliari P (2022b) Mix of trinexapac-ethyl and nitrogen application to reduce upland rice plant height and increase yield. Plant Growth Reg 96:209–219. https://doi.org/10.1007/s10725-021-00770-0
Fiala R, Fialová I, Vackulík M, Luxová M (2021) Effect of silicon on the young maize plants exposed to nickel stress. Plant Physiol Biochem 166:645–656. https://doi.org/10.1016/j.plaphy.2021.06.026
Freitas DS, Rodak BW, dos Reis AR, Reis FB, de Carvalho TS, Schulze J, Carneiro MAC, Guilherme LRG (2018) Hidden nickel deficiency? Nickel fertilization via soil improves nitrogen metabolism and grain yield in soybean genotypes. Front Plant Sci 9:614. https://doi.org/10.3389/fpls.2018.00614
Freitas DS, Rodak BW, Carneiro MAC, Guilherme LRG (2019) How does Ni fertilization affect a responsive soybean genotype? A dose study. Plant Soil 441:567–586. https://doi.org/10.1007/s11104-019-04146-2
Gerendás J, Sattelmacher B (1997) Significance of Ni supply for growth, urease activity and the concentrations of urea, amino acids and mineral nutrients of urea-grown plants. Plant Soil 190(1):153–162. https://doi.org/10.1023/A:1004260730027
Giannapolitis CN, Ries SK (1977) Superoxide dismutases. I Occorence in higher plants. Plant Physiol 59:309–314
Goncalves AZ, Oliveira PMR, Neto AAC, Mercier H (2020) Thinking of the leaf as a whole plant: how does N metabolism occur in a plant with foliar nutrient uptake? Environ Exp Bot 178:104163. https://doi.org/10.1016/j.envexpbot.2020.104163
González CI, Maine MA, Cazenave J, Hadad HR, Benavides MP (2015) Ni accumulation and its effects on physiological and biochemical parameters of Eichhornia crassipes. Environ Ex Bot 117:20–27. https://doi.org/10.1016/j.envexpbot.2015.04.006
Gouveia GCC, Galindo FS, Lanza MGDB, da Rocha Silva AC, de Brito Mateus MP, da Silva MS, Tavanti RF, Tavanti TF, Lavres J, Dos Reis AR (2020) Selenium toxicity stress-induced phenotypical, biochemical and physiological responses in rice plants: characterization of symptoms and plant metabolic adjustment. Ecotoxicol Environ Saf 202:110916. https://doi.org/10.1016/j.ecoenv.2020.110916
Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metalstressed plants a little easier. Funct Plant Biol 32:481–494. https://doi.org/10.1071/FP05016
Habibi G (2017) Physiological, photochemical and ionic responses of sunflower seedlings to exogenous selenium supply under salt stress. Acta Physiol Plant 39:1–9. https://doi.org/10.1007/s11738-017-2517-3
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Karwat H, Sparke MA, Rasche F, Arango J, Nuñez J, Rao I, Moreta D, Cadisch G (2019) Nitrate reductase activity in leaves as a plant physiological indicator of in vivo biological nitrification inhibition by Brachiaria humidicola. Plant Physiol Biochem 137:113–120. https://doi.org/10.1016/j.plaphy.2019.02.002
Khoshgoftarmanesh AH, Hosseini F, Afyuni M (2011) Nickel supplementation effect on the growth, urease activity and urea and nitrate concentrations in lettuce supplied with different nitrogen sources. Sci Hortic 130:381–385. https://doi.org/10.1016/j.scienta.2011.07.009
Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865. https://doi.org/10.1046/j.1365-3040.2003.01017.x
Klimov VV (2003) Discovery of pheophytin function in the photosynthetic energy conversion as the primary electron acceptor of Photosystem II. Photosynth Res 76:247–253. https://doi.org/10.1023/A:1024990408747
Kutman BY, Kutman UB, Camak I (2012) Nickel-enriched seed and externally supplied nickel improve growth and alleviate foliar urea damage in soybean. Plant Soil 1007:1–15. https://doi.org/10.1007/s11104-012-1284-6
Lanza MGDB, Dos Reis AR (2021) Roles of selenium in mineral plant nutrition: ROS scavenging responses against abiotic stresses. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2021.04.026
McCullough H (1967) The determination of ammonia in whole blood by a direct colorimetric method. Clin Chim Acta 17:297–304. https://doi.org/10.1016/0009-8981(67)90133-7
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
Moldes CA, Medici LO, Abrahao OS, Tsai SM, Azevedo RA (2008) Biochemical responses of glyphosate resistant and susceptible soybean plants exposed to glyphosate. Acta Physiol Plant 30:469–479. https://doi.org/10.1007/s11738-008-0144-8
Nawaz H, Anwar-ul-Haq M, Akhtar J, Arfan M (2021) Cadmium, chromium, nickel and nitrate accumulation in wheat (Triticum aestivum L) using wastewater irrigation and health risks assessment. Ecotoxicol Environ Saf 208:111685. https://doi.org/10.1016/j.ecoenv.2020.111685
Ohyama T, Ohtake N, Sueyoshi K, Ono Y, Tsutsumi K, Ueno M, Tanabata S, Sato T, Takahashi Y (2017) Amino acid metabolism and transport in soybean plants. Amino Acid-New Insights and Roles in Plant and Animal: 171-196. https://doi.org/10.5772/intechopen.68992
Reis AR, Favarin JL, Gallo LA, Malavolta JE, Moraes MF, Lavres Junior J (2009) Nitrate reductase and glutamine synthetase activity in cofee leaves during fruit development. R Bras Ci Sol 33:315–324. https://doi.org/10.1590/S0100-06832009000200009
Reis AR, de Queiroz Barcelos JP, de Souza Osório CRW, Santos EF, Lisboa LAM, Santini JMK, ..., Gratao PL (2017) A glimpse into the physiological, biochemical and nutritional status of soybean plants under Ni-stress conditions. Environ Exp Bot 144:76–87
Scalabrin E, Radaelli M, Capodaglio G (2016) Simultaneous determination of shikimic acid, salicylic acid and jasmonic acid in wild and transgenic Nicotiana langsdorffii plants exposed to abiotic stresses. Plant Physiol Biochem 103:53–60. https://doi.org/10.1016/j.plaphy.2016.02.040
Shahzad B, Tanveer M, Rehman A, Cheema SA, Fahad S, Rehman S, Sharma A (2018) Nickel: whether toxic or essential for plants and environment-a review. Plant Physiol Biochem 132:641–651. https://doi.org/10.1016/j.plaphy.2018.10.014
Silva VM, Boleta EHM, Lanza MGDB, Lavres J, Martins JT, Santos EF, dos Santos FLM, Putti FF, Junior EF, White PJ, Broadley MR, Carvalho HWP, Reis AR (2018) Physiological, biochemical, and ultrastructural characterization of selenium toxicity in cowpea plants. Environ Exp Bot 150:172–182. https://doi.org/10.1016/j.envexpbot.2018.03.020
Silva VM, Tavanti RFR, Gratão PL, Alcock TD, Dos Reis AR (2020) Selenate and selenite affect photosynthetic pigments and ROS scavenging through distinct mechanisms in cowpea (Vigna unguiculata (L) walp) plants. Ecotoxicol Environ Saf 201:110777. https://doi.org/10.1016/j.ecoenv.2020.110777
Smith NG, Woodburn J (1984) Nickel and ethylene involvement in the senescence of leaves and flowers. Sci Nat 71:210–211. https://doi.org/10.1007/BF00490435
Souza SCR, Sodek L, Polacco JC, Mazzafera P (2020) Urease deficiency alters nitrogen metabolism and gene expression in urease-null soybean without affecting growth or productivity under nitrate supply. Acta Physiol Plant 42:1–11. https://doi.org/10.1007/s11738-020-3020-9
Taghizadeh-Alisaraei A, Motevali A, Ghobadian B (2019) Ethanol production from date wastes: adapted technologies, challenges, and global potential. Renew Energy 143:1094–1110. https://doi.org/10.1016/j.renene.2019.05.048
Tavanti TR, de Melo AAR, Moreira LDK, Sanchez DEJ, dos Santos Silva R, da Silva RM, Dos Reis AR (2021) Micronutrient fertilization enhances ROS scavenging system for alleviation of abiotic stresses in plants. Plant Physiol Biochem 160:386–396. https://doi.org/10.1016/j.plaphy.2021.01.040
Tezotto T, Favarin JL, Azevedo RA, Alleoni LRF, Mazzafera P (2012) Coffee is highly tolerant to cadmium, nickel and zinc: plant and soil nutritional status, metal distribution and bean yield. Field Crop Res 125:25–34
Thomas CL, Alcock TD, Graham NS, Hayden S, Matterson L, Wilson SD, Young SD, Dupuy LX, White PJ, Hammond JP, Dnaku JMC, Sweeney A, Bancroft I, Broadle MR (2016) Root morphology and seed and leaf ionomic traits in a Brassica napus L. diversity panel show wide phenotypic variation and are characteristic of crop habit. Plant Biol 16:1–18. https://doi.org/10.1186/s12870-016-0902-5
Uruç Parlak K (2016) Effect of nickel on growth and biochemical characteristics of wheat (Triticum aestivum L.) seedlings. NJAS: Wageningen J Life Sci 76(1):1–5. https://doi.org/10.1016/j.njas.2012.07.001
Van Handel E (1968) Direct microdetermination of sucrose. Anal Biochem 22:280–283. https://doi.org/10.1016/0003-2697(68)90317-5
Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:534. https://doi.org/10.3389/fpls.2018.00614
Witte CP (2011) Urea metabolism in plants. Plant Sci 180(3):431–438
Wood BW, Reilly CC, Nyczepir AP (2004) Mouse-ear of pecan: a nickel deficiency. HortScience 39:1238–1242. https://doi.org/10.21273/hortsci.39.6.1238
Xiaoying L, Mingjuan Y, Xiaodong X, Khaldun ABM, Arif ATAK, Caihong Z, Dawei L (2022) Effect of light on growth and chlorophyll development in kiwifruit ex vitro and in vitro. Sci Hortic 291:110599. https://doi.org/10.1016/j.scienta.2021.110599
Zheng QL, Nakatsuka A, Matsumoto T, Itamura H (2006) Pre-harvest nickel application to the calyx of ‘Saijo’ persimmon fruit prolongs postharvest shelf-life. Postharvest Biol Technol 42:98–103. https://doi.org/10.1016/j.postharvbio.2006.05.001
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rampazzo, M.V., Cunha, M.L.O., de Oliveira, L.C.A. et al. Physiological Roles of Nickel on Antioxidant and Nitrogen Metabolism Increasing the Yield of Sugarcane Plants. J Soil Sci Plant Nutr 22, 4438–4448 (2022). https://doi.org/10.1007/s42729-022-01045-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-022-01045-x