Abstract
This study investigates the protective role of silicon (Si) on growth performance, nutrient homeostasis, and C:N:P stoichiometric of sugarcane (Saccharum spp.) seedlings under aluminum (Al) stress in hydroponic conditions. Experiments were conducted as a factorial scheme (2 × 2) in a randomized complete block design (RCBD), with four replications, for each sugarcane cultivar (“CTC9002” and “CTC9003”). They were grown in pots filled with normal Clark nutrient (pH = 5.8 without Al) and acidic Clark nutrient solution (pH = 4.5 with 15 mg L−1 of Al, as aluminum sulfate [Al2 (SO4)3·18H2O]) in the absence or presence of Si (2 mM, as potassium silicate (K2SiO3). Sugarcane seedlings of both cultivars grown under Al stress alone significantly decreased root, culm, and leaf dry biomass, and this adverse effect was reversed by Si supplementation. Added Si also modified nutrient homeostasis of both sugarcane cultivars, and these effects varied depending on plant organs. Si decreased the concentration of C, N, and P and correspondingly increased C:N, C:P, and N:P stoichiometric. In addition, both sugarcane cultivars had a positive response to Si supplementation, but cultivar “CTC9003” is more recommended under added Si to ameliorate the detrimental effects caused by Al toxicity. The findings of this study indicate that Si promoted attenuation of Al-stressed sugarcane seedlings by regulating nutrient and homeostasis stoichiometric, leading to improve dry biomass production.
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References
Ahmad P, Abass M, Alam P, Nasser M, Wijaya L, Ali S, Ashraf M (2019) Silicon (Si) supplementation alleviates NaCl toxicity in mung bean [Vigna radiata (L.) Wilczek] through the modifications of physio-biochemical attributes and key antioxidant enzymes. J Plant Growth Regul 38:70–82. https://doi.org/10.1007/s00344-018-9810-2
Al MM, Khan AL, Muneer S (2020) Silicon in horticultural crops: cross-talk, signaling, and tolerance mechanism under salinity stress. Plants 9:460. https://doi.org/10.3390/PLANTS9040460
Alzahrani Y, Kuşvuran A, Alharby HF, Kuşvuran S, Rady MM (2018) The defensive role of silicon in wheat against stress conditions induced by drought, salinity or cadmium. Ecotoxicol Environ Saf 154:187–196. https://doi.org/10.1016/j.ecoenv.2018.02.057
Balestrasse KB, Gallego SM, Tomaro ML (2006) Aluminium stress affects nitrogen fixation and assimilation in soybean (Glycine max L.). Plant Growth Regul 48:271–281. https://doi.org/10.1007/s10725-006-0010-x
Bataglia OC, Furlani AMC, Teixeira JPF, Gallo JR (1983) Métodos de análises química de plantas. Instituto Agronômico de Campinas, Campinas, p 48 (IAC, Boletim técnico, 78)
Calero Hurtado A, Chiconato DA, de Prado RM, da Sousa Junior GS, Felisberto G (2019) Silicon attenuates sodium toxicity by improving nutritional efficiency in sorghum and sunflower plants. Plant Physiol Biochem 142:224–233. https://doi.org/10.1016/j.plaphy.2019.07.010
Calero Hurtado A, AparecidaChiconato D, de Mello Prado R, da Silveira Sousa Junior G, OliveraViciedo D, de Cássia Piccolo M (2020) Silicon application induces changes C:N: P stoichiometry and enhances stoichiometric homeostasis of sorghum and sunflower plants under salt stress. Saudi J Biol Sci 27:3711–3719. https://doi.org/10.1016/j.sjbs.2020.08.017
Calero Hurtado A, Chiconato DA, de Prado RM, da Sousa Junior GS, Gratão PL, Felisberto G, OliveraViciedo D, dos Mathias Santos DM (2020) Different methods of silicon application attenuate salt stress in sorghum and sunflower by modifying the antioxidative defense mechanism. Ecotoxicol Environ Saf 203:110964. https://doi.org/10.1016/j.ecoenv.2020.110964
Chaiwong N, Prom-u-thai C (2022) Significant roles of silicon for improving crop productivity and factors affecting silicon uptake and accumulation in rice: a review. J Soil Sci Plant Nutr 2022:1–13. https://doi.org/10.1007/S42729-022-00787-Y
Cocker KM, Evans DE, Hodson MJ (1998) The amelioration of aluminium toxicity by silicon in higher plants: solution chemistry or an in planta mechanism? Physiol Plant 104:608–614. https://doi.org/10.1034/j.1399-3054.1998.1040413.x
da Silva RG, Rosa-Santos TM, de França SC, Kottapalli P, Kottapalli KR, Zingaretti SM (2019) Microtranscriptome analysis of sugarcane cultivars in response to aluminum stress. PLoS One 14:e0217806. https://doi.org/10.1371/journal.pone.0217806
de Sousa A, Saleh AM, Habeeb TH, Hassan YM, Zrieq R, Wadaan MAM, Hozzein WN, Selim S, Matos M, AbdElgawad H (2019) Silicon dioxide nanoparticles ameliorate the phytotoxic hazards of aluminum in maize grown on acidic soil. Sci Total Environ 693:133636. https://doi.org/10.1016/j.scitotenv.2019.133636
Deshmukh R, Sonah H, Belanger R (2020) New evidence defining the evolutionary path of aquaporins regulating silicon uptake in land plants. J Exp Bot 71:6775–6788. https://doi.org/10.1093/jxb/eraa342
Elser J (2006) Biological stoichiometry: a chemical bridge between ecosystem ecology and evolutionary biology. Am Nat 168:S25–S35
Etesami H, Jeong BR (2018) Silicon (Si): Review and future prospects on the action mechanisms in alleviating biotic and abiotic stresses in plants. Ecotoxicol Environ Saf 147:881–896. https://doi.org/10.1016/j.ecoenv.2017.09.063
Freitas LB, Fernandes DM, Maia SCM, Fernandes AM (2017) Effects of silicon on aluminum toxicity in upland rice plants. Plant Soil 420:263–275. https://doi.org/10.1007/s11104-017-3397-4
Haddad C, Arkoun M, Jamois F, Schwarzenberg A, Yvin JC, Etienne P, Laîné P (2018) Silicon promotes growth of Brassica napus L. and delays leaf senescence induced by nitrogen starvation. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.00516
Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot 96:1027–1046. https://doi.org/10.1093/aob/mci255
Hodson MJ, Evans DE (2020) Aluminium/silicon interactions in higher plants- an update. J Exp Bot eraa024. https://doi.org/10.1093/jxb/eraa024
Imadi SR, Waseem S, Kazi AG, Azooz MM, Ahmad P (2016) Aluminum toxicity in plants: an overview. Plant Met Interact Emerg Remediat Tech 1–20https://doi.org/10.1016/B978-0-12-803158-2.00001-1
Imtiaz M, Rizwan MS, Mushtaq MA, Ashraf M, Shahzad SM, Yousaf B, Saeed DA, Rizwan MS, Nawaz MA, Mehmood S, Tu S (2016) Silicon occurrence, uptake, transport and mechanisms of heavy metals, minerals and salinity enhanced tolerance in plants with future prospects: A review. J. Environ. Manage. 183
Khan W, Aziz T, Hussain I, Ramzani PMA, Reichenauer TG (2017) Silicon: a beneficial nutrient for maize crop to enhance photochemical efficiency of photosystem II under salt stress. Arch Agron Soil Sci 63:599–611. https://doi.org/10.1080/03650340.2016.1233322
Klotzbücher T, Klotzbücher A, Kaiser K, Vetterlein D, Jahn R, Mikutta R (2018) Variable silicon accumulation in plants affects terrestrial carbon cycling by controlling lignin synthesis. Glob Chang Biol 24:e183–e189. https://doi.org/10.1111/gcb.13845
Kopittke PM, Gianoncelli A, Kourousias G, Green K, McKenna BA (2017) Alleviation of Al toxicity by Si is associated with the formation of Al–Si complexes in root tissues of sorghum. Front Plant Sci 8:2189. https://doi.org/10.3389/fpls.2017.02189
Kostic L, Nikolic N, Bosnic D, Samardzic J, Nikolic M (2017) Silicon increases phosphorus (P) uptake by wheat under low P acid soil conditions. Plant Soil 419:447–455. https://doi.org/10.1007/s11104-017-3364-0
Kraska JE, Breitenbeck GA (2010) Simple, robust method for quantifying silicon in plant tissue. Commun Soil Sci Plant Anal 41:2075–2085. https://doi.org/10.1080/00103624.2010.498537
Kumar S, Milstein Y, Brami Y, Elbaum M, Elbaum R (2017) Mechanism of silica deposition in sorghum silica cells. New Phytol 213:791–798. https://doi.org/10.1111/nph.14173
Laîné P, Haddad C, Etienne P, Arkoun M, Yvin JC (2019) Silicon promotes agronomic performance in Brassica napus cultivated under field conditions with two nitrogen fertilizer inputs. Plants 8:137. https://doi.org/10.3390/PLANTS8050137
Liang Y, Yang C, Shi H (2001) Effects of silicon on growth and mineral composition of barley grown under toxic levels of aluminum. J Plant Nutr 24:229–243. https://doi.org/10.1081/PLN-100001384
Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428. https://doi.org/10.1016/j.envpol.2006.06.008
Mahdieh M, Habibollahi N, Amirjani MR, Abnosi MH, Ghorbanpour M (2015) Exogenous silicon nutrition ameliorates salt-induced stress by improving growth and efficiency of PSII in Oryza sativa L. cultivars. J Soil Sci Plant Nutr 15:0–0. https://doi.org/10.4067/S0718-95162015005000073
Maksimović JD, Bogdanović J, Maksimović V, Nikolic M (2007) Silicon modulates the metabolism and utilization of phenolic compounds in cucumber (Cucumis sativus L.) grown at excess manganese. J Plant Nutr Soil Sci 170:739–744. https://doi.org/10.1002/jpln.200700101
Moreno-Alvarado M, García-Morales S, Trejo-Téllez LI, Hidalgo-Contreras JV, Gómez-Merino FC (2017) Aluminum enhances growth and sugar concentration, alters macronutrient status and regulates the expression of NAC transcription factors in rice. Front Plant Sci 8:73. https://doi.org/10.3389/FPLS.2017.00073/BIBTEX
Namjoyan S, Sorooshzadeh A, Rajabi A, Aghaalikhani M (2021) Improving root quality and yield of sugar beet by nano-silicon and tebuconazole under limited irrigation. J Soil Sci Plant Nutr 21:3378–3386. https://doi.org/10.1007/S42729-021-00613-X/TABLES/6
Oliveira RLL de, Prado R de M, Felisberto G, Checchio MV, Gratão PL (2019) Silicon mitigates manganese deficiency stress by regulating the physiology and activity of antioxidant enzymes in sorghum plants. J Soil Sci Plant Nutr 1–11https://doi.org/10.1007/s42729-019-00051-w
Olivera D, Prado R, Lizcano R, Santos LC, Calero A, Nedd LL, Castellanos L (2019) Silicon supplementation alleviates ammonium toxicity in sugar beet (Beta vulgaris L.). J Soil Sci Plant Nutr 19:413–419. https://doi.org/10.1007/s42729-019-00043-w
Olivera-Viciedo D, de Mello PR, Martinez CA, Habermann E, de Cássia PM, Calero-Hurtado A, Barreto RF, Peña K (2021a) Are the interaction effects of warming and drought on nutritional status and biomass production in a tropical forage legume greater than their individual effects? Planta 254:1–10. https://doi.org/10.1007/S00425-021-03758-2/FIGURES/5
Olivera-Viciedo D, de Mello Prado R, Martinez CA, Habermann E, de Cássia Piccolo M, Calero Hurtado A, Barreto RF, Peña Calzada K (2021b) Changes in soil water availability and air-temperature impact biomass allocation and C:N:P stoichiometry in different organs of Stylosanthes capitata Vogel. J Environ Manage 278https://doi.org/10.1016/j.jenvman.2020.111540
Pontigo S, Ribera A, Gianfreda L, de la Luz MM, Nikolic M, Cartes P (2015) Silicon in vascular plants: uptake, transport and its influence on mineral stress under acidic conditions. Planta 242:23–37. https://doi.org/10.1007/s00425-015-2333-1
Pontigo S, Godoy K, Jiménez H, Gutiérrez-Moraga A, Mora MDLL, Cartes P (2017) Silicon-mediated alleviation of aluminum toxicity by modulation of Al/Si uptake and antioxidant performance in ryegrass plants. Front Plant Sci 8:642. https://doi.org/10.3389/fpls.2017.00642
Qian L, Chen B, Chen M (2016) Novel alleviation mechanisms of aluminum phytotoxicity via released biosilicon from rice straw-derived biochars. Sci Rep 6:1–11. https://doi.org/10.1038/srep29346
R Core Team (2019) “R: a language and environment for statistical computing; 2015.” 4
Raven JA (1983) The transport and function of silicon in plants. Biol Rev 58:179–207. https://doi.org/10.1111/j.1469-185x.1983.tb00385.x
Sade H, Meriga B, Surapu V, Gadi J, Sunita MSL, Suravajhala P, Kavi Kishor PB (2016) Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils. Biometals 29:187–210. https://doi.org/10.1007/s10534-016-9910-z
dos Santos AR, Melo YL, de Oliveira LF, Cavalcante IE, de Souza Ferraz RL, da Silva Sá FV, de Lacerda CF, de Melo AS (2022) Exogenous silicon and proline modulate osmoprotection and antioxidant activity in cowpea under drought stress. J Soil Sci Plant Nutr 1–8https://doi.org/10.1007/S42729-022-00764-5/FIGURES/3
Sardans J, Peñuelas J (2012) The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiol 160:1741–1761. https://doi.org/10.1104/pp.112.208785
Schaller J, Brackhage C, Dudel EG (2012) Silicon availability changes structural carbon ratio and phenol content of grasses. Environ Exp Bot 77:283–287. https://doi.org/10.1016/j.envexpbot.2011.12.009
Silva BS, Prado RDM, Hurtado AC, Andrade RADE (2020) Ammonia toxicity affects cations uptake and growth in papaya plants inclusive with silicon addition. Acta Biológica Colomb 25:345–353. https://doi.org/10.15446/abc.v25n3.79490
Singh S, Tripathi DK, Singh S, Sharma S, Dubey NK, Chauhan DK, Vaculík M (2017) Toxicity of aluminium on various levels of plant cells and organism: a review. Environ Exp Bot 137:177–193. https://doi.org/10.1016/j.envexpbot.2017.01.005
Souri Z, Khanna K, Karimi N, Ahmad P (2021) Silicon and plants: current knowledge and future prospects. J Plant Growth Regul 40:906–925. https://doi.org/10.1007/s00344-020-10172-7
Sousa Junior GS, Calero Hurtado A, Souza Junior JP, Mello Prado R, Mathias dos Santos DM (2022) Nutritional and structural role of silicon in attenuating aluminum toxicity in sugarcane plants. SILICON 14:5041–5055. https://doi.org/10.1007/s12633-021-01294-y
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere, 1st edn. Princeton University Press, Princeton
Teixeira GCM, de Mello PR, Oliveira KS, D’Amico-Damião V, da Silveira Sousa Junior G (2020) Silicon increases leaf chlorophyll content and iron nutritional efficiency and reduces iron deficiency in sorghum plants. J Soil Sci Plant Nutr in Press. https://doi.org/10.1007/s42729-020-00214-0
Udop (2021) CTC launches variety of sugarcane that produce more adaptable to the Brazilian cerrado
Vaculík M, Lukačová Z, Bokor B, Martinka M, Tripathi DK, Lux A (2020) Alleviation mechanisms of metal(loid) stress in plants by silicon: a review. J Exp Bot 71:6744–6757. https://doi.org/10.1093/jxb/eraa288
Vega I, Nikolic M, Pontigo S, Godoy K, de Mora MLL, Cartes P (2019) Silicon improves the production of high antioxidant or structural phenolic compounds in barley cultivars under aluminum stress. Agronomy 9:388. https://doi.org/10.3390/agronomy9070388
Vega I, Rumpel C, Ruíz A, de la Mora ML, Calderini DF, Cartes P (2020) Silicon modulates the production and composition of phenols in barley under aluminum stress. Agronomy 10:1138. https://doi.org/10.3390/agronomy10081138
Wang Y, Stass A, Horst WJ (2004) Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol 136:3762–3770. https://doi.org/10.1104/pp.104.045005
Zhang J, He Z, Tian H, Zhu G, Peng X (2007) Identification of aluminium-responsive genes in rice cultivars with different aluminium sensitivities. J Exp Bot 58:2269–2278. https://doi.org/10.1093/jxb/erm110
Acknowledgements
Financial support for this work was provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil (Finance Code 001). We would also like to thank São Paulo State University (UNESP), School of Agricultural and Veterinarian Sciences (FCAV), for the facilities given to research.
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The project was financially supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Brazil [Finance Code 001].
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D.M.M.S. and G.S.S.J. designed the study. D.M.M.S. and R.M.P.: resource, reagents, and materials. G.S.S.J. collected samples from all physiological and chemical measurements. M.C.P. helped with the analysis of carbon and nitrogen. G.S.S.J., D.M.M.S., J.P.S.J., and A.C.H. analyzed the data – interpretation and validation. G.S.S.J. and A.C.H. prepared Figs. 1–6. G.S.S.J., D.M.M.S., R.M.P., and A.C.H performed contributions to data. G.S.S.J.: funding acquisition. A.C.H. and G.S.S.J. managed the literature searches and writing the original draft preparation. All authors performed the writing, review, and editing. All authors have read and agreed to the published version of the manuscript.
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da Silveira Sousa Junior, G., Hurtado, A.C., de Souza Junior, J.P. et al. Beneficial Role of Silicon on Regulating C, N, and P Stoichiometric Homeostasis and the Growth of Sugarcane Seedlings under Aluminum Toxicity. J Soil Sci Plant Nutr 22, 4138–4152 (2022). https://doi.org/10.1007/s42729-022-01013-5
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DOI: https://doi.org/10.1007/s42729-022-01013-5