Abstract
This study aimed to evaluate the silicon (Si) capacity to attenuate the cadmium (Cd) effects on seed germination and seedling performance of lettuce. The seeds were subjected to three priming levels: without priming, hydropriming, and Si priming. Afterwards, the seeds were placed to germinate on paper moistened with the absence (0 mM) and presence (1 mM) of Cd. Seeds exposed to Cd showed the same percentage of germination verified in seeds unexposed to this metal (99%). Si priming increases 16% the germination speed of seeds not exposed to Cd and promoted greater expression of esterase during seed germination. However, Cd promoted the decrease of the intensity of esterase and acid phosphatase expression, regardless of the seed priming technique used. Although it does not influence the germination percentage of lettuce seeds, Cd markedly reduced the dry weight of seedlings. This harmful effect caused by the Cd was 33% minimized with Si priming. In addition to the lower weight, Cd induced a significant reduction in antioxidant activity in seedlings. However, Si seed priming caused a greater antioxidant activity—with emphasis on catalase—and, consequently, less lipid peroxidation. In conclusion, Si seed priming contributes to minimize the Cd effects in lettuce seedlings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdel Latef AA, Tran LSP (2016) Impacts of priming with silicon on the growth and tolerance of maize plants to alkaline stress. Front Plant Sci 7:243. https://doi.org/10.3389/fpls.2016.00243
Ahsan N, Lee SH, Lee DG, Lee H, Lee SW, Bahk JD, Lee BH (2007) Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. Comptes Rendus Biologies 330:735–746. https://doi.org/10.1016/j.crvi.2007.08.001
Alfenas AC (2006) Eletroforese e marcadores bioquímicos em plantas e microrganismos. Viçosa: UFV, 2v
Alves RDC, Nicolau MCM, Checchio MV, Sousa Junior GDS, Oliveira FDAD, Prado RM, Gratão PL (2020) Salt stress alleviation by seed priming with silicon in lettuce seedlings: an approach based on enhancing antioxidant responses. Bragantia, (AHEAD). https://doi.org/10.1590/1678-4499.20190360
Azevedo RAD, Alas RM, Smith RJ et al (1998) Response of antioxidant enzymes to transfer 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(2):280–292. https://doi.org/10.1034/j.1399-3054.1998.1040217.x
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bench AR, Fenner M, Edwards P (1991) Changes in germinability, ABA contente and ABA embryonic sensitivity in developing seeds of Sorghum bicolor (L.) Moench induced by water stress during grain filling. New Phytol 118:339–347. https://doi.org/10.1111/j.1469-8137.1991.tb00986.x
Biju S, Fuentes S, Gupta D (2017) Silicon improves seed germination and alleviates drought stress in lentil crops by regulating osmolytes, hydrolytic enzymes and antioxidant defense system. Plant Physiol Biochem 119:250–264. https://doi.org/10.1016/j.plaphy.2017.09.001
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(1–2):248–254
Brasil (2009) Regras para Análise de Sementes. Brasília: MAPA/ACS. p 399. https://www.agricultura.gov.br/assuntos/insumos-agropecuarios/arquivos-publicacoes-insumos/2946_regras_analise__sementes.pdf. Accessed 10 Jan 2020
Cai Y, Zhang S, Cai K, Huang F, Pan B, Wang W (2019) Cd accumulation, biomass and yield of rice are varied with silicon application at different growth phases under high concentration cadmium-contaminated soil. Chemosphere 242:125–128. https://doi.org/10.1016/j.chemosphere.2019.125128
Cakmak I, Strbac D, Marschner H (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J Exp Bot 44(1):127–132. https://doi.org/10.1093/jxb/44.1.127
Ellis RH, Roberts EH (1981) The quantification of aging and survival in orthodox seeds. Seed Sci Technol 9:373–409
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia 35:1039–1042
Fessel SA, Vieira RD, Rodrigues TDJD, Fagioli M (2002) Germinação de sementes de alface submetidas a condicionamento osmótico durante o armazenamento. Sci Agric 59:73–77. https://doi.org/10.1590/S0103-90162002000100011
Gallego SM, Benavides MP (2019) Cadmium-induced oxidative and nitrosative stress in plants. In: Cadmium toxicity and tolerance in plants. Academic Press, pp 233–274. https://doi.org/10.1016/C2017-0-02050-5
Gao M, Chang X, Yang Y, Song Z (2020) Foliar graphene oxide treatment increases photosynthetic capacity and reduces oxidative stress in cadmium-stressed lettuce. Plant Physiol Biochem 154:287–294. https://doi.org/10.1016/j.plaphy.2020.06.021
Gou T, Chen X, Han R et al (2020) Silicon can improve seed germination and ameliorate oxidative damage of bud seedlings in cucumber under salt stress. Acta Physiol Plant 42:1–11. https://doi.org/10.1016/j.plaphy.2014.02.009
Hameed A, Hameed A, Ahmad M, Farooq T (2020) Alleviation of cadmium toxicity by mercapto-triazole priming in wheat. Arch Agron Soil Sci 66(11):1467–1480. https://doi.org/10.1080/03650340.2020.1763965
Hassan M, Mansoor S (2017) Priming seeds with phytohormones alleviates cadmium toxicity in mung bean (Vigna radiata L. Wilczek) seedlings. Pak J Bot 49(6):2071–2078
Hu KD, Bai GS, Li WJ, Yan H, Hu LY, Li YH, Zhang H (2015) Sulfur dioxide promotes germination and plays an antioxidant role in cadmium-stressed wheat seeds. Plant Growth Regul 75:271–280. https://doi.org/10.1007/s10725-014-9951-7
Hussain A, Rizwan M, Ali Q, Ali S (2019) Seed priming with silicon nanoparticles improved the biomass and yield while reduced the oxidative stress and cadmium concentration in wheat grains. Environ Sci Pollut Res 26:7579–7588. https://doi.org/10.1007/s11356-019-04210-5
Huybrechts M, Cuypers A, Deckers J, Iven V, Vandionant S, Jozefczak M, Hendrix S (2019) Cadmium and plant development: an agony from seed to seed. Int J Mol Sci 20:3971. https://doi.org/10.3390/ijms20163971
Jaouani K, Karmous I, Ostrowski M, Ferjani EE, Jakubowska A, Chaoui A (2018) Cadmium effects on embryo growth of pea seeds during germination: investigation of the mechanisms of interference of the heavy metal with protein mobilization-related factors. J Plant Physiol 226:64–76. https://doi.org/10.1016/j.jplph.2018.02.009
Kalai T, Bouthour D, Manai J, Bettaieb Ben Kaab L, Gouia H (2016) Salicylic acid alleviates the toxicity of cadmium on seedling growth, amylases and phosphatases activity in germinating barley seeds. Arch Agron Soil Sci 62(6):892–904. https://doi.org/10.1080/03650340.2015.1100295
Karalija E, Selović A (2018) The effect of hydro and proline seed priming on growth, proline and sugar content, and antioxidant activity of maize under cadmium stress. Environ Sci Pollut Res 25(33):33370–33380. https://doi.org/10.1007/s11356-018-3220-7
Khan A, Bilal S, Khan AL et al (2020) Silicon-mediated alleviation of combined salinity and cadmium stress in date palm (Phoenix dactylifera L.) by regulating physio-hormonal alteration. Ecotoxicol Environ Saf 188:109885. https://doi.org/10.1016/j.ecoenv.2019.109885
Kim Y, Khan AL, Waqas M et al (2017) Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: a review. Front Plant Sci 8:510. https://doi.org/10.3389/fpls.2017.00510
Kolahi M, Kazemi EM, Yazdi M et al (2020) Oxidative stress induced by cadmium in lettuce (Lactuca sativa Linn.): oxidative stress indicators and prediction of their genes. Plant Physiol Biochem 146:71–89. https://doi.org/10.1016/j.plaphy.2019.10.032
Kubier A, Wilkin RT, Pichler T (2019) Cadmium in soils and groundwater: a review. Appl Geochem:104388. https://doi.org/10.1016/j.apgeochem.2019.104388
Kumar M, Pant B, Mondal S, Bose B (2016) Hydro and halo priming: influenced germination responses in wheat Var-HUW-468 under heavy metal stress. Acta Physiol Plant 38(9):217. https://doi.org/10.1007/s11738-016-2226-3
Lavres J, Rabêlo FHS, Capaldi FR, dos Reis AR, Rosssi ML, Franco MR et al (2019) Investigation into the relationship among Cd bioaccumulation, nutrient composition, ultrastructural changes and antioxidative metabolism in lettuce genotypes under Cd stress. Ecotoxicol Environ Saf 170:578–589. https://doi.org/10.1016/j.ecoenv.2018.12.033
Lefèvre I, Marchal G, Corréal E, Zanuzzi A, Lutts S (2009) Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regul 59(1):1–11. https://doi.org/10.1007/s10725-009-9382-z
Maguire JD (1962) Speed of germination - aid in selection and evaluation for seedling emergence and vigour. Crop Sci 2:176–177. https://doi.org/10.2135/cropsci1962.0011183X000200020033x
Nabaei M, Amooaghaie R (2019) Interactive effect of melatonin and sodium nitroprusside on seed germination and seedling growth of Catharanthus roseus under cadmium stress. Russ J Plant Physiol:1–12. https://doi.org/10.1134/S1021443719010126
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Pereira AS, Dorneles AOS, Bernardy K, Sasso VM, Bernardy D, Possebom G, Rossato LV, Dressler VL, Tabaldi LA (2018) Selenium and silicon reduce cadmium uptake and mitigate cadmium toxicity in Pfaffia glomerata (Spreng.) Pedersen plants by activation antioxidant enzyme system. Environ Sci Pollut Res 25(19):18548–18558. https://doi.org/10.1007/s11356-018-2005-3
Rostami M, Mohammadi H, Müller T, Mirzaeitalarposhti R (2020) Silicon application affects cadmium translocation and physiological traits of Lallemantia royleana under cadmium stress. J Plant Nutr 43(5):753–761. https://doi.org/10.1080/01904167.2019.1701022
Šabanović M, Parić A, Briga M, Karalija E (2018) Effect of salicylic acid seed priming on resistance to high levels of cadmium in lettuce (Lactuca sativa L.). Genetics & Applications 2(2):67–72. https://doi.org/10.31383/ga.vol2iss2pp67-72
Saboor A, Mustafa G, Arshad M, Ahmad M, Hussain S, Ahmed N, Ahmad S, Shahid M, Ali MA (2019) Seed priming and metal/metalloid stress tolerance in plants. In: Priming and pretreatment of seeds and seedlings. Springer, Singapore, pp 287–311
Silva P, Matos M (2016) Assessment of the impact of aluminum on germination, early growth and free proline content in Lactuca sativa L. Ecotoxicol Environ Saf 131:151–156. https://doi.org/10.1016/j.ecoenv.2016.05.014
Singh S, Prasad SM, Sharma S, Dubey NK, Ramawat N, Prasad R, Singh VP, Tripathi DK, Chauhan DK (2020) Silicon and nitric oxide-mediated mechanisms of cadmium toxicity alleviation in wheat seedlings. Physiol Plant. https://doi.org/10.1111/ppl.13065
Tabelin CB, Igarashi T, Villacorte-Tabelin M, Park I, Opiso EM, Ito M, Hiroyoshi N (2018) Arsenic, selenium, boron, lead, cadmium, copper, and zinc in naturally contaminated rocks: a review of their sources, modes of enrichment, mechanisms of release, and mitigation strategies. Sci Total Environ 645:1522–1553. https://doi.org/10.1016/j.scitotenv.2018.07.103
Wang Y, Yang R, Zheng J, Shen Z, Xu X (2019) Exogenous foliar application of fulvic acid alleviate cadmium toxicity in lettuce (Lactuca sativa L.). Ecotoxicol Environ Saf 167:10–19. https://doi.org/10.1016/j.ecoenv.2018.08.064
Zayneb C, Lamia K, Olfa E, Naïma J, Grubb CD, Bassem K et al (2015) Morphological, physiological and biochemical impact of ink industry effluent on germination of maize (Zea mays), Barley (Hordeum vulgare) and Sorghum (Sorghum bicolor). Bull Environ Contam Toxicol 95(5):687–693. https://doi.org/10.1007/s00128-015-1600-y
Funding
This study was funded by the—Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Financing Code 001.
Author information
Authors and Affiliations
Contributions
Aline Soares Pereira: formal analysis, project administration, writing—original draft. Gabriel Streck Bortolin: formal analysis, project administration, writing—original draft. Athos Odin Severo Dorneles: formal analysis, project administration, writing—original draft. Geri Eduardo Meneghello: formal analysis. Luciano do Amarante: formal analysis. Carlos Rogério Mauch: formal analysis.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent to participate
The authors declare consent to participate.
Consent to publish
The authors declare consent to publish.
Additional information
Responsible Editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 515 kb)
Rights and permissions
About this article
Cite this article
Pereira, A.S., Bortolin, G.S., Dorneles, A.O.S. et al. Silicon seed priming attenuates cadmium toxicity in lettuce seedlings. Environ Sci Pollut Res 28, 21101–21109 (2021). https://doi.org/10.1007/s11356-020-12249-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-12249-y