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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Trans-generational effect of cerium oxide-nanoparticles (nCeO2) on Chenopodium rubrum L. and Sinapis alba L. seeds

Ivana Milenković https://orcid.org/0000-0001-7957-4485 A * , Maria Baruh Krstić A , Slađana Z. Spasić A B and Ksenija Radotić A
+ Author Affiliations
- Author Affiliations

A University of Belgrade - Institute for Multidisciplinary Research, Kneza Višeslava 1, Belgrade 11030, Serbia.

B Singidunum University, Danijelova 32, Belgrade 11010, Serbia.

* Correspondence to: ivana.milenkovic@imsi.rs

Handling Editor: Honghong Wu

Functional Plant Biology 50(4) 303-313 https://doi.org/10.1071/FP22213
Submitted: 15 September 2022  Accepted: 26 January 2023   Published: 14 March 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Cerium oxide nanoparticles (nCeO2) are interesting nanomaterials due to their redox properties. Their wide application could result in unexpected consequences to environmental safety. Unlike acute toxicity, the trans-generational effects of carbohydrate-coated nCeO2 in the environment are still unknown. The main aim of this study was to investigate the effect of treating maternal plants of Chenopodium rubrum L. (red goosefoot) and Sinapis alba L. (white mustard) with uncoated (CeO2) and glucose-, levan-, or pullulan-coated nCeO2 (G-, L-, or P-CeO2) during seed germination on morphological and physiological characteristics of produced seeds in two subsequent generations. The plant response was studied by measuring germination percentage (Ger), total protein content (TPC), total phenolic content (TPhC), total antioxidative activity (TAA), and catalase (CAT) activity. Results showed that maternal effects of the different nCeO2 treatments persist to at least the second generation in seeds. Generally, C. rubrum was more sensitive to nCeO2 treatments than S. alba. The coated nCeO2 were more effective than uncoated ones in both plant species; L- and P-CeO2 were the most effective in S. alba, while CeO2 and G-CeO2 had a dominant impact in C. rubrum. Enhanced germination in all tested generations of S. alba seeds recommends nCeO2 for seed priming.

Keywords: CeO2, Chenopodium rubrum, generation, nanoparticles, plants, seed, Sinapis alba, trans-generational effect.


References

Altman DW, McCuistion WL, Kronstad WE (1983) Grain protein percentage, kernel hardness, and grain yield of winter wheat with foliar applied ureal. Agronomy Journal 75, 87–91.
Grain protein percentage, kernel hardness, and grain yield of winter wheat with foliar applied ureal.Crossref | GoogleScholarGoogle Scholar |

An J, Hu P, Li F, Wu H, Shen Y, White JC, Tian X, Li Z, Giraldo JP (2020) Emerging investigator series: molecular mechanisms of plant salinity stress tolerance improvement by seed priming with cerium oxide nanoparticles. Environmental Science: Nano 7, 2214–2228.
Emerging investigator series: molecular mechanisms of plant salinity stress tolerance improvement by seed priming with cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Antony D, Yadav R, Kalimuthu R (2021) Accumulation of phyto-mediated nano-CeO2 and selenium doped CeO2 on Macrotyloma uniflorum (horse gram) seed by nano-priming to enhance seedling vigor. Biocatalysis and Agricultural Biotechnology 31, 101923
Accumulation of phyto-mediated nano-CeO2 and selenium doped CeO2 on Macrotyloma uniflorum (horse gram) seed by nano-priming to enhance seedling vigor.Crossref | GoogleScholarGoogle Scholar |

Asati A, Santra S, Kaittanis C, Perez JM (2010) Surface-charge-dependent cell localization and cytotoxicity of cerium oxide nanoparticles. ACS Nano 4, 5321–5331.
Surface-charge-dependent cell localization and cytotoxicity of cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Asztemborska M, Steborowski R, Kowalska J, Bystrzejewska-Piotrowska G (2015) Accumulation of platinum nanoparticles by Sinapis alba and Lepidium sativum plants. Water, Air, & Soil Pollution 226, 126
Accumulation of platinum nanoparticles by Sinapis alba and Lepidium sativum plants.Crossref | GoogleScholarGoogle Scholar |

Bodson M, King RW, Evans LT, Bernier G (1977) The role of photosynthesis in flowering of the long-day plant Sinapis alba. Functional Plant Biology 4, 467–478.
The role of photosynthesis in flowering of the long-day plant Sinapis alba.Crossref | GoogleScholarGoogle Scholar |

Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar |

Cassee FR, van Balen EC, Singh C, Green D, Muijser H, Weinstein J, Dreher K (2011) Exposure, health and ecological effects review of engineered nanoscale cerium and cerium oxide associated with its use as a fuel additive. Critical Reviews in Toxicology 41, 213–229.
Exposure, health and ecological effects review of engineered nanoscale cerium and cerium oxide associated with its use as a fuel additive.Crossref | GoogleScholarGoogle Scholar |

Donohue K (2009) Completing the cycle: maternal effects as the missing link in plant life histories. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 1059–1074.
Completing the cycle: maternal effects as the missing link in plant life histories.Crossref | GoogleScholarGoogle Scholar |

Herman JJ, Sultan SE (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science 2, 102
Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations.Crossref | GoogleScholarGoogle Scholar |

Hu Z, Richter H, Sparovek G, Schnug E (2004) Physiological and biochemical effects of rare earth elements on plants and their agricultural significance: a review. Journal of Plant Nutrition 27, 183–220.
Physiological and biochemical effects of rare earth elements on plants and their agricultural significance: a review.Crossref | GoogleScholarGoogle Scholar |

Khan MN, Li Y, Fu C, Hu J, Chen L, Yan J, Khan Z, Wu H, Li Z (2022) CeO2 nanoparticles seed priming increases salicylic acid level and ROS scavenging ability to improve rapeseed salt tolerance. Global Challenges 6, 2200025
CeO2 nanoparticles seed priming increases salicylic acid level and ROS scavenging ability to improve rapeseed salt tolerance.Crossref | GoogleScholarGoogle Scholar |

King RW (1979) Photoperiodic time measurement and effects of temperature on flowering in Chenopodium rubrum L. Australian Journal of Plant Physiology 6, 417–422.
Photoperiodic time measurement and effects of temperature on flowering in Chenopodium rubrum L.Crossref | GoogleScholarGoogle Scholar |

Kulbat K (2016) The role of phenolic compounds in plant resistance. Biotechnology and Food Sciences 80, 97–108.

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar |

Layet C, Auffan M, Santaella C, Chevassus-Rosset C, Montes M, Ortet P, Barakat M, Collin B, Legros S, Bravin MN, Angeletti B, Kieffer I, Proux O, Hazemann J-L, Doelsch E (2017) Evidence that soil properties and organic coating drive the phytoavailability of cerium oxide nanoparticles. Environmental Science & Technology 51, 9756–9764.
Evidence that soil properties and organic coating drive the phytoavailability of cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |

López-Moreno ML, de la Rosa G, Hernández-Viezcas JÁ, Castillo-Michel H, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL (2010) Evidence of the differential biotransformation and genotoxicity of ZnO and CeO2 nanoparticles on soybean (Glycine max) plants. Environmental Science & Technology 44, 7315–7320.
Evidence of the differential biotransformation and genotoxicity of ZnO and CeO2 nanoparticles on soybean (Glycine max) plants.Crossref | GoogleScholarGoogle Scholar |

Ma X, Wang Q, Rossi L, Ebbs SD, White JC (2016) Multigenerational exposure to cerium oxide nanoparticles: physiological and biochemical analysis reveals transmissible changes in rapid cycling Brassica rapa. NanoImpact 1, 46–54.
Multigenerational exposure to cerium oxide nanoparticles: physiological and biochemical analysis reveals transmissible changes in rapid cycling Brassica rapa.Crossref | GoogleScholarGoogle Scholar |

Milenković I, Radotić K, Matović B, Prekajski M, Živković L, Jakovljević D, Gojgić-Cvijović G, Beškoski V (2018) Improving stability of cerium oxide nanoparticles by microbial polysaccharides coating. Journal of the Serbian Chemical Society 83, 745–757.
Improving stability of cerium oxide nanoparticles by microbial polysaccharides coating.Crossref | GoogleScholarGoogle Scholar |

Milenković I, Mitrović A, Algarra M, Lázaro-Martínez JM, Rodríguez-Castellón E, Maksimović V, Spasić SZ, Beškoski VP, Radotić K (2019) Interaction of carbohydrate coated cerium-oxide nanoparticles with wheat and pea: stress induction potential and effect on development. Plants 8, 478
Interaction of carbohydrate coated cerium-oxide nanoparticles with wheat and pea: stress induction potential and effect on development.Crossref | GoogleScholarGoogle Scholar |

Milenković I, Radotić K, Despotović J, Lončarević B, Lješević M, Spasić SZ, Nikolić A, Beškoski VP (2021) Toxicity investigation of CeO2 nanoparticles coated with glucose and exopolysaccharides levan and pullulan on the bacterium Vibrio fischeri and aquatic organisms Daphnia magna and Danio rerio. Aquatic Toxicology 236, 105867
Toxicity investigation of CeO2 nanoparticles coated with glucose and exopolysaccharides levan and pullulan on the bacterium Vibrio fischeri and aquatic organisms Daphnia magna and Danio rerio.Crossref | GoogleScholarGoogle Scholar |

Mitrović A, Dučić T, Lirić-Rajlić I, Radotić K, Živanović B (2005) Changes in Chenopodium rubrum seeds with aging. Annals of the New York Academy of Sciences 1048, 505–508.
Changes in Chenopodium rubrum seeds with aging.Crossref | GoogleScholarGoogle Scholar |

Mitrović A, Bogdanović J, Giba Z, Ćulafić L (2010) Effect of photoperiod during growth of Chenopodium rubrum mother plants on properties of offspring. Biologia Plantarum 54, 735–739.
Effect of photoperiod during growth of Chenopodium rubrum mother plants on properties of offspring.Crossref | GoogleScholarGoogle Scholar |

Mitrović PM, Stamenković OS, Banković-Ilić I, Djalović IG, Nježić ZB, Farooq M, Siddique KHM, Veljković VB (2020) White mustard (Sinapis alba L.) oil in biodiesel production: a review. Frontiers in Plant Science 11, 299
White mustard (Sinapis alba L.) oil in biodiesel production: a review.Crossref | GoogleScholarGoogle Scholar |

Pehlivan FE (2017) Free radicals and antioxidant system in seed biology. In ‘Advances in seed biology’. (Ed. JC Jimenez-Lopez) p. 167. (InTech: London, UK)

Rico CM, Morales MI, Barrios AC, McCreary R, Hong J, Lee W-Y, Nunez J, Peralta-Videa JR, Gardea-Torresdey JL (2013) Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains. Journal of Agricultural and Food Chemistry 61, 11278–11285.
Effect of cerium oxide nanoparticles on the quality of rice (Oryza sativa L.) grains.Crossref | GoogleScholarGoogle Scholar |

Rico CM, Johnson MG, Marcus MA, Andersen CP (2017) Intergenerational responses of wheat (Triticum aestivum L.) to cerium oxide nanoparticles exposure. Environmental Science: Nano 4, 700–711.
Intergenerational responses of wheat (Triticum aestivum L.) to cerium oxide nanoparticles exposure.Crossref | GoogleScholarGoogle Scholar |

Rico CM, Abolade OM, Wagner D, Lottes B, Rodriguez J, Biagioni R, Andersen CP (2020a) Wheat exposure to cerium oxide nanoparticles over three generations reveals transmissible changes in nutrition, biochemical pools, and response to soil N. Journal of Hazardous Materials 384, 121364
Wheat exposure to cerium oxide nanoparticles over three generations reveals transmissible changes in nutrition, biochemical pools, and response to soil N.Crossref | GoogleScholarGoogle Scholar |

Rico CM, Wagner D, Abolade O, Lottes B, Coates K (2020b) Metabolomics of wheat grains generationally-exposed to cerium oxide nanoparticles. Science of The Total Environment 712, 136487
Metabolomics of wheat grains generationally-exposed to cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16, 144–158.

Skiba E, Pietrzak M, Gapińska M, Wolf WM (2020) Metal homeostasis and gas exchange dynamics in Pisum sativum L. exposed to cerium oxide nanoparticles. International Journal of Molecular Sciences 21, 8497
Metal homeostasis and gas exchange dynamics in Pisum sativum L. exposed to cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |

Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiology 127, 426–435.
Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system.Crossref | GoogleScholarGoogle Scholar |

Wang Q, Ebbs SD, Chen Y, Ma X (2013) Trans-generational impact of cerium oxide nanoparticles on tomato plants. Metallomics 5, 753–759.
Trans-generational impact of cerium oxide nanoparticles on tomato plants.Crossref | GoogleScholarGoogle Scholar |

Xue Y, Luan Q, Yang D, Yao X, Zhou K (2011) Direct evidence for hydroxyl radical scavenging activity of cerium oxide nanoparticles. The Journal of Physical Chemistry C 115, 4433–4438.
Direct evidence for hydroxyl radical scavenging activity of cerium oxide nanoparticles.Crossref | GoogleScholarGoogle Scholar |