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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

Cerium oxide nanoparticles promoted lateral root formation in Arabidopsis by modulating reactive oxygen species and Ca2+ level

Guangjing Li A B , Quanlong Gao A B , Ashadu Nyande A B , Zihao Dong A B , Ehtisham Hassan Khan A B , Yuqian Han A B and Honghong Wu https://orcid.org/0000-0001-6629-0280 A B C D *
+ Author Affiliations
- Author Affiliations

A National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, The Center of Crop Nanobiotechnology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China.

B Hubei Hongshan Laboratory, Wuhan 430070, China.

C Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Shenzhen 511464, China.

D Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 511464, China.

* Correspondence to: honghong.wu@mail.hzau.edu.cn

Handling Editor: Sergey Shabala

Functional Plant Biology 51, FP24196 https://doi.org/10.1071/FP24196
Submitted: 13 August 2024  Accepted: 18 September 2024  Published: 4 October 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Roots play an important role in plant growth, including providing essential mechanical support, water uptake, and nutrient absorption. Nanomaterials play a positive role in improving plant root development, but there is limited knowledge of how nanomaterials affect lateral root (LR) formation. Poly (acrylic) acid coated nanoceria (cerium oxide nanoparticles, PNC) are commonly used to improve plant stress tolerance due to their ability to scavenge reactive oxygen species (ROS). However, its impact on LR formation remains unclear. In this study, we investigated the effects of PNC on LR formation in Arabidopsis thaliana by monitoring ROS levels and Ca2+ distribution in roots. Our results demonstrate that PNC significantly promote LR formation, increasing LR numbers by 26.2%. Compared to controls, PNC-treated Arabidopsis seedlings exhibited reduced H2O2 levels by 18.9% in primary roots (PRs) and 40.6% in LRs, as well as decreased O2· levels by 47.7% in PRs and 88.5% in LRs. When compared with control plants, Ca2+ levels were reduced by 35.7% in PRs and 22.7% in LRs of PNC-treated plants. Overall, these results indicate that PNC could enhance LR development by modulating ROS and Ca2+ levels in roots.

Keywords: Ca2+, histochemical staining, laser confocal microscopy, lateral root formation, nanoceria, qPCR, ROS, transmission electron microscopy.

References

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.
| Crossref | Google Scholar |

Andersen CP, King G, Plocher M, Storm M, Pokhrel LR, Johnson MG, Rygiewicz PT (2016) Germination and early plant development of ten plant species exposed to titanium dioxide and cerium oxide nanoparticles. Environmental Toxicology and Chemistry 35, 2223-2229.
| Crossref | Google Scholar | PubMed |

Chen L, Peng Y, Zhu L, Huang Y, Bie Z, Wu H (2022) CeO2 nanoparticles improved cucumber salt tolerance is associated with its induced early stimulation on antioxidant system. Chemosphere 299, 134474.
| Crossref | Google Scholar | PubMed |

Chieb M, Gachomo EW (2023) The role of plant growth promoting rhizobacteria in plant drought stress responses. BMC Plant Biology 23, 407.
| Crossref | Google Scholar | PubMed |

Djanaguiraman M, Nair R, Giraldo JP, Prasad PVV (2018) Cerium oxide nanoparticles decrease drought-induced oxidative damage in sorghum leading to higher photosynthesis and grain yield. ACS Omega 3, 14406-14416.
| Crossref | Google Scholar | PubMed |

Dumanović J, Nepovimova E, Natić M, Kuča K, Jaćević V (2021) The significance of reactive oxygen species and antioxidant defense system in plants: a concise overview. Frontiers in Plant Science 11, 552969.
| Crossref | Google Scholar | PubMed |

Fu C, Khan MN, Yan J, Hong X, Zhao F, Chen L, Ma H, Li Y, Li J, Wu H (2022) Mechanisms of nanomaterials for improving plant salt tolerance. Crop and Environment 2, 92-99.
| Crossref | Google Scholar |

Huang Q, Ayyaz A, Farooq MA, Zhang K, Chen W, Hannan F (2024) Silicon dioxide nanoparticles enhance plant growth, photosynthetic performance, and antioxidants defence machinery through suppressing chromium uptake in Brassica napus L. Environmental Pollution 342, 123013.
| Crossref | Google Scholar | PubMed |

Ji R, Min J, Wang Y, Kronzucker HJ, Shi W (2022) The role of plant growth regulators in modulating root architecture and tolerance to high-nitrate stress in tomato. Frontiers in Plant Science 13, 864285.
| Crossref | Google Scholar | PubMed |

Karakoti AS, Monteiro-Riviere NA, Aggarwal R, Davis JP, Narayan RJ, Self WT, McGinnis J, Seal S (2008) Nanoceria as antioxidant: synthesis and biomedical applications. JOM (1989) 60, 33-37.
| Crossref | Google Scholar | PubMed |

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.
| Crossref | Google Scholar | PubMed |

Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2013) Modulation of antioxidant machinery in α-tocopherol-enriched transgenic Brassica juncea plants tolerant to abiotic stress conditions. Protoplasma 250, 1079-1089.
| Crossref | Google Scholar | PubMed |

Leitão N, Dangeville P, Carter R, Charpentier M (2019) Nuclear calcium signatures are associated with root development. Nature Communications 10, 4865.
| Crossref | Google Scholar | PubMed |

Li Y, Liu J, Fu C, Khan MN, Hu J, Zhao F, Wu H, Li Z (2022) CeO2 nanoparticles modulate Cu-Zn superoxide dismutase and lipoxygenase-IV isozyme activities to alleviate membrane oxidative damage to improve rapeseed salt tolerance. Environmental Science: Nano 9, 1116-1132.
| Crossref | Google Scholar |

Li Y, Xi K, Liu X, Han S, Han X, Li G, Yang L, Ma D, Fang Z, Gong S, Yin J, Zhu Y (2023) Silica nanoparticles promote wheat growth by mediating hormones and sugar metabolism. Journal of Nanobiotechnology 21, 2.
| Crossref | Google Scholar | PubMed |

Liu J, Li G, Chen L, Gu J, Wu H, Li Z (2021) Cerium oxide nanoparticles improve cotton salt tolerance by enabling better ability to maintain cytosolic K+/Na+ ratio. Journal of Nanobiotechnology 19, 153.
| Crossref | Google Scholar | PubMed |

Mase K, Tsukagoshi H (2021) Reactive oxygen species link gene regulatory networks during Arabidopsis root development. Frontiers in Plant Science 12, 660274.
| Crossref | Google Scholar | PubMed |

Nisar M, Ali Z, Ali A, Aman R, Park HJ, Ullah I, Ullah A, Yun DJ (2020) CaСl2 salt signaling in primary root architecture and lateral root emergence in Arabidopsis thaliana. Russian Journal of Plant Physiology 67, 515-520.
| Crossref | Google Scholar |

Orman-Ligeza B, Parizot B, de Rycke R, Fernandez A, Himschoot E, Van Breusegem F (2016) RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 143, 3328-3339.
| Google Scholar | PubMed |

Pasternak T, Palme K, Pérez-Pérez JM (2023) Role of reactive oxygen species in the modulation of auxin flux and root development in Arabidopsis thaliana. The Plant Journal 114, 83-95.
| Crossref | Google Scholar | PubMed |

Peng Y, Chen L, Zhu L, Cui L, Yang L, Wu H, Bie Z (2022) CsAKT1 is a key gene for the CeO2 nanoparticle’s improved cucumber salt tolerance: a validation from CRISPR-Cas9 lines. Environmental Science: Nano 9, 4367-4381.
| Crossref | Google Scholar |

Prakash V, Vishwakarma K, Singh VP, Rai P, Ramawat N, Tripathi DK, Sharma S (2020) NO and ROS implications in the organization of root system architecture. Physiologia Plantarum 168, 473-489.
| Crossref | Google Scholar | PubMed |

Rahmati Ishka M, Brown E, Rosenberg A, Romanowsky S, Davis JA, Choi W-G, Harper JF (2021) Arabidopsis Ca2+-ATPases 1, 2, and 7 in the endoplasmic reticulum contribute to growth and pollen fitness. Plant Physiology 185, 1966-1985.
| Crossref | Google Scholar |

Singh P, Singh RK, Zhou Y, Wang J, Jiang Y, Shen N, Wang Y, Yang L, Jiang M (2022) Unlocking the strength of plant growth promoting Pseudomonas in improving crop productivity in normal and challenging environments: a review. Journal of Plant Interactions 17, 220-238.
| Crossref | Google Scholar |

Skiba E, Pietrzak M, Gapinska 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.
| Crossref | Google Scholar | PubMed |

Su C, Liu L, Liu H, Ferguson BJ, Zou Y, Zhao Y, Wang T, Wang Y, Li X (2016) H2O2 regulates root system architecture by modulating the polar transport and redistribution of auxin. Journal of Plant Biology 59, 260-270.
| Crossref | Google Scholar |

Wang Y, Lv P, Kong L, Shen W, He Q (2021) Nanomaterial-mediated sustainable hydrogen supply induces lateral root formation via nitrate reductase-dependent nitric oxide. Chemical Engineering Journal 405, 126905.
| Crossref | Google Scholar |

Wu H, Tito N, Giraldo JP (2017) Anionic cerium oxide nanoparticles protect plant photosynthesis from abiotic stress by scavenging reactive oxygen species. ACS Nano 11, 11283-11297.
| Crossref | Google Scholar | PubMed |

Yan S, Zhao L, Li H, Zhang Q, Tan J, Huang M, He S, Li L (2013) Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression. Journal of Hazardous Materials 246–247, 110-118.
| Crossref | Google Scholar | PubMed |

Zhang S, Yu R, Yu D, Chang P, Guo S, Yang X, Liu X, Xu C, Hu Y (2022) The calcium signaling module CaM–IQM destabilizes IAA–ARF interaction to regulate callus and lateral root formation. Proceedings of the National Academy of Sciences 119, e2202669119.
| Crossref | Google Scholar |

Zhang W, Fang D, Dong K, Hu F, Ye Z, Cao J (2023) Insights into the environmental factors shaping lateral root development. Physiologia Plantarum 175, e13878.
| Crossref | Google Scholar | PubMed |