Research Progress on Application of Carbon Nanomaterials in Plant Gene Transfection
LIU Wen-Jing1, ZHU Sheng-Jie2, LIU Xiang2, HUANG Hou-Jin1,*
1 School of Chemical and Environmental Engineering, Shanghai Institute of Technology, Shanghai 201418, China; 2 School of Ecological Technology and Engineering, Shanghai Institute of Technology, Shanghai 201418, China
Abstract：Carbon nanomaterials demonstrate significant potential in plant gene transfection due to their superior physicochemical properties and biocompatibility. They can effectively penetrate plant cell walls, markedly enhancing gene delivery efficiency while protecting exogenous genes from degradation and inactivation. Surface functionalization further optimizes their targeting and gene expression capabilities, rendering them crucial tools for plant genetic engineering. However, their biosafety and environmental impact require further investigation. This review provides an in-depth analysis of their application progress in plant gene transfection, covering carbon dots, carbon nanotubes, graphene, fullerenes, and carbon nanofibers, and explores their potential in improving gene delivery efficiency and precise expression, and discusses their biosafety and environmental impact. This review offers theoretical and experimental guidance for plant genetic engineering applications.
[1] 曹凡, 吴玲, 谷青青, 等. 2023. 碳纳米管在植物繁育中的应用研究进展[J]. 世界林业研究, 36(3): 28-32. (Cao F, Wu L, Gu Q Q, et al.2023. Research progress on the application of carbon nanotubes in plant breeding[J]. World Forestry Research, 36(3): 28-32.) [2] 程莎, 类延华, 李环亭, 等. 2023. 石墨烯材料在农业领域的研究进展[J]. 中国农学通报, 39(24): 108-113. (Cheng S, Lei Y H, Li, H T, et al.2023. Research progress of graphene materials in agriculture[J]. Chinese Agronomy Bulletin, 39(24): 108-113.) [3] 葛赛, 韩亚梅, 孙曼銮, 等. 2024. 氧化石墨烯应用于农林种植业中的研究进展[J]. 植物科学学报, 42(3): 395-403. (Ge S, Han Y M, Sun M L, et al.2024. Progress of graphene oxide application in agroforestry[J]. Journal of Plant Sciences, 42(3): 395-403.) [4] 刘晶慧, 姚晓青, 罗军玲, 等. 2024. 利用单壁碳纳米管介导植物瞬时遗传转化的研究[J]. 中国油料作物学报, 46(1): 84-91. (Liu J H, Yao X Q, Luo J L, et al.2024. A study on the use of single-walled carbon nanotubes to mediate transient genetic transformation in plants[J]. Chinese Journal of Oil Crop Sciences, 46(1): 84-91.) [5] 孙晓丽, 汤素雷, 王慕华, 等. 2025. 碳点在促进植物生长领域的研究进展[J]. 天津科技大学学报, 1-9. (Sun X l, Tang S L, Wang M H, et al.2025. Research progress of carbon dots in the field of promoting plant growth[J]. Journal of Tianjin University of Science and Technology, 1-9.) [6] 吴腾飞, 唐拴虎, 黄建凤, 等. 2023. 氧化石墨烯在农业领域的应用研究进展[J]. 广东农业科学, 50(8): 126-135. (Wu T F, Tang S H, Huang J F, et al.2023. Progress of graphene oxide in agriculture[J]. Guangdong Agricultural Science, 50(8): 126-135.) [7] 杨沁, 刘灿玉, 樊继德, 等. 2025. 碳点在植物上的应用研究进展[J]. 现代农业科技, (4): 85-89. (Yang Q, Liu C, Fan J, et al. 2025. Research progress on the application of carbon dots in plants[J]. Modern Agricultural Science and Technology, (4): 85-89.) [8] Abd-Elsalam K A.2024. Special issue: Agricultural nanotechnology[J]. Plants, 13(4): 489. [9] Ali S, Ahmad N, Dar M A, et al.2023. Nano-agrochemicals as substitutes for pesticides: Prospects and risks[J]. Plants, 13(1): 109. [10] Ali Z, Serag M F, Demirer G S, et al.2022. DNA-carbon nanotube binding mode determines the efficiency of carbon nanotube-mediated DNA delivery to intact plants[J]. ACS Applied Nano Materials, 5(4): 4663-4676. [11] Alghuthaymi M A, Ahmad A, Khan Z, et al.2021. Exosome/liposome-like nanoparticles: New carriers for CRISPR genome editing in plants[J]. International Journal of Molecular Sciences, 22(14): 7456. [12] Aziza A A, Ola A G, Mohamed F M E S.2018. Enhancement of somaclonal variations and genetic diversity using graphite nanoparticles (GtNPs) in sweet potato plants[J]. African Journal of Biotechnology, 17(27): 847-855. [13] Chang X L, Ruan L, Yang S T, et al.2014. Quantification of carbon nanomaterials in vivo: Direct stable isotope labeling on the skeleton of fullerene C60[J]. Environmental Science: Nano, 1(1): 64-70. [14] Chen L, Wang C, Li H, et al.2017. Bioaccumulation and toxicity of 13 C-skeleton labeled graphene oxide in wheat[J]. Environmental Science & Technology, 51(17): 10146-10153. [15] Chen Z, Zhao J, Cao J, et al.2022. Opportunities for graphene, single-walled and multi-walled carbon nanotube applications in agriculture: A review[J]. Crop Design, 1(1): 100006. [16] Davern S M, McKnight T E, Standaert R F, et al.2016. Carbon nanofiber arrays: A novel tool for microdelivery of biomolecules to plants[J]. PLOS ONE, 11(4): e0153621. [17] Demirer G S, Zhang H, Matos J L, et al.2019. High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants[J]. Nature Nanotechnology, 14(5): 456-464. [18] Demirer G S, Silva T N, Jackson C T, et al.2021. Nanotechnology to advance CRISPR-Cas genetic engineering of plants[J]. Nature Nanotechnology, 16(3): 243-250. [19] Delgado-Martín J, Delgado-Olidén A, Velasco L.2022. Carbon dots boost dsRNA delivery in plants and increase local and systemic siRNA production[J]. International Journal of Molecular Sciences, 23(10): 5338. [20] Dong H, Ding L, Yan F, et al.2011. The use of polyethylenimine-grafted graphene nanoribbon for cellular delivery of locked nucleic acid modified molecular beacon for recognition of microRNA[J]. Biomaterials, 32(15): 3875-3882. [21] Doyle C, Higginbottom K, Swift T A, et al.2019.A simple method for spray-on gene editing in planta[EB/OL]. bioRxiv, https://doi.org/10.1101/805036 [22] El-Bialy S M, El-Mahrouk M E, Elesawy T, et al.2023.Biological nanofertilizers to enhance growth potential of strawberry seedlings by boosting photosynthetic pigments, plant enzymatic antioxidants, and nutritional status[J]. Plants, 12(2): 302. [23] El-Ramady H, Abdalla N, Sári D, et al.2023. Nanofarming: Promising solutions for the future of the global agricultural industry[J]. Agronomy, 13(6): 1600. [24] Feng L, Yang X, Shi X, et al.2013. Polyethylene glycol and polyethylenimine dual‐functionalized nano‐graphene oxide for photothermally enhanced gene delivery[J]. Small, 9(11): 1989-1997. [25] Ferrier D C, Honeychurch K C.2021. Carbon nanotube (CNT)-based biosensors[J]. Biosensors, 11(12): 486. [26] Gao Y, Chen L, Cheng S, et al.2022. An overview of light-mediated impact of graphene oxide on algae: Photo-transform, toxicity and mechanism[J]. Water, 14(19): 2997. [27] Ghosh S, Chatterjee K.2020. Poly (ethylene glycol) functionalized graphene oxide in tissue engineering: A review on recent advances[J]. International Journal of Nanomedicine, 15: 5991-6006. [28] Gogoi N, Susila H, Leach J, et al.2024. Developing frameworks for nanotechnology-driven DNA-free plant ge-nome-editing[J]. Trends in Plant Science, 2024: S1360138524002644. [29] Golestanipour A, Nikkhah M, Aalami A, et al.2018. Gene delivery to tobacco root cells with single-walled carbon nanotubes and cell-penetrating fusogenic peptides[J]. Molecular Biotechnology, 60(12): 863-878. [30] González-Grandío E, Demirer G S, Jackson C T, et al.2021. Carbon nanotube biocompatibility in plants is determined by their surface chemistry[J]. Journal of Nanobiotechnology, 19(1): 431. [31] Imani R, Shao W, Taherkhani S, et al.2016. Dual-functionalized graphene oxide for enhanced siRNA delivery to breast cancer cells[J]. Colloids and Surfaces B: Biointerfaces, 147: 315-325. [32] Ingle P U, Shende S S, Shingote P R, et al.2022. Chitosan nanoparticles (ChNPs): A versatile growth promoter in modern agricultural production[J]. Heliyon, 8(11): e11893. [33] Jasim M M, Al-Tikrity S F S.2023. Depositing layers of nano graphene on P-type Silicon substrate and studying the structural and optical properties[J]. Journal for Research in Applied Sciences and Biotechnology, 2(5): 83-88. [34] Kanaoujiya R, Saroj S K, Rajput V D, et al.2023. Emerging application of nanotechnology for mankind[J]. Emergent Materials, 6(2): 439-452. [35] Kaphle A, Navya P N, Umapathi A, et al.2018. Nanomaterials for agriculture, food and environment: Applications, toxicity and regulation[J]. Environmental Chemistry Letters, 16(1): 43-58. [36] Khan S, Zahoor M, Sher Khan R, et al.2023. The impact of silver nanoparticles on the growth of plants: The agriculture applications[J]. Heliyon, 9(6): e16928. [37] Komarova T, Ilina I, Taliansky M, et al.2023. Nanoplatforms for the delivery of nucleic acids into plant cells[J]. International Journal of Molecular Sciences, 24(23): 16665. [38] Komisarenko A G, Mykhalska S I, Kurchii V M.2022. Agrobacterium-mediated transformation-method of genetic modification of Triticum aestivum L. plants[J]. Faktori eksperimental'noi Evolucii Organizmiv, 30: 85-90. [39] Kwak S Y, Lew T T S, Sweeney C J, et al.2019. Chloroplast-selective gene delivery and expression in planta using chitosan-complexed single-walled carbon nanotube carriers[J]. Nature Nanotechnology, 14(5): 447-455. [40] Lawal A T, Bolarinwa H S, Animasahun L O, et al.2019.Progress in carbon nanotube-based electrochemical biosensors-A review[J]. Fountain Journal of Natural and Applied Sciences, 8(2): 1-15. [41] Law S S Y, Miyamoto T, Numata K.2023. Organelle-targeted gene delivery in plants by nanomaterials[J]. Chemical Communications, 59(47): 7166-7181. [42] Li S, Li J, Du M, et al.2022. Efficient gene silencing in intact plant cells using siRNA delivered by functional graphene oxide nanoparticles[J]. Angewandte Chemie International Edition, 61(40): e202210014. [43] Liu C, Zhou H, Zhou J.2021. The applications of nanotechnology in crop production[J]. Molecules, 26(23): 7070. [44] Liu J.2020. The development and evaluation of transgenic sorghum lines for con-ferred phenotypes[D]. Thesis for M.S., Kingston, University of Rhode Island, Superviser: Kausch A P, pp. 185. [45] Liu Q, Chen B, Wang Q, et al.2009. Carbon nanotubes as molecular transporters for walled plant cells[J]. Nano Letters, 9(3): 1007-1010. [46] Liu Q, Zhang J, He H, et al.2018. Green preparation of high-yield fluorescent graphene quantum dots from coal-tar-pitch by mild oxidation[J]. Nanomaterials, 8(10): 844. [47] Mahmoud Z H, Ahmed N S, Shamkhi W, et al.2020. Nanoparticles: A review of preparation and characterization of nanoparticles with application[J]. Earthline Journal of Chemical Sciences, 2020: 141-149. [48] Manzoor N, Ali L, Ahmed T, et al.2022. Recent advancements and development in nano-enabled agriculture for improving abiotic stress tolerance in plants[J]. Frontiers in Plant Science, 13: 951752. [49] Martins I, Tomás H, Lahoz F, et al.2021. Engineered fluorescent carbon dots and G4-G6 PAMAM dendrimer nanohybrids for bioimaging and gene delivery[J]. Biomacromolecules, 22(6): 2436-2450. [50] Matthew M A.2021. Effects of suspended multi-walled carbon nanotubes on daphnid growth and reproduction[J]. 74(7): 1839-1843. [51] Morgan J M, Jelenska J, Hensley D, et al.2022. An efficient and broadly applicable method for the transient transformation of plants using vertically aligned carbon nanofiber arrays[J]. Frontiers in Plant Science, 13: 1051340. [52] Morgan J M, Jelenska J, Hensley D K, et al.2023. Using vertically aligned carbon nanofiber arrays on rigid or flexible substrates for delivery of biomolecules and dyes to plants[J]. Journal of Visualized Experiments, (197): 65602. [53] Osmani Z, Wang L, Xiao W, et al.2024. Nanomaterials as tools in plant transformation: A protoplast-centric perspective[J]. Plant Nano Biology, 10: 100100. [54] Pantarotto D, Singh R, McCarthy D, et al.2004. Functionalized carbon nanotubes for plasmid DNA gene delivery[J]. Angewandte Chemie International Edition, 43(39): 5242-5246. [55] Patra J K, Das G, Fraceto L F, et al.2018. Nano based drug delivery systems: Recent developments and future prospects[J]. Journal of Nanobiotechnology, 16(1): 71. [56] Porter A E, Gass M, Muller K, et al.2007. Direct imaging of single-walled carbon nanotubes in cells[J]. Nature Nanotechnology, 2(11): 713-717. [57] Raffa V, Ciofani G, Vittorio O, et al.2010. Physicochemical properties affecting cellular uptake of carbon nanotubes[J]. Nanomedicine, 5(1): 89-97. [58] Rajput V D, Singh A, Minkina T, et al.2021. Nano-enabled products: Challenges and opportunities for sustainable agriculture[J]. Plants, 10(12): 2727. [59] Rai P K, Kumar V, Lee S, et al.2018. Nanoparticle-plant interaction: Implications in energy, environment, and agriculture[J]. Environment International, 119: 1-19. [60] Ray P C, Yu H, Fu P P.2009. Toxicity and environmental risks of nanomaterials: Challenges and future needs[J]. Journal of Environmental Science and Health, Part C, 27(1): 1-35. [61] Roy T, Mamun S M A A. 2022. Carbon nanomaterials towards transformation in agriculture: A review[J]. International Journal of Research Publication and Reviews, 2022: 3730-3735. [62] Rustgi S, Naveed S, Windham J, et al.2022.Plant biomacromolecule delivery methods in the 21st century[J]. Frontiers in Genome Editing, 4: 1011934. [63] Sanzari I, Leone A, Ambrosone A.2019. Nanotechnology in plant science: To make a long story short[J]. Frontiers in Bioengineering and Biotechnology, 7: 120. [64] Schwartz S H, Hendrix B, Hoffer P, et al.2020. Carbon dots for efficient small interfering RNA delivery and gene silencing in plants[J]. Plant Physiology, 184(2): 647-657. [65] Shabbir H, Csapó E, Wojnicki M.2023. Carbon quantum dots: The role of surface functional groups and proposed mechanisms for metal ion sensing[J]. Inorganics, 11(6): 262. [66] Shi Q, Wang C L, Zhang H, et al.2020. Trophic transfer and biomagnification of fullerenol nanoparticles in an aquatic food chain[J]. Environmental Science: Nano, 7(4): 1240-1251. [67] Szczepankowska J, Khachatryan G, Khachatryan K, et al.2023. Carbon dots-types, obtaining and application in biotechnology and food technology[J]. International Journal of Molecular Sciences, 24(19): 14984. [68] Tampieri A, Sprio S.2020. Novel Advances and Approaches in Biomedical Materials Based on Calcium Phosphates[M]. Basel, Switzerland: MDPI, pp. 45. [69] Tayeb A, Amini E, Ghasemi S, et al.2018. Cellulose nanomaterials-binding properties and applications: A review[J]. Molecules, 23(10): 2684. [70] Torney F, Trewyn B G, Lin V S Y, et al.2007. Mesoporous silica nanoparticles deliver DNA and chemicals into plants[J]. Nature Nanotechnology, 2(5): 295-300. [71] Tripathi S, Mahra S, Jha VK, et al.2023. Recent advances and perspectives of nanomaterials in agricultural management and associated environmental risk: A review[J]. Nanomaterials, 13(10): 1604. [72] Ur Rahim H, Qaswar M, Uddin M, et al.2021. Nano-enable materials promoting sustainability and resilience in modern agriculture[J]. Nanomaterials, 11(8): 2068. [73] Verma K K, Song X P, Joshi A, et al.2022. Recent trends in nano-fertilizers for sustainable agriculture under climate change for global food security[J]. Nanomaterials, 12(1): 173. [74] Vincent M, De Lázaro I, Kostarelos K.2017. Graphene materials as 2D non-viral gene transfer vector platforms[J]. Gene Therapy, 24(3): 123-132. [75] Wang B, Huang J, Zhang M, et al.2020. Carbon dots enable efficient delivery of functional DNA in plants[J]. ACS Applied Bio Materials, 3(12): 8857-8864. [76] Wang L, Gu D, Su Y, et al.2022a. Easy synthesis and characterization of novel carbon dots using the one-pot green method for cancer therapy[J]. Pharmaceutics, 14(11): 2423. [77] Wang M, He J, Qi G, et al.2024. Potential applications of PEI-loaded graphene oxide quantum dots in safe and efficient DNA delivery[J]. Journal of Drug Delivery Science and Technology, 101: 106146. [78] Wang P, Zhao F J, Kopittke P M.2019. Engineering crops without genome integration using nanotechnology[J]. Trends in Plant Science, 24(7): 574-577. [79] Wang Z, Zhang Z, Zheng D, et al.2022b. Efficient and genotype independent maize transformation using pollen transfected by DNA‐coated magnetic nanoparticles[J]. Journal of Integrative Plant Biology, 64(6): 1145-1156. [80] Willig C.2021. Investigation of genes involved in somatic embryogenesis and plant-Agrobacterium interactions through transcriptional profiling[D]. Thesis for Ph.D., University of Missouri-Columbia, Supervisor: Yang B, pp. 158. [81] Wu Y, An C, Guo Y, et al.2024. Highly aligned graphene aerogels for multifunctional composites[J]. Nano-Micro Letters, 16(1): 118. [82] Xue Y, Liu C, Andrews G, et al.2022. Recent advances in carbon quantum dots for virus detection, as well as inhibition and treatment of viral infection[J]. Nano Convergence, 9(1): 15. [83] Zaytseva O, Neumann G.2016. Carbon nanomaterials: Production, impact on plant development, agricultural and environmental applications[J]. Chemical and Biological Technologies in Agriculture, 3(1): 17. [84] Zhang F, Wang Z, Peijnenburg W J G M, et al.2023. Machine learning-driven QSAR models for predicting the mixture toxicity of nanoparticles[J]. Environment International, 177: 108025. [85] Zhu L, Chen L, Gu J, et al.2022.Carbon-based nanomaterials for sustainable agriculture: Their application as light converters, nanosensors, and delivery tools[J]. Plants, 11(4): 511.
