Enhanced Antiviral Defense Against Begomoviral Infection in Nicotiana Benthamiana Through Strategic Utilization of Fluorescent Carbon Quantum Dots to Activate Plant Immunity

Overview

Journal J Nanobiotechnology

Publisher Biomed Central

Specialty Biotechnology

Date 2024 Nov 15

PMID 39543670

Authors

Tahir Farooq

Muhammad Dilshad Hussain

Yuan Wang

Ali Kamran

Muhammad Umar

Yafei Tang

Zifu He

Xiaoman She

Affiliations

Soon will be listed here.

Abstract

Background: Owing to their unique physiochemical properties, low toxicity, antipathogenic effects and tunability, fluorescent carbon quantum dots (CQDs) represent a new generation of carbon-based nanomaterials. Despite the mounting research on the efficacy of CQDs against resilient plant pathogens, their potential ability to mitigate viral pathogens and the underlying molecular mechanism(s) remain understudied. In this study, we optimized the CQDs to maximize their antiviral effects against a highly pathogenic Begomovirus (cotton leaf curl Multan virus, CLCuMuV) and elucidated the mechanistic pathways associated with CQDs-mediated viral inhibition. To fine-tune the CQDs-induced antiviral effects against CLCuMuV and investigate the underlying molecular mechanisms,we used HR-TEM, XRD, FT-IR, XPS, and UV‒Vis spectrophotometry to characterize the CQDs. SPAD and FluorCam were used for physiological and photosynthetic performance analysis. Transcriptome, RT‒qPCR, integrated bioinformatics and molecular biology were employed to investigate gene expression, viral quantification and data validation.

Results: The application of fluorescent, hexagonal crystalline, UV-absorptive and water-soluble CQDs (0.01 mg/ml) significantly reduced the CLCuMuV titer and mitigated viral symptoms in N. benthamiana at the early (5 dpi) and late (20 dpi) stages of infection. CQDs significantly increased the morphophysiological properties, relative chlorophyll contents and photosynthetic (Fv/Fm, QY_max, NPQ and Rfd) performance of the CLCuMuV-infected plants. While CLCuMuV infection disrupted plant immunity, the CQDs improved the antiviral defense response by regulating important immunity-related genes involved in endocytosis/necroptosis, Tam3-transposase, the ABC transporter/sphingolipid signaling pathway and serine/threonine protein kinase activities. CQDs potentially triggered TSS and TTS alternative splicing events in CLCuMuV-infected plants.

Conclusions: Overall, these findings underscore the antiviral potential of CQDs, their impact on plant resilience, and their ability to modulate gene expression in response to viral stress. This study's molecular insights provide a foundation for further research on nanomaterial applications in plant virology and crop protection, emphasizing the promising role of CQDs in enhancing plant health and combating viral infections.

References

Zhang X, Wang X, Xu K, Jiang Z, Dong K, Xie X . The serine/threonine/tyrosine kinase STY46 defends against hordeivirus infection by phosphorylating γb protein. Plant Physiol. 2021; 186(1):715-730. PMC: 8154058. DOI: 10.1093/plphys/kiab056. View

Wang X, Liu Y, Chen L, Zhao D, Wang X, Zhang Z . Wheat resistome in response to barley yellow dwarf virus infection. Funct Integr Genomics. 2013; 13(2):155-65. DOI: 10.1007/s10142-013-0309-4. View

Snell L, McGaha T, Brooks D . Type I Interferon in Chronic Virus Infection and Cancer. Trends Immunol. 2017; 38(8):542-557. PMC: 8059441. DOI: 10.1016/j.it.2017.05.005. View

Kwee Y, Zhou Y, Fahmi M, Sharon M, Kristanti A . Progress on Applying Carbon Dots for Inhibition of RNA Virus Infection. Nanotheranostics. 2022; 6(4):436-450. PMC: 9428922. DOI: 10.7150/ntno.73918. View

Verma S, Das A, Gantait S, Kumar V, Gurel E . Applications of carbon nanomaterials in the plant system: A perspective view on the pros and cons. Sci Total Environ. 2019; 667:485-499. DOI: 10.1016/j.scitotenv.2019.02.409. View

Guo Y, Zhao W . Hydrothermal synthesis of highly fluorescent nitrogen-doped carbon quantum dots with good biocompatibility and the application for sensing ellagic acid. Spectrochim Acta A Mol Biomol Spectrosc. 2020; 240:118580. DOI: 10.1016/j.saa.2020.118580. View

Xue Y, Liu C, Andrews G, Wang J, Ge Y . Recent advances in carbon quantum dots for virus detection, as well as inhibition and treatment of viral infection. Nano Converg. 2022; 9(1):15. PMC: 8976173. DOI: 10.1186/s40580-022-00307-9. View

Rossner P, Vrbova K, Strapacova S, Rossnerova A, Ambroz A, Brzicova T . Inhalation of ZnO Nanoparticles: Splice Junction Expression and Alternative Splicing in Mice. Toxicol Sci. 2018; 168(1):190-200. PMC: 6390655. DOI: 10.1093/toxsci/kfy288. View

Farooq T, Lin Q, She X, Chen T, Tang Y, He Z . Comparative transcriptome profiling reveals a network of differentially expressed genes in Asia II 7 and MEAM1 whitefly cryptic species in response to early infection of . Front Microbiol. 2022; 13:1004513. PMC: 9577181. DOI: 10.3389/fmicb.2022.1004513. View

10.

Yang M, Ismayil A, Gao T, Ye Z, Yue N, Wu J . Cotton leaf curl Multan virus C4 protein suppresses autophagy to facilitate viral infection. Plant Physiol. 2023; 193(1):708-720. DOI: 10.1093/plphys/kiad235. View

11.

Zhou H, Hirata M, Osawa R, Fujino K, Kishima Y . Detainment of Tam3 Transposase at Plasma Membrane by Its BED-Zinc Finger Domain. Plant Physiol. 2016; 173(2):1492-1501. PMC: 5291012. DOI: 10.1104/pp.16.00996. View

12.

Zhao J, Zhang X, Hong Y, Liu Y . Chloroplast in Plant-Virus Interaction. Front Microbiol. 2016; 7:1565. PMC: 5047884. DOI: 10.3389/fmicb.2016.01565. View

13.

Wang N, Zhao P, Ma Y, Yao X, Sun Y, Huang X . A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance. Philos Trans R Soc Lond B Biol Sci. 2019; 374(1767):20180313. PMC: 6367160. DOI: 10.1098/rstb.2018.0313. View

14.

Xu X, Yu T, Zhang D, Song H, Huang K, Wang Y . Evaluation of the anti-viral efficacy of three different dsRNA nanoparticles against potato virus Y using various delivery methods. Ecotoxicol Environ Saf. 2023; 255:114775. DOI: 10.1016/j.ecoenv.2023.114775. View

15.

Wu G, Cui X, Chen H, Renaud J, Yu K, Chen X . Dynamin-Like Proteins of Endocytosis in Plants Are Coopted by Potyviruses To Enhance Virus Infection. J Virol. 2018; 92(23). PMC: 6232491. DOI: 10.1128/JVI.01320-18. View

16.

Fiallo-Olive E, Navas-Castillo J . Begomoviruses: what is the secret(s) of their success?. Trends Plant Sci. 2023; 28(6):715-727. DOI: 10.1016/j.tplants.2023.01.012. View

17.

Love M, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12):550. PMC: 4302049. DOI: 10.1186/s13059-014-0550-8. View

18.

Du K, Peng D, Wu J, Zhu Y, Jiang T, Wang P . Maize splicing-mediated mRNA surveillance impeded by sugarcane mosaic virus-coded pathogenic protein NIa-Pro. Sci Adv. 2024; 10(34):eadn3010. PMC: 11343020. DOI: 10.1126/sciadv.adn3010. View

19.

Hesketh E, Saunders K, Fisher C, Potze J, Stanley J, Lomonossoff G . The 3.3 Å structure of a plant geminivirus using cryo-EM. Nat Commun. 2018; 9(1):2369. PMC: 6006435. DOI: 10.1038/s41467-018-04793-6. View

20.

Chu J, Newman J, Cho J . Molecular Mimicry of Transposable Elements in Plants. Plant Cell Physiol. 2024; . DOI: 10.1093/pcp/pcae058. View