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DNA–Carbon Nanotube Binding Mode Determines the Efficiency of Carbon Nanotube-Mediated DNA Delivery to Intact Plants

Ali, Zahir and Serag, Maged F. and Demirer, Gozde S. and Torre, Bruno and di Fabrizio, Enzo and Landry, Markita P. and Habuchi, Satoshi and Mahfouz, Magdy (2022) DNA–Carbon Nanotube Binding Mode Determines the Efficiency of Carbon Nanotube-Mediated DNA Delivery to Intact Plants. ACS Applied Nano Materials, 5 (4). pp. 4663-4676. ISSN 2574-0970. doi:10.1021/acsanm.1c03482. https://resolver.caltech.edu/CaltechAUTHORS:20220324-689513000

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Abstract

Efficient delivery of DNA, RNA, and genome engineering machinery to plant cells will enable efforts to genetically modify plants for global food security, sustainable energy production, synthetic biology applications, and climate change resilience. For the delivery of functional genetic units into plant cells, nanoparticles, particularly carbon nanotubes (CNTs), have attracted considerable interest. Although some success has been achieved using CNT-based approaches, the efficiency and practicality of the method for genome editing applications remain elusive. This is partly due to insufficient knowledge about the mechanisms of CNT-mediated delivery and expression of CNT-condensed DNA in plants. Here, we characterize the transcription and transformation efficiency of DNA deposited on CNTs coated with positively charged polymers by applying multiple experimental settings and reporter systems controlling the delivery and expression of DNA in plants. We found that the formation of partially condensed DNA on the CNT surface is a prerequisite for transfection and expression. In addition, we show that DNA irreversibly binds to the CNT and does not detach completely from the CNT surface. These results, together with an in vitro transcription assay, suggest that only the partially condensed part of the DNA is accessible to the cellular transcription machinery. Thus, the overall transcription and translation efficiency remains low, in particular for the large DNA units that are required for genome editing applications. Understanding the underlying mechanisms and limitations of CNT-mediated delivery of DNA through the plant cell wall is of considerable importance in guiding efforts to design nanomaterials for efficient transformation, agricultural trait engineering, and synthetic biology applications.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1021/acsanm.1c03482DOIArticle
ORCID:
AuthorORCID
Ali, Zahir0000-0002-7814-8908
Serag, Maged F.0000-0002-6153-1089
Demirer, Gozde S.0000-0002-3007-1489
Torre, Bruno0000-0002-6056-3759
di Fabrizio, Enzo0000-0001-5886-4678
Landry, Markita P.0000-0002-5832-8522
Habuchi, Satoshi0000-0002-6663-2807
Mahfouz, Magdy0000-0002-0616-6365
Additional Information:© 2022 The Authors. Published by American Chemical Society. ACS AuthorChoice - Attribution 4.0 International (CC BY 4.0). Received 1 November 2021. Accepted 14 March 2022. Published online 23 March 2022. The authors would like to thank the members of the genome engineering and synthetic biology laboratory for insightful discussions and technical support. This work was supported by KAUST grant to M. Mahfouz. This study was supported by the King Abdullah University of Science and Technology (KAUST) and the KAUST Office of Sponsored Research (OSR) under Award No. OSR-CRG2020-4390. Author Contributions. Z.A. and M.F.S. contributed equally to this work. M.M.M., S.H., and M.P.L. conceived research. Z.A. and M.F.S. designed the research. Z.A., M.F.S., G.S.D., and B.T. performed the research. Z.A., M.F.S., M.M.M., and S.H. wrote the paper with input from M.P.L., G.S.D., M.F.S., B.T., and E.d.F. The authors declare no competing financial interest.
Funders:
Funding AgencyGrant Number
King Abdullah University of Science and TechnologyOSR-CRG2020-4390
Subject Keywords:carbon nanotubes; DNA; plant cell; gene delivery; genetic transformation; plants genome engineering; nanobiotechnology
Issue or Number:4
DOI:10.1021/acsanm.1c03482
Record Number:CaltechAUTHORS:20220324-689513000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220324-689513000
Official Citation:DNA–Carbon Nanotube Binding Mode Determines the Efficiency of Carbon Nanotube-Mediated DNA Delivery to Intact Plants. Zahir Ali, Maged F. Serag, Gozde S. Demirer, Bruno Torre, Enzo di Fabrizio, Markita P. Landry, Satoshi Habuchi, and Magdy Mahfouz. ACS Applied Nano Materials 2022 5 (4), 4663-4676; DOI: 10.1021/acsanm.1c03482
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114071
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:25 Mar 2022 17:45
Last Modified:26 Apr 2022 16:44

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