CaltechAUTHORS
  A Caltech Library Service

Carbon nanotube biocompatibility in plants is determined by their surface chemistry

González-Grandío, Eduardo and Demirer, Gözde S. and Jackson, Christopher T. and Yang, Darwin and Ebert, Sophia and Molawi, Kian and Keller, Harald and Landry, Markita P. (2021) Carbon nanotube biocompatibility in plants is determined by their surface chemistry. Journal of Nanobiotechnology, 19 . Art. No. 431. ISSN 1477-3155. PMCID PMC8686619; PMC8851704. doi:10.1186/s12951-021-01178-8. https://resolver.caltech.edu/CaltechAUTHORS:20220302-323796000

[img] PDF - Published Version
Creative Commons Attribution.

2MB
[img] PDF - Erratum
Creative Commons Attribution.

682kB

Use this Persistent URL to link to this item: https://resolver.caltech.edu/CaltechAUTHORS:20220302-323796000

Abstract

Background. Agriculture faces significant global challenges including climate change and an increasing food demand due to a growing population. Addressing these challenges will require the adoption of transformative innovations into biotechnology practice, such as nanotechnology. Recently, nanomaterials have emerged as unmatched tools for their use as biosensors, or as biomolecule delivery vehicles. Despite their increasingly prolific use, plant-nanomaterial interactions remain poorly characterized, drawing into question the breadth of their utility and their broader environmental compatibility. Results. Herein, we characterize the response of Arabidopsis thaliana to single walled carbon nanotube (SWNT) exposure with two different surface chemistries commonly used for biosensing and nucleic acid delivery: oligonucleotide adsorbed-pristine SWNTs, and polyethyleneimine-SWNTs loaded with plasmid DNA (PEI-SWNTs), both introduced by leaf infiltration. We observed that pristine SWNTs elicit a mild stress response almost undistinguishable from the infiltration process, indicating that these nanomaterials are well-tolerated by the plant. However, PEI-SWNTs induce a much larger transcriptional reprogramming that involves stress, immunity, and senescence responses. PEI-SWNT-induced transcriptional profile is very similar to that of mutant plants displaying a constitutive immune response or treated with stress-priming agrochemicals. We selected molecular markers from our transcriptomic analysis and identified PEI as the main cause of this adverse reaction. We show that PEI-SWNT response is concentration-dependent and, when persistent over time, leads to cell death. We probed a panel of PEI variant-functionalized SWNTs across two plant species and identified biocompatible SWNT surface functionalizations. Conclusions. While SWNTs themselves are well tolerated by plants, SWNTs surface-functionalized with positively charged polymers become toxic and produce cell death. We use molecular markers to identify more biocompatible SWNT formulations. Our results highlight the importance of nanoparticle surface chemistry on their biocompatibility and will facilitate the use of functionalized nanomaterials for agricultural improvement.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1186/s12951-021-01178-8DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc8686619/PubMed CentralArticle
https://doi.org/10.1186/s12951-022-01302-2DOICorrection
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc8851704/PubMed CentralCorrection
ORCID:
AuthorORCID
Demirer, Gözde S.0000-0002-3007-1489
Landry, Markita P.0000-0002-5832-8522
Additional Information:© 2022 BioMed Central © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Received 12 August 2021. Accepted 02 December 2021. Published 20 December 2021. We thank Frederic Bouche, parkjisun from Noun Project, and Natalie Goh for the graphics used in Fig. 1A. The GFP plasmid was obtained from the Sheen Lab (Harvard Medical School). We thank BASF for providing the L-PEI-800 and H-PEI polymers and Elena Kreimer of the Microanalytical Facility at UC Berkeley for running elemental analyses. We acknowledge support a Burroughs Wellcome Fund Career Award at the Scientific Interface (CASI) (to M.P.L.), a Dreyfus foundation award (to M.P.L.), a Beckman Foundation Young Investigator Award (to M.P.L.), an NIH MIRA award (to M.P.L.), an NSF CAREER award (to M.P.L), an NSF CBET award (to M.P.L.), an NSF CGEM award (to M.P.L.), a FFAR Young Investigator award (to M.P.L.), a CZI investigator award (to M.P.L), a Sloan Foundation Award (to M.P.L.), a USDA BBT EAGER award (to M.P.L), a USDA NIFA Award (to M.P.L), a Moore Foundation Award (to M.P.L.), and a DOE office of Science grant with award number DE-SC0020366 (to M.P.L.) and NSF GRFP (to C.T.J.). M.P.L. is a Chan Zuckerberg Biohub investigator, a Hellen Wills Neuroscience Institute Investigator, and an IGI Investigator. Contributions. EG, GSD and MPL conceived the project, designed the experiments and wrote the manuscript. EG, GSD and CTJ performed the experiments. EG and DY performed data analysis. SE, KM and HK synthesised polymers. All authors have edited and commented on the manuscript and have given their approval of the final version. All authors read and approved the final manuscript. Availability of data and materials. Sequencing dataset supporting the conclusions of this article is available in the Gene Expression Omnibus repository [66], under GEO Series accession number GSE172278. The authors declare that they have no competing interests.
Errata:Gonzalez‑Grandio, E., Demirer, G.S., Jackson, C.T. et al. Correction to: Carbon nanotube biocompatibility in plants is determined by their surface chemistry. J Nanobiotechnol 20, 81 (2022). https://doi.org/10.1186/s12951-022-01302-2
Funders:
Funding AgencyGrant Number
Burroughs Wellcome FundUNSPECIFIED
Camille and Henry Dreyfus FoundationUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
NIHUNSPECIFIED
NSF Graduate Research FellowshipUNSPECIFIED
Foundation for Food and Agriculture ResearchUNSPECIFIED
Chan Zuckerberg InitiativeUNSPECIFIED
Alfred P. Sloan FoundationUNSPECIFIED
Department of AgricultureUNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
Department of Energy (DOE)DE-SC0020366
Hellen Wills Neuroscience InstituteUNSPECIFIED
Innovative Genomics InstituteUNSPECIFIED
Subject Keywords:Plant biotechnology, Nanotechnology, DNA delivery, Carbon nanotube, RNA sequencing
PubMed Central ID:PMC8686619; PMC8851704
DOI:10.1186/s12951-021-01178-8
Record Number:CaltechAUTHORS:20220302-323796000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220302-323796000
Official Citation:González-Grandío, E., Demirer, G.S., Jackson, C.T. et al. Carbon nanotube biocompatibility in plants is determined by their surface chemistry. J Nanobiotechnol 19, 431 (2021). https://doi.org/10.1186/s12951-021-01178-8
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:113698
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:03 Mar 2022 15:34
Last Modified:03 Mar 2022 15:36

Repository Staff Only: item control page