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Rational Design Principles for the Transport and Subcellular Distribution of Nanomaterials into Plant Protoplasts

Journal Article · · Small
 [1];  [2];  [2];  [2];  [2];  [2]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); DOE/OSTI
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

The ability to control the subcellular localization of nanoparticles within living plants offers unique advantages for targeted biomolecule delivery and enables important applications in plant bioengineering. However, the mechanism of nanoparticle transport past plant biological membranes is poorly understood. Here, a mechanistic study of nanoparticle cellular uptake into plant protoplasts is presented. An experimentally validated mathematical model of lipid exchange envelope penetration mechanism for protoplasts, which predicts that the subcellular distribution of nanoparticles in plant cells is dictated by the particle size and the magnitude of the zeta potential, is advanced. The mechanism is completely generic, describing nanoparticles ranging from quantum dots, gold and silica nanoparticles, nanoceria, and single-walled carbon nanotubes (SWNTs). In addition, the use of imaging flow cytometry to investigate the influence of protoplasts' morphological characteristics on nanoparticle uptake efficiency is demonstrated. Using DNA-wrapped SWNTs as model nanoparticles, it is found that glycerolipids, the predominant lipids in chloroplast membranes, exhibit stronger lipid–nanoparticle interaction than phospholipids, the major constituent in protoplast membrane. This work can guide the rational design of nanoparticles for targeted delivery into specific compartments within plant cells without the use of chemical or mechanical aid, potentially enabling various plant engineering applications.

Research Organization:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
FG02-08ER46488
OSTI ID:
1609981
Alternate ID(s):
OSTI ID: 1469026
Journal Information:
Small, Journal Name: Small Journal Issue: 44 Vol. 14; ISSN 1613-6810
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English

References (87)

Application of Nanoparticle Antioxidants to Enable Hyperstable Chloroplasts for Solar Energy Harvesting journal March 2013
Functionalized Carbon Nanotubes for Plasmid DNA Gene Delivery journal October 2004
Functionalized Carbon Nanotubes for Plasmid DNA Gene Delivery journal October 2004
Enhancement of biomolecule transport by electroporation: A review of theory and practical application to transformation ofCorynebacterium glutamicum journal January 2006
Synthesis of Water-Soluble Blue Photoluminescent Silicon Nanocrystals with Oxide Surface Passivation journal January 2009
On The Mechanical and Dynamic Properties of Plant Cell Membranes: Their Role in Growth, Direct Gene Transfer and Protoplast Fusion journal January 1993
Hybrid genes in the analysis of transformation conditions: I. Setting up a simple method for direct gene transfer in plant protoplasts journal January 1987
Transient gene expression in electroporated Solanum protoplasts journal November 1989
Electroporation-mediated infection of tobacco leaf protoplasts with tobacco mosaic virus RNA and cucumber mosaic virus RNA journal February 1986
Surface charge of protoplasts and their significance in cell-cell interaction journal January 1978
The thickness, composition and structure of some lipid bilayers and natural membranes journal September 1971
Cell Surface Area Regulation and Membrane Tension journal January 2001
Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol journal June 2007
Highly efficient uptake of ultrafine mesoporous silica nanoparticles with excellent biocompatibility by Liriodendron hybrid suspension cells journal December 2012
Plant lipids and their role in membrane function journal January 1979
Biochemical and biophysical properties of thylakoid acyl lipids journal October 1991
Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order journal September 2002
Dielectric spectroscopy of plant protoplasts journal December 1992
Non-endocytic penetration of core histones into petunia protoplasts and cultured cells: a novel mechanism for the introduction of macromolecules into plant cells journal August 2004
Laurdan fluorescence spectroscopy in the thylakoid bilayer: The effect of violaxanthin to zeaxanthin conversion on the galactolipid dominated lipid environment journal January 2008
Cellular Image Analysis and Imaging by Flow Cytometry journal September 2007
Assessment of cell wall porosity in Arabidopsis thaliana by NMR spectroscopy journal March 2008
A simple and effective method to encapsulate tobacco mesophyll protoplasts to maintain cell viability journal January 2015
Molecular Insight into the Line Tension of Bilayer Membranes Containing Hybrid Polyunsaturated Lipids journal February 2017
Lipid Exchange Envelope Penetration (LEEP) of Nanoparticles for Plant Engineering: A Universal Localization Mechanism journal January 2016
A Nanobionic Light-Emitting Plant journal November 2017
Urea-Hydroxyapatite Nanohybrids for Slow Release of Nitrogen journal January 2017
Chemical Basis of Interactions Between Engineered Nanoparticles and Biological Systems journal June 2014
Root Uptake and Phytotoxicity of ZnO Nanoparticles journal August 2008
Bioconjugated Nanoparticles for DNA Protection from Cleavage journal June 2003
Coating Single-Walled Carbon Nanotubes with Phospholipids journal February 2006
Debundling of Single-Walled Nanotubes by Dilution:  Observation of Large Populations of Individual Nanotubes in Amide Solvent Dispersions journal August 2006
Direct Synthesis of Nanoceria in Aqueous Polyhydroxyl Solutions journal October 2007
Self-Assembly of Lipids and Single-Walled Carbon Nanotubes: Effects of Lipid Structure and PEGylation journal April 2012
Interparticle Dispersion, Membrane Curvature, and Penetration Induced by Single-Walled Carbon Nanotubes Wrapped with Lipids and PEGylated Lipids journal January 2013
Cationic Au Nanoparticle Binding with Plasma Membrane-like Lipid Bilayers: Potential Mechanism for Spontaneous Permeation to Cells Revealed by Atomistic Simulations journal May 2014
Homogeneous Hydrophobic–Hydrophilic Surface Patterns Enhance Permeation of Nanoparticles through Lipid Membranes journal May 2013
Spectroscopy of Single- and Double-Wall Carbon Nanotubes in Different Environments journal March 2005
Carbon Nanotubes as Molecular Transporters for Walled Plant Cells journal March 2009
Enhanced Gene Delivery and siRNA Silencing by Gold Nanoparticles Coated with Charge-Reversal Polyelectrolyte journal August 2010
Surface Patterning of Carbon Nanotubes Can Enhance Their Penetration through a Phospholipid Bilayer journal January 2011
Functional Platform for Controlled Subcellular Distribution of Carbon Nanotubes journal October 2011
Designing Nanoparticle Translocation through Membranes by Computer Simulations journal January 2012
Cellular Uptake of Nanoparticles by Membrane Penetration: A Study Combining Confocal Microscopy with FTIR Spectroelectrochemistry journal January 2012
Nanoparticle-Induced Permeability of Lipid Membranes journal November 2012
Ultrasmall Gold Nanoparticles as Carriers for Nucleus-Based Gene Therapy Due to Size-Dependent Nuclear Entry journal May 2014
Carbon Nanotubes Protect DNA Strands during Cellular Delivery journal October 2008
In vitro transformation of plant protoplasts with Ti-plasmid DNA journal March 1982
High-velocity microprojectiles for delivering nucleic acids into living cells journal May 1987
Enhancement of transfection by physical concentration of DNA at the cell surface journal August 2000
Protein-targeted corona phase molecular recognition journal January 2016
Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles journal May 2008
Plant nanobionics approach to augment photosynthesis and biochemical sensing journal March 2014
Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics journal October 2016
Mesoporous silica nanoparticles deliver DNA and chemicals into plants journal April 2007
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis journal June 2007
Translocation of polyarginines and conjugated nanoparticles across asymmetric membranes journal January 2013
Calcium phosphate nanoparticle mediated genetic transformation in plants journal January 2012
A simple plant gene delivery system using mesoporous silica nanoparticles as carriers journal January 2013
Organically modified silica nanoparticles: A nonviral vector for in vivo gene delivery and expression in the brain journal July 2005
Nanoparticle-induced surface reconstruction of phospholipid membranes journal November 2008
Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons journal February 2013
Plant nanobionic materials with a giant temperature response mediated by pectin-Ca 2+ journal March 2015
Expression of genes transferred into monocot and dicot plant cells by electroporation. journal September 1985
Signal Transduction in Maize and Arabidopsis Mesophyll Protoplasts journal December 2001
Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions) journal September 1995
One Protoplast Is Not the Other! journal March 2011
Mechanical Properties of the Plasma Membrane of Isolated Plant Protoplasts: Mechanism of Hyperosmotic and Extracellular Freezing Injury journal February 1983
A Polyethylene Glycol-Mediated Protoplast Transformation System for Production of Fertile Transgenic Rice Plants journal July 1990
Physical Trauma and Tungsten Toxicity Reduce the Efficiency of Biolistic Transformation journal March 1992
Molecular biology of the plasma membrane of higher plants. journal October 1989
Transient transformation of Arabidopsis leaf protoplasts: a versatile experimental system to study gene expression journal March 1994
Polyethylene glycol and electric field treatment of plant protoplasts: characterization of some membrane properties journal July 1986
Optical Detection of DNA Conformational Polymorphism on Single-Walled Carbon Nanotubes journal January 2006
Determination of the Pore Size of Cell Walls of Living Plant Cells journal September 1979
Nanosensor Technology Applied to Living Plant Systems journal June 2017
Role of the Plasma Membrane in Freezing Injury and Cold Acclimation journal June 1984
Free Volume Properties of Sphingomyelin, DMPC, DPPC, and PLPC Bilayers journal September 2005
SoyDB: a knowledge database of soybean transcription factors journal January 2010
Imaging Flow Cytometry: Coping with Heterogeneity in Biological Systems journal June 2012
Chemical Basis of Interactions Between Engineered Nanoparticles and Biological Systems text January 2014
Urea-Hydroxyapatite Nanohybrids for Slow Release of Nitrogen text January 2017
journal January 2002
Molecular Biology of the Plasma Membrane of Higher Plants journal October 1989
Vehicles and ways for efficient nuclear transformation in plants journal November 2010
Fluid Phase Endocytic Uptake of Artificial Nano-Spheres and Fluorescent Quantum Dots by Sycamore Cultured Cells: Evidence for the Distribution of Solutes to Different Intracellular Compartments journal July 2006
Surface patterning of carbon nanotubes can enhance their penetration through a phospholipid bilayer text January 2012

Cited By (4)

The Emergence of Plant Nanobionics and Living Plants as Technology journal November 2019
Enhancing bioelectricity generation in microbial fuel cells and biophotovoltaics using nanomaterials journal June 2019
Chloroplast-selective gene delivery and expression in planta using chitosan-complexed single-walled carbon nanotube carriers journal February 2019
High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants journal February 2019

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