Delivered complementation in planta (DCIP) enables measurement of peptide-mediated protein delivery efficiency in plants

Wang, Jeffrey W.; Squire, Henry J.; Goh, Natalie S.; Ni, Heyuan Michael; Lien, Edward; Wong, Cerise; González-Grandío, Eduardo; Landry, Markita P.

doi:10.1038/s42003-023-05191-5

Title: Delivered complementation in planta (DCIP) enables measurement of peptide-mediated protein delivery efficiency in plants

Journal Article · 11 August 2023 · Communications Biology

DOI: https://doi.org/10.1038/s42003-023-05191-5 · OSTI ID:1994906

;

; Goh, Natalie S.;

; Lien, Edward; Wong, Cerise;

;

Abstract Using a fluorescence complementation assay, Delivered Complementation in Planta (DCIP), we demonstrate cell-penetrating peptide-mediated cytosolic delivery of peptides and recombinant proteins in Nicotiana benthamiana. We show that DCIP enables quantitative measurement of protein delivery efficiency and enables functional screening of cell-penetrating peptides for in-planta protein delivery. Finally, we demonstrate that DCIP detects cell-penetrating peptide-mediated delivery of recombinantly expressed proteins such as mCherry and Lifeact into intact leaves. We also demonstrate delivery of a recombinant plant transcription factor, WUSCHEL (AtWUS), into N. benthamiana. RT-qPCR analysis of AtWUS delivery in Arabidopsis seedlings also suggests delivered WUS can recapitulate transcriptional changes induced by overexpression of AtWUS. Taken together, our findings demonstrate that DCIP offers a new and powerful tool for interrogating cytosolic delivery of proteins in plants and highlights future avenues for engineering plant physiology.

View Journal Article

Cite

Export

Save

Research Organization:: Carnegie Inst. of Washington, Washington, DC (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0020366

OSTI ID:: 1994906

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 6; ISSN 2399-3642

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (81)

Detecting Cytosolic Peptide Delivery with the GFP Complementation Assay in the Low Micromolar Range Schmidt, Samuel; Adjobo-Hermans, Merel J. W.; Wallbrecher, Rike Angewandte Chemie International Edition, Vol. 54, Issue 50 https://doi.org/10.1002/anie.201505913	journal	October 2015
Using the Peptide Bp100 as a Cell-Penetrating Tool for the Chemical Engineering of Actin Filaments within Living Plant Cells Eggenberger, Kai; Mink, Christian; Wadhwani, Parvesh ChemBioChem, Vol. 12, Issue 1 https://doi.org/10.1002/cbic.201000402	journal	December 2010
Latrunculin B-Induced Plant Dwarfism: Plant Cell Elongation Is F-Actin-Dependent Baluška, F.; Jasik, J.; Edelmann, H. G. Developmental Biology, Vol. 231, Issue 1 https://doi.org/10.1006/dbio.2000.0115	journal	March 2001
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Cell Wall Porosity and Its Determination Read, Stephen M.; Bacic, Antony Plant Cell Wall Analysis https://doi.org/10.1007/978-3-642-60989-3_4	book	January 1996
Wuschel overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro Bouchabké-Coussa, O.; Obellianne, M.; Linderme, D. Plant Cell Reports, Vol. 32, Issue 5 https://doi.org/10.1007/s00299-013-1402-9	journal	March 2013
Quantitative dot-blot assay for proteins using enhanced chemiluminescence Heinicke, E.; Kumar, U.; Munoz, D. G. Journal of Immunological Methods, Vol. 152, Issue 2 https://doi.org/10.1016/0022-1759(92)90144-I	journal	August 1992
The Stem Cell Population of Arabidopsis Shoot Meristems Is Maintained by a Regulatory Loop between the CLAVATA and WUSCHEL Genes Schoof, Heiko; Lenhard, Michael; Haecker, Achim Cell, Vol. 100, Issue 6 https://doi.org/10.1016/S0092-8674(00)80700-X	journal	March 2000
Visualization of Interactions among bZIP and Rel Family Proteins in Living Cells Using Bimolecular Fluorescence Complementation Hu, Chang-Deng; Chinenov, Yurii; Kerppola, Tom K. Molecular Cell, Vol. 9, Issue 4, p. 789-798 https://doi.org/10.1016/S1097-2765(02)00496-3	journal	April 2002
Translocation and nuclear accumulation of monomer and dimer of HIV-1 Tat basic domain in triticale mesophyll protoplasts Chugh, Archana; Eudes, François Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 3 https://doi.org/10.1016/j.bbamem.2006.11.012	journal	March 2007
Peptide degradation is a critical determinant for cell-penetrating peptide uptake Palm, Caroline; Jayamanne, Mala; Kjellander, Marcus Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 7 https://doi.org/10.1016/j.bbamem.2007.03.029	journal	July 2007
Fluorophore labeling of a cell-penetrating peptide induces differential effects on its cellular distribution and affects cell viability Birch, Ditlev; Christensen, Malene Vinther; Staerk, Dan Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1859, Issue 12 https://doi.org/10.1016/j.bbamem.2017.09.015	journal	December 2017
Global Analysis of Intercellular Homeodomain Protein Transfer Lee, Eun Jung; Kim, Namsuk; Park, Jun Woo Cell Reports, Vol. 28, Issue 3 https://doi.org/10.1016/j.celrep.2019.06.056	journal	July 2019
The maximal size of protein to diffuse through the nuclear pore is larger than 60 kDa Wang, Ruiwen; Brattain, Michael G. FEBS Letters, Vol. 581, Issue 17 https://doi.org/10.1016/j.febslet.2007.05.082	journal	June 2007
Uptake of fluorescent nano beads into BY2-cells involves clathrin-dependent and clathrin-independent endocytosis Bandmann, Vera; Müller, Jasmin Daniela; Köhler, Tim FEBS Letters, Vol. 586, Issue 20 https://doi.org/10.1016/j.febslet.2012.08.008	journal	August 2012
Membrane permeation of arginine-rich cell-penetrating peptides independent of transmembrane potential as a function of lipid composition and membrane fluidity Wallbrecher, Rike; Ackels, Tobias; Olea, R. Alis Journal of Controlled Release, Vol. 256 https://doi.org/10.1016/j.jconrel.2017.04.013	journal	June 2017
Engineered miniature CRISPR-Cas system for mammalian genome regulation and editing Xu, Xiaoshu; Chemparathy, Augustine; Zeng, Leiping Molecular Cell, Vol. 81, Issue 20 https://doi.org/10.1016/j.molcel.2021.08.008	journal	October 2021
Precise Modifications of Both Exogenous and Endogenous Genes in Rice by Prime Editing Li, Huiyuan; Li, Jingying; Chen, Jilin Molecular Plant, Vol. 13, Issue 5 https://doi.org/10.1016/j.molp.2020.03.011	journal	May 2020
Nanoparticles for protein delivery in planta Wang, Jeffrey W.; Cunningham, Francis J.; Goh, Natalie S. Current Opinion in Plant Biology, Vol. 60 https://doi.org/10.1016/j.pbi.2021.102052	journal	April 2021
Regulation of Cell Wall Thickening by a Medley of Mechanisms McCahill, Ian W.; Hazen, Samuel P. Trends in Plant Science, Vol. 24, Issue 9 https://doi.org/10.1016/j.tplants.2019.05.012	journal	September 2019
Apoplastic Proteases: Powerful Weapons against Pathogen Infection in Plants Wang, Yan; Wang, Yuanchao; Wang, Yiming Plant Communications, Vol. 1, Issue 4 https://doi.org/10.1016/j.xplc.2020.100085	journal	July 2020
Uptake and Fate of Fluorescently Labeled DNA Nanostructures in Cellular Environments: A Cautionary Tale Lacroix, Aurélie; Vengut-Climent, Empar; de Rochambeau, Donatien ACS Central Science, Vol. 5, Issue 5 https://doi.org/10.1021/acscentsci.9b00174	journal	April 2019
Non-transgenic Gene Modulation via Spray Delivery of Nucleic Acid/Peptide Complexes into Plant Nuclei and Chloroplasts Thagun, Chonprakun; Horii, Yoko; Mori, Maai ACS Nano, Vol. 16, Issue 3 https://doi.org/10.1021/acsnano.1c07723	journal	February 2022
Stability of Cell-Penetrating Peptide−Morpholino Oligomer Conjugates in Human Serum and in Cells Youngblood, Derek S.; Hatlevig, Susie A.; Hassinger, Jed N. Bioconjugate Chemistry, Vol. 18, Issue 1 https://doi.org/10.1021/bc060138s	journal	December 2006
The Uptake of Arginine-Rich Cell-Penetrating Peptides: Putting the Puzzle Together Brock, Roland Bioconjugate Chemistry, Vol. 25, Issue 5 https://doi.org/10.1021/bc500017t	journal	April 2014
Cellular Internalization and Distribution of Arginine-Rich Peptides as a Function of Extracellular Peptide Concentration, Serum, and Plasma Membrane Associated Proteoglycans Kosuge, Michie; Takeuchi, Toshihide; Nakase, Ikuhiko Bioconjugate Chemistry, Vol. 19, Issue 3 https://doi.org/10.1021/bc700289w	journal	February 2008
The Cationic Cell-Penetrating Peptide CPP ^TAT Derived from the HIV-1 Protein TAT Is Rapidly Transported into Living Fibroblasts: Optical, Biophysical, and Metabolic Evidence ^† Ziegler, André; Nervi, Pierluigi; Dürrenberger, Markus Biochemistry, Vol. 44, Issue 1 https://doi.org/10.1021/bi0491604	journal	January 2005
Comparison of Penetratin and Other Homeodomain-Derived Cell-Penetrating Peptides: Interaction in a Membrane-Mimicking Environment and Cellular Uptake Efficiency Balayssac, Stéphane; Burlina, Fabienne; Convert, Odile Biochemistry, Vol. 45, Issue 5 https://doi.org/10.1021/bi0518390	journal	January 2006
Cell Penetration Profiling Using the Chloroalkane Penetration Assay Peraro, Leila; Deprey, Kirsten L.; Moser, Matthew K. Journal of the American Chemical Society, Vol. 140, Issue 36 https://doi.org/10.1021/jacs.8b06144	journal	August 2018
pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation Hellens, Roger P.; Edwards, E. Anne; Leyland, Nicola R. Plant Molecular Biology, Vol. 42, Issue 6, p. 819-832 https://doi.org/10.1023/A:1006496308160	journal	January 2000
Plant stem cell maintenance involves direct transcriptional repression of differentiation program Yadav, Ram Kishor; Perales, Mariano; Gruel, Jérémy Molecular Systems Biology, Vol. 9, Issue 1 https://doi.org/10.1038/msb.2013.8	journal	January 2013
WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators Leibfried, Andrea; To, Jennifer P. C.; Busch, Wolfgang Nature, Vol. 438, Issue 7071 https://doi.org/10.1038/nature04270	journal	December 2005
Versatile protein tagging in cells with split fluorescent protein Kamiyama, Daichi; Sekine, Sayaka; Barsi-Rhyne, Benjamin Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11046	journal	March 2016
Lifeact: a versatile marker to visualize F-actin Riedl, Julia; Crevenna, Alvaro H.; Kessenbrock, Kai Nature Methods, Vol. 5, Issue 7 https://doi.org/10.1038/nmeth.1220	journal	June 2008
Fluorescent fusion protein knockout mediated by anti-GFP nanobody Caussinus, Emmanuel; Kanca, Oguz; Affolter, Markus Nature Structural & Molecular Biology, Vol. 19, Issue 1 https://doi.org/10.1038/nsmb.2180	journal	December 2011
Unravelling cytosolic delivery of cell penetrating peptides with a quantitative endosomal escape assay Teo, Serena L. Y.; Rennick, Joshua J.; Yuen, Daniel Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-23997-x	journal	June 2021
High aspect ratio nanomaterials enable delivery of functional genetic material without DNA integration in mature plants Demirer, Gozde S.; Zhang, Huan; Matos, Juliana L. Nature Nanotechnology, Vol. 14, Issue 5 https://doi.org/10.1038/s41565-019-0382-5	journal	February 2019
Nanoparticle cellular internalization is not required for RNA delivery to mature plant leaves Zhang, Huan; Goh, Natalie S.; Wang, Jeffrey W. Nature Nanotechnology, Vol. 17, Issue 2 https://doi.org/10.1038/s41565-021-01018-8	journal	November 2021
Library screening of cell-penetrating peptide for BY-2 cells, leaves of Arabidopsis, tobacco, tomato, poplar, and rice callus Numata, Keiji; Horii, Yoko; Oikawa, Kazusato Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-29298-6	journal	July 2018
Biolistic-delivery-based transient CRISPR/Cas9 expression enables in planta genome editing in wheat Hamada, Haruyasu; Liu, Yuelin; Nagira, Yozo Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-32714-6	journal	September 2018
Cell-penetrating peptide sequence and modification dependent uptake and subcellular distribution of green florescent protein in different cell lines Patel, Sanjay G.; Sayers, Edward J.; He, Lin Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-42456-8	journal	April 2019
Hydrophobicity is a key determinant in the activity of arginine-rich cell penetrating peptides Allen, Jason; Pellois, Jean-Philippe Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-20425-y	journal	September 2022
Wuschel2 enables highly efficient CRISPR/Cas-targeted genome editing during rapid de novo shoot regeneration in sorghum Che, Ping; Wu, Emily; Simon, Marissa K. Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03308-w	journal	April 2022
GFP-complementation assay to detect functional CPP and protein delivery into living cells Milech, Nadia; Longville, Brooke AC; Cunningham, Paula T. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep18329	journal	December 2015
Translocation of bioactive peptides across cell membranes by carbon nanotubesElectronic supplementary information (ESI) available: details of the synthesis and characterization, cell culture, TEM, epifluorescence and confocal microscopy images of CNTs 1, 2 and fluorescein. See http://www.rsc.org/suppdata/cc/b3/b311254c/ Pantarotto, Davide; Briand, Jean-Paul; Prato, Maurizio Chemical Communications, Issue 1 https://doi.org/10.1039/b311254c	journal	January 2004
The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis Zuo, Jianru; Niu, Qi-Wen; Frugis, Giovanna The Plant Journal, Vol. 30, Issue 3 https://doi.org/10.1046/j.1365-313X.2002.01289.x	journal	May 2002
A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis Daum, Gabor; Medzihradszky, Anna; Suzaki, Takuya Proceedings of the National Academy of Sciences, Vol. 111, Issue 40 https://doi.org/10.1073/pnas.1406446111	journal	September 2014
DNA nanostructures coordinate gene silencing in mature plants Zhang, Huan; Demirer, Gozde S.; Zhang, Honglu Proceedings of the National Academy of Sciences, Vol. 116, Issue 15 https://doi.org/10.1073/pnas.1818290116	journal	March 2019
Use of Ranks in One-Criterion Variance Analysis Kruskal, William H.; Wallis, W. Allen Journal of the American Statistical Association, Vol. 47, Issue 260 https://doi.org/10.1080/01621459.1952.10483441	journal	December 1952
Principles of protein targeting to the nucleolus Martin, Robert M.; Ter-Avetisyan, Gohar; Herce, Henry D. Nucleus, Vol. 6, Issue 4 https://doi.org/10.1080/19491034.2015.1079680	journal	July 2015
Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor Gjetting, Sisse Krag; Ytting, Cecilie Karkov; Schulz, Alexander Journal of Experimental Botany, Vol. 63, Issue 8 https://doi.org/10.1093/jxb/ers040	journal	March 2012
Ligation-independent cloning of PCR products (LIC-PCR) Aslanidis, Charalampos; de Jong, Pieter J. Nucleic Acids Research, Vol. 18, Issue 20 https://doi.org/10.1093/nar/18.20.6069	journal	January 1990
Deciphering key features in protein structures with the new ENDscript server Robert, Xavier; Gouet, Patrice Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku316	journal	April 2014
Attenuation of green fluorescent protein half-life in mammalian cells Corish, Pete; Tyler-Smith, Chris Protein Engineering, Design and Selection, Vol. 12, Issue 12 https://doi.org/10.1093/protein/12.12.1035	journal	December 1999
Three Classes of Nuclear Import Signals Bind to Plant Nuclei Hicks, G. R.; Smith, Hms.; Shieh, M. Plant Physiology, Vol. 107, Issue 4 https://doi.org/10.1104/pp.107.4.1055	journal	April 1995
GoldenBraid 2.0: A Comprehensive DNA Assembly Framework for Plant Synthetic Biology Sarrion-Perdigones, A.; Vazquez-Vilar, M.; Palaci, J. Plant Physiology, Vol. 162, Issue 3, p. 1618-1631 https://doi.org/10.1104/pp.113.217661	journal	May 2013
Mesoporous Silica Nanoparticle-Mediated Intracellular Cre Protein Delivery for Maize Genome Editing via loxP Site Excision^, Martin-Ortigosa, Susana; Peterson, David J.; Valenstein, Justin S. Plant Physiology, Vol. 164, Issue 2 https://doi.org/10.1104/pp.113.233650	journal	December 2013
A Decrease in Mesophyll Conductance by Cell-Wall Thickening Contributes to Photosynthetic Downregulation Sugiura, Daisuke; Terashima, Ichiro; Evans, John R. Plant Physiology, Vol. 183, Issue 4 https://doi.org/10.1104/pp.20.00328	journal	June 2020
Carbon Dots for Efficient Small Interfering RNA Delivery and Gene Silencing in Plants Schwartz, Steven H.; Hendrix, Bill; Hoffer, Paul Plant Physiology, Vol. 184, Issue 2 https://doi.org/10.1104/pp.20.00733	journal	August 2020
Arabidopsis WUSCHEL Is a Bifunctional Transcription Factor That Acts as a Repressor in Stem Cell Regulation and as an Activator in Floral Patterning Ikeda, Miho; Mitsuda, Nobutaka; Ohme-Takagi, Masaru The Plant Cell, Vol. 21, Issue 11 https://doi.org/10.1105/tpc.109.069997	journal	November 2009
Morphogenic Regulators Baby boom and Wuschel Improve Monocot Transformation Lowe, Keith; Wu, Emily; Wang, Ning The Plant Cell, Vol. 28, Issue 9 https://doi.org/10.1105/tpc.16.00124	journal	September 2016
Spatiotemporal Monitoring of Pseudomonas syringae Effectors via Type III Secretion Using Split Fluorescent Protein Fragments Park, Eunsook; Lee, Hye-Young; Woo, Jongchan The Plant Cell, Vol. 29, Issue 7 https://doi.org/10.1105/tpc.17.00047	journal	June 2017
A Threshold Selection Method from Gray-Level Histograms Otsu, Nobuyuki IEEE Transactions on Systems, Man, and Cybernetics, Vol. 9, Issue 1 https://doi.org/10.1109/TSMC.1979.4310076	journal	January 1979
Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta Martin, Kathleen; Kopperud, Kristin; Chakrabarty, Romit The Plant Journal, Vol. 59, Issue 1 https://doi.org/10.1111/j.1365-313X.2009.03850.x	journal	July 2009
Clathrin-independent endocytosis contributes to uptake of glucose into BY-2 protoplasts Bandmann, Vera; Homann, Ulrike The Plant Journal, Vol. 70, Issue 4 https://doi.org/10.1111/j.1365-313X.2011.04892.x	journal	February 2012
A simple method for discriminating between cell membrane and cytosolic proteins Serna, Laura New Phytologist, Vol. 165, Issue 3 https://doi.org/10.1111/j.1469-8137.2004.01278.x	journal	December 2004
Noncovalent protein transduction in plant cells by macropinocytosis Chang, Microsugar; Chou, Jyh‐Ching; Chen, Chung‐Pin New Phytologist, Vol. 174, Issue 1 https://doi.org/10.1111/j.1469-8137.2007.01977.x	journal	January 2007
Targeting of TMV Movement Protein to Plasmodesmata Requires the Actin/ER Network; Evidence From FRAP Wright, Kathryn M.; Wood, Nicola T.; Roberts, Alison G. Traffic, Vol. 8, Issue 1 https://doi.org/10.1111/j.1600-0854.2006.00510.x	journal	October 2006
Nanobody-mediated resistance to Grapevine fanleaf virus in plants Hemmer, Caroline; Djennane, Samia; Ackerer, Léa Plant Biotechnology Journal, Vol. 16, Issue 2 https://doi.org/10.1111/pbi.12819	journal	October 2017
Ikarugamycin: A Natural Product Inhibitor of Clathrin-Mediated Endocytosis: Ikarugamycin selectively inhibits CME Elkin, Sarah R.; Oswald, Nathaniel W.; Reed, Dana K. Traffic, Vol. 17, Issue 10 https://doi.org/10.1111/tra.12425	journal	August 2016
Carbon nanocarriers deliver siRNA to intact plant cells for efficient gene knockdown Demirer, Gozde S.; Zhang, Huan; Goh, Natalie S. Science Advances, Vol. 6, Issue 26 https://doi.org/10.1126/sciadv.aaz0495	journal	June 2020
Concentration-dependent transcriptional switching through a collective action of cis-elements Rodriguez, Kevin; Do, Albert; Senay-Aras, Betul Science Advances, Vol. 8, Issue 32 https://doi.org/10.1126/sciadv.abo6157	journal	August 2022
A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity Jinek, M.; Chylinski, K.; Fonfara, I. Science, Vol. 337, Issue 6096, p. 816-821 https://doi.org/10.1126/science.1225829	journal	June 2012
Statistical analysis of real-time PCR data Yuan, Joshua S.; Reed, Ann; Chen, Feng BMC Bioinformatics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2105-7-85	journal	February 2006
Characterization of a novel cell penetrating peptide derived from human Oct4 Harreither, Eva; Rydberg, Hanna A.; Åmand, Helene L. Cell Regeneration, Vol. 3, Issue 1 https://doi.org/10.1186/2045-9769-3-2	journal	January 2014
CellProfiler 4: improvements in speed, utility and usability Stirling, David R.; Swain-Bowden, Madison J.; Lucas, Alice M. BMC Bioinformatics, Vol. 22, Issue 1 https://doi.org/10.1186/s12859-021-04344-9	journal	September 2021
Antennapedia homeobox as a signal for the cellular internalization and nuclear addressing of a small exogenous peptide Perez, F.; Joliot, A.; Bloch-Gallego, E. Journal of Cell Science, Vol. 102, Issue 4 https://doi.org/10.1242/jcs.102.4.717	journal	August 1992
Native protein delivery into rice callus using ionic complexes of protein and cell-penetrating peptides Guo, Boyang; Itami, Jun; Oikawa, Kazusato PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0214033	journal	July 2019
At the Frontier; RXLR Effectors Crossing the Phytophthora?Host Interface Bouwmeester, Klaas; Meijer, Harold J. G.; Govers, Francine Frontiers in Plant Science, Vol. 2 https://doi.org/10.3389/fpls.2011.00075	journal	January 2011
Common Functions of Disordered Proteins across Evolutionary Distant Organisms Wallmann, Arndt; Kesten, Christopher International Journal of Molecular Sciences, Vol. 21, Issue 6 https://doi.org/10.3390/ijms21062105	journal	March 2020
Autofluorescence in Plants Donaldson, Lloyd Molecules, Vol. 25, Issue 10 https://doi.org/10.3390/molecules25102393	journal	May 2020

Similar Records

Data for Rapid and Efficient in planta Genome Editing in Sorghum Using Foxtail Mosaic Virus-mediated sgRNA Delivery

Dataset · 2024 · OSTI ID:3015198

Baysal, Can; Kausch, Albert P.; Cody, Jon P.; +2 more

Arginine-rich intracellular delivery peptides noncovalently transport protein into living cells

Journal Article · 2006 · Biochemical and Biophysical Research Communications · OSTI ID:20854388

Wang, Y -H; Chen, C -P; Chan, M -H; +6 more

Rapid and efficient in planta genome editing in sorghum using foxtail mosaic virus‐mediated sgRNA delivery

Journal Article · 2024 · The Plant Journal · OSTI ID:2480984

Baysal, Can; Kausch, Albert P.; Cody, Jon P.; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Delivered complementation in planta (DCIP) enables measurement of peptide-mediated protein delivery efficiency in plants

Citation Formats

References (81)

Similar Records

Related Subjects