Lattice light-sheet microscopy allows for super-resolution imaging of receptors in leaf tissue

Traeger, Jeremiah; Yang, Mengran; Stacey, Gary; Orr, Galya; Hu, Dehong

doi:10.1016/j.bpj.2024.12.028

Lattice light-sheet microscopy allows for super-resolution imaging of receptors in leaf tissue

Journal Article · Mon Dec 30 00:00:00 EST 2024 · Biophysical Journal

DOI:https://doi.org/10.1016/j.bpj.2024.12.028· OSTI ID:2565257

Traeger, Jeremiah ^[1]; Yang, Mengran ^[2]; ^[2]; ^[1]; ^[1]

Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Univ. of Missouri, Columbia, MO (United States)

Plant leaf tissues are difficult to image via fluorescent microscopy, largely due to the presence of chlorophyll and other pigments that provide large background fluorescence. An advantage of Lattice Light-Sheet microscopy is its use of Bessel beams that illuminate a thin focal region of interest for microscopy, allowing for the excitation of fluorescent molecules within this region without surrounding chlorophyll-like objects outside of the region of interest. Here, we apply STORM Super-resolution techniques to observe Receptor-Like Kinases in Arabidopsis thaliana leaf cells. By applying this technique with the Lattice Light-Sheet, we can localize immune response proteins in sub-100 nm length scales and reconstruct three-dimensional locations of proteins within individual leaf cells. Using this technique, we observed the effect of the elicitors ATP and flg22, where we observed a significant degree of internalization of cognate receptors P2K1 and FLS2. We were also able to similarly observe differences in colocalization due to stimulation with these elicitors, where we observe proteins on the membrane becoming less colocalized as a result of stimulation, suggesting an immune response mechanism involving receptors internalizing via pathways distinct to the receptor. Further, these data show the Lattice Light-Sheet’s capabilities for imaging tissue with problematic background fluorescence that otherwise makes super-resolution fluorescence microscopy difficult.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: National Institutes of Health (NIH), National Institute of General Medical Sciences (NIGMS); National Science Foundation (NSF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-76RL01830; SC0020346

OSTI ID:: 2565257

Report Number(s):: PNNL-SA--197440

Journal Information:: Biophysical Journal, Journal Name: Biophysical Journal Journal Issue: 3 Vol. 124; ISSN 0006-3495

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (35)

PALM and STORM: Unlocking live-cell super-resolution Henriques, Ricardo; Griffiths, Caron; Hesper Rego, E. Biopolymers, Vol. 95, Issue 5 https://doi.org/10.1002/bip.21586	journal	January 2011
Precise Nanometer Localization Analysis for Individual Fluorescent Probes Thompson, Russell E.; Larson, Daniel R.; Webb, Watt W. Biophysical Journal, Vol. 82, Issue 5 https://doi.org/10.1016/S0006-3495(02)75618-X	journal	May 2002
High-resolution light-sheet microscopy for whole-cell sub-cellular dynamics Kreplin, Laura Zoe; Arumugam, Senthil Current Opinion in Cell Biology, Vol. 85 https://doi.org/10.1016/j.ceb.2023.102272	journal	December 2023
Receptor-associated independent cAMP nanodomains mediate spatiotemporal specificity of GPCR signaling Anton, Selma E.; Kayser, Charlotte; Maiellaro, Isabella Cell, Vol. 185, Issue 7 https://doi.org/10.1016/j.cell.2022.02.011	journal	March 2022
Membrane permeabilization induced by Triton X-100: The role of membrane phase state and edge tension Mattei, Bruno; Lira, Rafael B.; Perez, Katia R. Chemistry and Physics of Lipids, Vol. 202 https://doi.org/10.1016/j.chemphyslip.2016.11.009	journal	January 2017
Plant Pattern-Recognition Receptor FLS2 Is Directed for Degradation by the Bacterial Ubiquitin Ligase AvrPtoB Göhre, Vera; Spallek, Thomas; Häweker, Heidrun Current Biology, Vol. 18, Issue 23 https://doi.org/10.1016/j.cub.2008.10.063	journal	December 2008
A Plasma Membrane Nanodomain Ensures Signal Specificity during Osmotic Signaling in Plants Smokvarska, Marija; Francis, Charbel; Platre, Matthieu Pierre Current Biology, Vol. 30, Issue 23 https://doi.org/10.1016/j.cub.2020.09.013	journal	December 2020
Spatiotemporal Dynamics of the BRI1 Receptor and its Regulation by Membrane Microdomains in Living Arabidopsis Cells Wang, Li; Li, Hong; Lv, Xueqin Molecular Plant, Vol. 8, Issue 9 https://doi.org/10.1016/j.molp.2015.04.005	journal	September 2015
Dynamic spatial reorganization of BSK1 complexes in the plasma membrane underpins signal-specific activation for growth and immunity Su, Bodan; Zhang, Xi; Li, Li Molecular Plant, Vol. 14, Issue 4 https://doi.org/10.1016/j.molp.2021.01.019	journal	April 2021
Advances in Imaging Plant Cell Walls Zhao, Yuanyuan; Man, Yi; Wen, Jialong Trends in Plant Science, Vol. 24, Issue 9 https://doi.org/10.1016/j.tplants.2019.05.009	journal	September 2019
Spectrally Resolved and Functional Super-resolution Microscopy via Ultrahigh-Throughput Single-Molecule Spectroscopy Yan, Rui; Moon, Seonah; Kenny, Samuel J. Accounts of Chemical Research, Vol. 51, Issue 3 https://doi.org/10.1021/acs.accounts.7b00545	journal	February 2018
Membrane Lipid Nanodomains Cebecauer, Marek; Amaro, Mariana; Jurkiewicz, Piotr Chemical Reviews, Vol. 118, Issue 23 https://doi.org/10.1021/acs.chemrev.8b00322	journal	October 2018
Hydroporphyrin-Doped Near-Infrared-Emitting Polymer Dots for Cellular Fluorescence Imaging Riahin, Connor; Meares, Adam; Esemoto, Nopondo N. ACS Applied Materials & Interfaces, Vol. 14, Issue 18 https://doi.org/10.1021/acsami.2c02551	journal	April 2022
Photoswitching Mechanism of Cyanine Dyes Dempsey, Graham T.; Bates, Mark; Kowtoniuk, Walter E. Journal of the American Chemical Society, Vol. 131, Issue 51 https://doi.org/10.1021/ja904588g	journal	December 2009
Bacterial disease resistance in Arabidopsis through flagellin perception Zipfel, Cyril; Robatzek, Silke; Navarro, Lionel Nature, Vol. 428, Issue 6984 https://doi.org/10.1038/nature02485	journal	April 2004
Smart lattice light-sheet microscopy for imaging rare and complex cellular events Shi, Yu; Tabet, Jimmy S.; Milkie, Daniel E. Nature Methods, Vol. 21, Issue 2 https://doi.org/10.1038/s41592-023-02126-0	journal	January 2024
Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases Mbengue, Malick; Bourdais, Gildas; Gervasi, Fabio Proceedings of the National Academy of Sciences, Vol. 113, Issue 39 https://doi.org/10.1073/pnas.1606004113	journal	September 2016
Symbiotic root infections in Medicago truncatula require remorin-mediated receptor stabilization in membrane nanodomains Liang, Pengbo; Stratil, Thomas F.; Popp, Claudia Proceedings of the National Academy of Sciences, Vol. 115, Issue 20 https://doi.org/10.1073/pnas.1721868115	journal	April 2018
Membrane nanodomains and transport functions in plant Martinière, Alexandre; Zelazny, Enric Plant Physiology, Vol. 187, Issue 4 https://doi.org/10.1093/plphys/kiab312	journal	July 2021
X-ray microscopy enables multiscale high-resolution 3D imaging of plant cells, tissues, and organs Duncan, Keith E.; Czymmek, Kirk J.; Jiang, Ni Plant Physiology, Vol. 188, Issue 2 https://doi.org/10.1093/plphys/kiab405	journal	September 2021
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis Robatzek, S. Genes & Development, Vol. 20, Issue 5 https://doi.org/10.1101/gad.366506	journal	March 2006
Stochastic Optical Reconstruction Microscopy (STORM): A Method for Superresolution Fluorescence Imaging Bates, Mark; Jones, Sara A.; Zhuang, Xiaowei Cold Spring Harbor Protocols, Vol. 2013, Issue 6 https://doi.org/10.1101/pdb.top075143	journal	June 2013
Sensitivity to Flg22 Is Modulated by Ligand-Induced Degradation and de Novo Synthesis of the Endogenous Flagellin-Receptor FLAGELLIN-SENSING2 Smith, J. M.; Salamango, D. J.; Leslie, M. E. PLANT PHYSIOLOGY, Vol. 164, Issue 1 https://doi.org/10.1104/pp.113.229179	journal	November 2013
Innate Immune Responses Activated in Arabidopsis Roots by Microbe-Associated Molecular Patterns Millet, Yves A.; Danna, Cristian H.; Clay, Nicole K. The Plant Cell, Vol. 22, Issue 3 https://doi.org/10.1105/tpc.109.069658	journal	March 2010
Plasma Membranes Are Subcompartmentalized into a Plethora of Coexisting and Diverse Microdomains in Arabidopsis and Nicotiana benthamiana Jarsch, Iris K.; Konrad, Sebastian S. A.; Stratil, Thomas F. The Plant Cell, Vol. 26, Issue 4 https://doi.org/10.1105/tpc.114.124446	journal	April 2014
Induced Genome-Wide Binding of Three Arabidopsis WRKY Transcription Factors during Early MAMP-Triggered Immunity Birkenbihl, Rainer P.; Kracher, Barbara; Roccaro, Mario The Plant Cell, Vol. 29, Issue 1 https://doi.org/10.1105/tpc.16.00681	journal	December 2016
Nearest Neighbor Distance Distribution in Hard-Core Point Processes Al-Hourani, Akram; Evans, Robin J.; Kandeepan, Sithamparanathan IEEE Communications Letters, Vol. 20, Issue 9 https://doi.org/10.1109/LCOMM.2016.2591017	journal	September 2016
Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution Chen, Bi-Chang; Legant, Wesley R.; Wang, Kai Science, Vol. 346, Issue 6208 https://doi.org/10.1126/science.1257998	journal	October 2014
Identification of a Plant Receptor for Extracellular ATP Choi, J.; Tanaka, K.; Cao, Y. Science, Vol. 343, Issue 6168 https://doi.org/10.1126/science.343.6168.290	journal	January 2014
Protocol: an improved and universal procedure for whole-mount immunolocalization in plants Pasternak, Taras; Tietz, Olaf; Rapp, Katja Plant Methods, Vol. 11, Issue 1 https://doi.org/10.1186/s13007-015-0094-2	journal	October 2015
Light-sheet microscopy: a tutorial Olarte, Omar E.; Andilla, Jordi; Gualda, Emilio J. Advances in Optics and Photonics, Vol. 10, Issue 1 https://doi.org/10.1364/AOP.10.000111	journal	January 2018
How to define and optimize axial resolution in light-sheet microscopy: a simulation-based approach Remacha, Elena; Friedrich, Lars; Vermot, Julien Biomedical Optics Express, Vol. 11, Issue 1 https://doi.org/10.1364/BOE.11.000008	journal	December 2019
Purinoceptor P2K1/DORN1 Enhances Plant Resistance Against a Soilborne Fungal Pathogen, Rhizoctonia solani Kumar, Sonika; Tripathi, Diwaker; Okubara, Patricia A. Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.572920	journal	September 2020
Super-Resolution Imaging of Plant Receptor-Like Kinases Uncovers Their Colocalization and Coordination with Nanometer Resolution Traeger, Jeremiah; Hu, Dehong; Yang, Mengran Membranes, Vol. 13, Issue 2 https://doi.org/10.3390/membranes13020142	journal	January 2023
Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains Bücherl, Christoph A.; Jarsch, Iris K.; Schudoma, Christian eLife, Vol. 6 https://doi.org/10.7554/eLife.25114	journal	March 2017

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