Molecular Sensors Reveal the Mechano-chemical Response of Walls and Membranes to Mechanical and Chemical Stress

Overview

Journal Cell Surf

Publisher Elsevier

Date 2022 Jan 21

PMID 35059532

Authors

Lucile Michels

Jochem Bronkhorst

Michiel Kasteel

Djanick de Jong

Bauke Albada

Tijs Ketelaar

Francine Govers

Joris Sprakel

Affiliations

Soon will be listed here.

Abstract

, causal agent of late blight in potato and tomato, remains challenging to control. Unravelling its biomechanics of host invasion, and its response to mechanical and chemical stress, could provide new handles to combat this devastating pathogen. Here we introduce two fluorescent molecular sensors, CWP-BDP and NR12S, that reveal the micromechanical response of the cell wall-plasma membrane continuum in during invasive growth and upon chemical treatment. When visualized by live-cell imaging, CWP-BDP reports changes in cell wall (CW) porosity while NR12S reports variations in chemical polarity and lipid order in the plasma membrane (PM). During invasive growth, mechanical interactions between the pathogen and a surface reveal clear and localized changes in the structure of the CW. Moreover, the molecular sensors can reveal the effect of chemical treatment to CW and/or PM, thereby revealing the site-of-action of crop protection agents. This mechano-chemical imaging strategy resolves, non-invasively and with high spatio-temporal resolution, how the CW-PM continuum adapts and responds to abiotic stress, and provides information on the dynamics and location of cellular stress responses for which, to date, no other methods are available.

Citing Articles

Arabinosylation of cell wall extensin is required for the directional response to salinity in roots.

Zou Y, Gigli-Bisceglia N, van Zelm E, Kokkinopoulou P, Julkowska M, Besten M Plant Cell. 2024; 36(9):3328-3343.

PMID: 38691576 PMC: 11371136. DOI: 10.1093/plcell/koae135.

Molecular Rotors: Fluorescent Sensors for Microviscosity and Conformation of Biomolecules.

Paez-Perez M, Kuimova M Angew Chem Int Ed Engl. 2023; 63(6):e202311233.

PMID: 37856157 PMC: 10952837. DOI: 10.1002/anie.202311233.

A molecular mechanosensor for real-time visualization of appressorium membrane tension in Magnaporthe oryzae.

Ryder L, Lopez S, Michels L, Eseola A, Sprakel J, Ma W Nat Microbiol. 2023; 8(8):1508-1519.

PMID: 37474734 PMC: 10390335. DOI: 10.1038/s41564-023-01430-x.

Osmotic Pressure Enables High-Yield Assembly of Giant Vesicles in Solutions of Physiological Ionic Strengths.

Cooper A, Girish V, Subramaniam A Langmuir. 2023; 39(15):5579-5590.

PMID: 37021722 PMC: 10116648. DOI: 10.1021/acs.langmuir.3c00457.

References

Blum M, Boehler M, Randall E, Young V, Csukai M, Kraus S . Mandipropamid targets the cellulose synthase-like PiCesA3 to inhibit cell wall biosynthesis in the oomycete plant pathogen, Phytophthora infestans. Mol Plant Pathol. 2010; 11(2):227-43. PMC: 6640402. DOI: 10.1111/j.1364-3703.2009.00604.x. View

Saville A, Graham K, Grunwald N, Myers K, Fry W, Ristaino J . Fungicide Sensitivity of U.S. Genotypes of Phytophthora infestans to Six Oomycete-Targeted Compounds. Plant Dis. 2019; 99(5):659-666. DOI: 10.1094/PDIS-05-14-0452-RE. View

Geitmann A, Emons A . The cytoskeleton in plant and fungal cell tip growth. J Microsc. 2000; 198(Pt 3):218-45. DOI: 10.1046/j.1365-2818.2000.00702.x. View

Fabro G . Oomycete intracellular effectors: specialised weapons targeting strategic plant processes. New Phytol. 2021; 233(3):1074-1082. DOI: 10.1111/nph.17828. View

Kock C, Dufrene Y, Heinisch J . Up against the wall: is yeast cell wall integrity ensured by mechanosensing in plasma membrane microdomains?. Appl Environ Microbiol. 2014; 81(3):806-11. PMC: 4292499. DOI: 10.1128/AEM.03273-14. View

Sun X, Zhang A, Baker B, Sun L, Howard A, Buswell J . Development of SNAP-tag fluorogenic probes for wash-free fluorescence imaging. Chembiochem. 2011; 12(14):2217-26. PMC: 3213346. DOI: 10.1002/cbic.201100173. View

Ketelaar T, Meijer H, Spiekerman M, Weide R, Govers F . Effects of latrunculin B on the actin cytoskeleton and hyphal growth in Phytophthora infestans. Fungal Genet Biol. 2012; 49(12):1014-22. DOI: 10.1016/j.fgb.2012.09.008. View

Haas B, Kamoun S, Zody M, Jiang R, Handsaker R, Cano L . Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 2009; 461(7262):393-8. DOI: 10.1038/nature08358. View

Boots J, Fokkink R, van der Gucht J, Kodger T . Development of a multi-position indentation setup: Mapping soft and patternable heterogeneously crosslinked polymer networks. Rev Sci Instrum. 2019; 90(1):015108. DOI: 10.1063/1.5043628. View

10.

Neeli-Venkata R, Diaz C, Celador R, Sanchez Y, Minc N . Detection of surface forces by the cell-wall mechanosensor Wsc1 in yeast. Dev Cell. 2021; 56(20):2856-2870.e7. DOI: 10.1016/j.devcel.2021.09.024. View

11.

Pang Z, Srivastava V, Liu X, Bulone V . Quantitative proteomics links metabolic pathways to specific developmental stages of the plant-pathogenic oomycete Phytophthora capsici. Mol Plant Pathol. 2016; 18(3):378-390. PMC: 6638298. DOI: 10.1111/mpp.12406. View

12.

Lew R, Levina N, Walker S, Garrill A . Turgor regulation in hyphal organisms. Fungal Genet Biol. 2004; 41(11):1007-15. DOI: 10.1016/j.fgb.2004.07.007. View

13.

Grunwald N, Sturbaum A, Montes G, Serrano E, Lozoya-Saldana H, Fry W . Selection for Fungicide Resistance Within a Growing Season in Field Populations of Phytophthora infestans at the Center of Origin. Phytopathology. 2008; 96(12):1397-403. DOI: 10.1094/PHYTO-96-1397. View

14.

Wang Y, Wang Y . Phytophthora sojae effectors orchestrate warfare with host immunity. Curr Opin Microbiol. 2018; 46:7-13. DOI: 10.1016/j.mib.2018.01.008. View

15.

Du Y, Mpina M, Birch P, Bouwmeester K, Govers F . Phytophthora infestans RXLR Effector AVR1 Interacts with Exocyst Component Sec5 to Manipulate Plant Immunity. Plant Physiol. 2015; 169(3):1975-90. PMC: 4634092. DOI: 10.1104/pp.15.01169. View

16.

Wu C, Zhao J, Li Z, Liu W, Mei X, Ning J . Modeling of the Phytophthora capsici cellulose synthase 3 and its inhibitors activity assay. Pest Manag Sci. 2019; 75(11):3024-3030. DOI: 10.1002/ps.5417. View

17.

Dostal V, Libusova L . Microtubule drugs: action, selectivity, and resistance across the kingdoms of life. Protoplasma. 2014; 251(5):991-1005. DOI: 10.1007/s00709-014-0633-0. View

18.

Boevink P, Birch P, Turnbull D, Whisson S . Devastating intimacy: the cell biology of plant-Phytophthora interactions. New Phytol. 2020; 228(2):445-458. PMC: 7540312. DOI: 10.1111/nph.16650. View

19.

Money N . Osmotic Pressure of Aqueous Polyethylene Glycols : Relationship between Molecular Weight and Vapor Pressure Deficit. Plant Physiol. 1989; 91(2):766-9. PMC: 1062068. DOI: 10.1104/pp.91.2.766. View

20.

Vleeshouwers V, Raffaele S, Vossen J, Champouret N, Oliva R, Segretin M . Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol. 2011; 49:507-31. DOI: 10.1146/annurev-phyto-072910-095326. View