Molecular sensors reveal the mechano-chemical response of Phytophthora infestans walls and membranes to mechanical and chemical stress

Lucile Michels; Jochem Bronkhorst; Michiel Kasteel; Djanick de Jong; Bauke Albada; Tijs Ketelaar; Francine Govers; Joris Sprakel

doi:10.1016/j.tcsw.2021.100071

Molecular sensors reveal the mechano-chemical response of Phytophthora infestans walls and membranes to mechanical and chemical stress

Cell Surf. 2022 Jan 7:8:100071. doi: 10.1016/j.tcsw.2021.100071. eCollection 2022 Dec.

Authors

Lucile Michels¹, Jochem Bronkhorst¹, Michiel Kasteel^{2

3}, Djanick de Jong¹, Bauke Albada⁴, Tijs Ketelaar³, Francine Govers², Joris Sprakel¹

Affiliations

¹ Physical Chemistry and Soft Matter, Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, the Netherlands.
² Laboratory of Phytopathology, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.
³ Laboratory of Cell Biology, Wageningen University & Research, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.
⁴ Laboratory of Organic Chemistry, Wageningen University & Research, Stippeneng 4, 6708 WE, Wageningen, the Netherlands.

Abstract

Phytophthora infestans, 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 P. infestans 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.

Keywords: Cell wall; Crop protection agents; Fluorescence Lifetime Imaging; Mechanobiology; Molecular mechanosensors; Phytophthora infestans; Plant pathogens; Plasma membrane.