The burning glass effect of water droplets triggers a high light-induced calcium response in the chloroplast stroma

Author(s)
Dominic Kuang, Shanna Romand, Anna S Zvereva, Bianca Maria Orlando Marchesano, Matteo Grenzi, Stefano Buratti, Qun Yang, Ke Zheng, Dimitra Valadorou, Evelien Mylle, Zuzana Benedikty, Martin Trtílek, Maria Tenje, Cornelia Spetea, Daniël Van Damme, Bernhard Wurzinger, Markus Schwarzländer, Markus Teige, Alex Costa, Simon Stael
Abstract

Plants rely on water and light for photosynthesis, but water droplets on leaves can focus light into high-intensity spots, risking photodamage. Excessive light can impair growth or induce cell death, making it essential for plants to detect and respond to light fluctuations. While Ca2+ signaling has been linked to high light (HL) acclimation, the subcellular dynamics remain unclear. Here, we investigate Ca2+ responses to HL exposure in Arabidopsis thaliana. Using a glass bead to simulate light-focusing by water droplets, a biphasic increase of Ca2+ concentration was detected in the chloroplast stroma by the genetically encoded calcium indicator YC3.6 and confirmed using a newly established stroma-localized R-GECO1 (NTRC-R-GECO1). The stromal response was largely independent of light wavelength and unaffected in phot1 phot2 and cry1 cry2 mutants. Chemical inhibition of photosynthetic electron transport, microscopy-based Fv/Fm experiments, and measurement of the reactive oxygen species (ROS)-redox balance with roGFP-based reporters and Singlet Oxygen Sensor Green (SOSG) chemical dye suggested that photodamage and singlet oxygen contribute to the stromal Ca2+ response. While blue and white light also triggered a Ca2+ response in the cytosol and nucleus, pharmacological inhibition with cyclopiazonic acid (CPA) and loss-of-function mutants of the Ca2+ transporters BIVALENT CATION TRANSPORTER 2 (BICAT2) and endoplasmic reticulum (ER)-type Ca2+-ATPase (ECA) suggested that the HL response depends on a Ca2+ exchange between the ER and chloroplast stroma. The response was primarily light dependent but accelerated by increasing external temperature. This study implicates a novel Ca2+-mediated acclimation mechanism to HL stress, a process of growing relevance in the context of climate change.

Organisation(s)
Functional and Evolutionary Ecology, Department of Biochemistry and Cell Biology
External organisation(s)
Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007 Uppsala, Sweden., Department of Biosciences, University of Milan, Via Giovanni Celoria 26, 20133 Milan, Italy., Institute of Plant Biology and Biotechnology (IBBP), Universität Münster, Schlossplatz 8, 48143 Münster, Germany., Department of Materials Science and Engineering, Uppsala University, 75103 Uppsala, Sweden; Science for Life Laboratory, Uppsala University, 75103 Uppsala, Sweden., Ghent University , Photon Systems Instruments, 66424 Drasov, Czech Republic., University of Gothenburg, Department of Biosciences, University of Milan, Via Giovanni Celoria 26, 20133 Milan, Italy; Institute of Biophysics, National Research Council of Italy (CNR), 20133 Milan, Italy., Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, 75007 Uppsala, Sweden. Electronic address: simon.stael@slu.se.
Journal
Current Biology
Volume
35
Pages
2642-2658.e7
ISSN
0960-9822
DOI
https://doi.org/10.1016/j.cub.2025.04.065
Publication date
06-2025
Peer reviewed
Yes
Austrian Fields of Science 2012
106022 Microbiology
Keywords
Sustainable Development Goals
SDG 13 - Climate Action
Portal url
https://ucrisportal.univie.ac.at/en/publications/6041ab30-26b4-4696-98c2-86ea816f767f