A novel glutathione peroxidase-based biosensor disentangles differential subcellular accumulation of H2O2 and lipid hydroperoxides

Exposito-Rodriguez, Marino; Reeder, Brandon; Brooke, Greg N.; Hough, Michael A.; Laissue, Philippe P.; Mullineaux, Philip M.

doi:10.1101/2024.01.18.576236

Cited by 2 publications

References 91 publications

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Diatoms exhibit dynamic chloroplast calcium signals in response to high light and oxidative stress

Flori,

Dickenson,

Gaikwad

et al. 2024

Plant Physiology

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Diatoms are a group of silicified algae that play a major role in marine and freshwater ecosystems. Diatom chloroplasts were acquired by secondary endosymbiosis and exhibit important structural and functional differences from the primary plastids of land plants and green algae. Many functions of primary plastids, including photoacclimation and inorganic carbon acquisition, are regulated by calcium-dependent signalling processes. Calcium signalling has also been implicated in the photoprotective responses of diatoms; however, the nature of calcium elevations in diatom chloroplasts and their wider role in cell signalling remains unknown. Using genetically encoded calcium indicators, we find that the diatom Phaeodactylum tricornutum exhibits dynamic calcium elevations within the chloroplast stroma. Stromal calcium ([Ca2+]str) acts independently from the cytosol and is not elevated by stimuli that induce large cytosolic calcium ([Ca2+]cyt) elevations. In contrast, high light and exogenous hydrogen peroxide (H2O2) induce large, sustained [Ca2+]str elevations that are not replicated in the cytosol. Measurements using the fluorescent H2O2 sensor roGFP2-Oxidant Receptor Peroxidase 1 (Orp1) indicate that [Ca2+]str elevations induced by these stimuli correspond to the accumulation of H2O2 in the chloroplast. [Ca2+]str elevations were also induced by adding methyl viologen, which generates superoxide within the chloroplast, and by treatments that disrupt non-photochemical quenching (NPQ). The findings indicate that diatoms generate specific [Ca2+]str elevations in response to high light and oxidative stress that likely modulate the activity of calcium-sensitive components in photoprotection and other regulatory pathways.

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Diatoms exhibit dynamic chloroplast calcium signals in response to high light and oxidative stress

Flori,

Dickenson,

Gaikwad

et al. 2024

Plant Physiology

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Burning glass effect of water droplets triggers an ER-derived calcium response in the chloroplast stroma ofArabidopsis thalianaleaves

Kuang,

Romand,

Zvereva

et al. 2024

Preprint

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Plants require water and light for photosynthesis, but light, when focused by water droplets on leaves, can create high light intensity spots that are harmful to plants. As excessive light intensity can reduce growth or even induce cell death, it is vital for plants to detect and react to changes in light exposure and acclimate to high light stress. Ca2+ signaling was previously implicated in high light acclimation. However, the dynamics of free Ca2+ concentration in the chloroplast, the primary site of photosynthesis, or in the nucleus and in the cytoplasm, where transcription and translation for long term acclimation occurs, remain unknown. Here we studied the dynamics and mechanism of the Ca2+ response to high light exposure. Focusing light through a glass bead to mimic water droplets triggered an increase of the free Ca2+ concentration in the chloroplast stroma of Arabidopsis thaliana. This finding was corroborated using established and newly developed genetically encoded calcium indicators, which revealed a biphasic increase in the stromal free Ca2+ concentration when exposed to varying intensities and qualities of light. Among photosynthetic by products, reactive oxygen and lipophilic species in particular, have been implicated in high light stress acclimation. A H2O2 signature was induced, albeit with different dynamics than the Ca2+ response, while chemical inhibition of the photosynthetic electron transport points towards singlet oxygen as a potential culprit of the high light-induced increase in stromal free Ca2+ concentration. The observed dynamics differed from those of a heat shock induced Ca2+ signature, although temperature had a positive effect on the Ca2+ response. Based on Ca2+ inhibitor treatments and the free Ca2+ concentration dynamics, we suggest that the high light induced stromal Ca2+ is derived from the endoplasmic reticulum rather than from the cytoplasm. In conclusion, inspired by the burning glass effect of water droplets on leaves, we uncovered a Ca2+ response that implicates a novel mechanism for plants to acclimate to high light stress, a process that will become increasingly relevant in a changing climate.

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A novel glutathione peroxidase-based biosensor disentangles differential subcellular accumulation of H2O2 and lipid hydroperoxides

Cited by 2 publications

References 91 publications

Diatoms exhibit dynamic chloroplast calcium signals in response to high light and oxidative stress

Diatoms exhibit dynamic chloroplast calcium signals in response to high light and oxidative stress

Burning glass effect of water droplets triggers an ER-derived calcium response in the chloroplast stroma ofArabidopsis thalianaleaves

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