Systemic Calcium Wave Propagation in Physcomitrella patens

Abstract

The adaptation to dehydration and rehydration cycles represents a key step in the evolution of photosynthetic organisms and requires the development of mechanisms by which to sense external stimuli and translate them into signaling components. In this study, we used genetically encoded fluorescent sensors to detect specific transient increases in the Ca2+ concentration in the moss Physcomitrella patens upon dehydration and rehydration treatment. Observation of the entire plant in a single time-series acquisition revealed that various cell types exhibited different sensitivities to osmotic stress and that Ca2+ waves originated from the basal part of the gametophore and were directionally propagated towards the top of the plant. Under similar conditions, the vascular plant Arabidopsis thaliana exhibited Ca2+ waves that propagated at a higher speed than those of P. patens. Our results suggest that systemic Ca2+ propagation occurs in plants even in the absence of vascular tissue, even though the rates can be different.

Photosynthetic activity triggers pH and NAD redox signatures across different plant cell compartments

“…Fluorescent protein-based biosensing has been developed towards a powerful approach to monitor dynamic changes in metabolite concentrations, signalling molecules and other physiological parameters in planta (Walia et al, 2018), allowing to monitor responses to external and internal stimuli live and with subcellular resolution (e.g. Chaudhuri et al, 2008; Keinath et al, 2015; Storti et al, 2018; Waadt et al, 2020; Wagner et al, 2019). Several biosensors to monitor bioenergetic parameters related to photosynthesis at the subcellular level, including pH as component of the proton motive force and ATP, are available in plants (De Col et al, 2017; Demes et al, 2020; Hatsugai et al, 2012; Schwarzländer et al, 2011; Voon et al, 2018; Yang et al, 2017).…”

Rapid systemic signaling during abiotic and biotic stresses: is the ROS wave master of all trades?

“…Although it would be tempting to speculate that all systemic signals are transduced though the plant vascular system (somewhat akin to the nervous system of animals), one should keep an open mind when it comes to this important question (e.g. systemic calcium waves were shown to propagate in the nonvascular plant Physcomitrella ; Storti et al , ). Different systemic signals could propagate through different plant tissues or cell types interacting only at particular locations (Figure ).…”

CamelliA-based simultaneous imaging of Ca2+ dynamics in subcellular compartments

“…Different subcellular compartments display distinct levels of free Ca 2+ ion (Suzuki et al, 2016;Costa et al, 2018). As such, effective monitoring of the changes in Ca 2+ levels require the selection of GECIs with appropriate binding affinity to Ca 2+ (Kd).…”

“…As such, effective monitoring of the changes in Ca 2+ levels require the selection of GECIs with appropriate binding affinity to Ca 2+ (Kd). Thus, we employed three single-colored GECIs: B-GECO1 (Zhao et al, 2011), GCaMP6f (Chen et al, 2013Li et al, 2019), andjRGECO1a (Dana et al, 2016), for imaging the cytosolic and the nuclear Ca 2+ levels, because their Kd is within the range of the cytosolic and nuclear Ca 2+ concentrations (van Der Luit et al, 1999;Mithofer and Mazars, 2002;Stael et al, 2012;Sello et al, 2016;Costa et al, 2018;Jiang et al, 2019). They were each tagged with an N-terminal nuclear export signal peptide from PKIα (Wen et al, 1995) or C-terminal three tandem repeats of the nuclear localization signal from the SV40 large T antigen (Kalderon et al, 1984) for cytosolic and nuclear targeting respectively.…”

“…As second messengers, specific Ca 2+ signatures exhibit as spikes, waves, and oscillations with a defined duration, amplitude, frequency, and/or subcellular location to regulate plant adaptive responses to developmental and environmental signals (Dodd et al, 2010;Kudla et al, 2018;Vigani and Costa, 2019;Lamers et al, 2020). Ca 2+ signatures are generated by Ca 2+ channels, Ca 2+ pumps, and/or Ca 2+ transporters localized in the plasma membrane or organellar membranes (Stael et al, 2012;Costa et al, 2018;Kudla et al, 2018;Pan et al, 2019;Hilleary et al, 2020;He et al, 2021), and presumably decoded by Ca 2+ sensing proteins, e.g., calmodulin, calmodulin-like proteins, calcium-dependent protein kinases (CDPKs), and calcineurin B-like proteins (CBLs) (Harmon et al, 2000;Cheng et al, 2002;Luan et al, 2002;Harper et al, 2004;McCormack et al, 2005;DeFalco et al, 2009;Weinl and Kudla, 2009;Kudla et al, 2018;Tang et al, 2020). The mechanisms for encoding Ca 2+ signatures are poorly characterized, largely due to the spatiotemporal complexity of Ca 2+ signaling, which often involves a large number of Ca 2+ signature encoders and decoders distributed widely in multiple subcellular compartments (Stael et al, 2012;Costa et al, 2018;Kudla et al, 2018;Wudick et al, 2018).…”