Transport, functions, and interaction of calcium and manganese in plant organellar compartments

Abstract

Calcium (Ca2+) and manganese (Mn2+) are essential elements for plants and have similar ionic radii and binding coordination. They are assigned specific functions within organelles, but share many transport mechanisms to cross organellar membranes. Despite their points of interaction, those elements are usually investigated and reviewed separately. This review takes them out of this isolation. It highlights our current mechanistic understanding and points to open questions of their functions, their transport, and their interplay in the endoplasmic reticulum (ER), vesicular compartments [Golgi apparatus, trans-Golgi Network (TGN), prevacuolar compartment (PVC)], vacuoles, chloroplasts, mitochondria, and peroxisomes. Complex processes demanding these cations, such as Mn2+-dependent glycosylation or systemic Ca2+ signaling, are covered in some detail if they have not been reviewed recently or if recent findings add to current models. The function of Ca2+ as signaling agent released from organelles into the cytosol and within the organelles themselves is a recurrent theme of this review, again keeping the interference by Mn2+ in mind. The involvement of organellar channels [e.g., Glutamate-Receptor-Likes (GLRs), Cyclic-Nucleotide-Gated Channels (CNGCs), Mitochondrial Conductivity Units (MCUs), Two-Pore Channel1 (TPC1)], transporters [e.g., Natural-Resistance-Associated Macrophage Proteins (NRAMPs), Calcium Exchangers (CAXs), Metal-Tolerance Proteins (MTPs), Bivalent-Cation Transporters (BICATs)] and pumps [Autoinhibited Ca2+-ATPases (ACAs), ER Ca2+-ATPases (ECAs)] in the import and export of organellar Ca2+ and Mn2+ is scrutinized, whereby current controversial issues are pointed out. Mechanisms in animals and yeast are taken into account where they may provide a blueprint for processes in plants, in particular with respect to tunable molecular mechanisms of Ca2+-versus-Mn2+ selectivity.

Manganese matters: feeding manganese into the secretory system for cell wall synthesis

“…It establishes a link between Mn entry in the Golgi, the presence of Mn dependent glycosyl transferase in this compartment and the formation of the cell wall. Both protein glycosylation and glycosylation of cell wall polymers such as homogalacturonans, rhamnogalacturonans, xylogalacturonans and xyloglucans, involve Mn‐dependent glycosyl transferases (He et al ., 2021). The data presented show that arabinose, xylose and mannose contents are specifically decreased in the pml3 mutant cell walls under Mn deficiency.…”

“…Downstream of the TGN, the flux of vesicles might also be targeted to the vacuole. This pathway would contribute to the storage of Mn in the vacuole together with Mn transporters that reside on the vacuolar membrane such as MTP8 and CAX2 (He et al ., 2021). Collectively, these transporters are required for tolerance to Mn excess.…”

“…Manganese (Mn) is an essential element for plants, playing major roles as a co-factor of enzymes involved in photosynthesis and oxygen species detoxification (Schmidt & Husted, 2019). Manganese acts in various plant cell compartments and needs to be transported in chloroplasts and mitochondria (He et al, 2021). The manganese/calcium (Mn/Ca) efflux transporters of the UPF0016/GDT family (Demaegd et al, 2014), PAM71 and CMT1, have been shown to allow Mn transport at the thylakoid and inner membranes of the chloroplast, respectively (Fig.…”

Calcium Mediated Cold Acclimation in Plants: Underlying Signaling and Molecular Mechanisms

“…In Arabidopsis thaliana , plasma membrane-bound Ca 2+ -permeable channels are categorized into four main families, namely, cyclic nucleotide-gated channels (CNGCs), glutamate receptor-like channels (GLRs), stretch-activated Ca 2+ channels (OSCAs), and the MID1-complementing activity (MCA) ( Romola, 2002 ; Kurusu et al, 2013 ; Jha et al, 2016 ; Liu X. et al, 2018 ). Several other Ca 2+ channels are localized in organelles, such as endoplasmic reticulum, mitochondria, golgi body, and plant vacuole ( Costa et al, 2018 ; Thor, 2019 ; He et al, 2021 ; Pandey and Sanyal, 2021 ). These include autoinhibited Ca 2+ -ATPases (ACAs), ER-type Ca 2+ -ATPases (ECAs), mitochondrial Ca 2+ uniporter (MCU), P1-ATPases (e.g., HMA1), Ca 2+ exchangers (CAX), two-pore channel (TPC), 1,4,5-trisphosphate receptor-like channel (InsP 3 R), 1,4,5-trisphosphate (IP 3 ), cyclic ADP-ribose (cADPR)-activator ryanodine receptor-like channel (RyR), slow-activating vacuolar channel (SV), and sodium–calcium exchanger (NCX).…”

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

“…As a second messenger, Ca 2+ plays a pivotal role in regulating plant adaptive responses to developmental and environmental signals by forming specific Ca 2+ signatures that occur in spikes, waves, and oscillations with a defined duration, amplitude, frequency, and/or subcellular location ( 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 (PM) 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 are presumably decoded by Ca 2+ sensing proteins, for example calmodulin (CaM), CaM-like proteins, calcium-dependent protein kinases, and calcineurin B-like proteins ( 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) .…”