The role of P-type IIA and P-type IIB Ca2+-ATPases in plant development and growth

Abstract

As sessile organisms, plants have evolved mechanisms to adapt to variable and rapidly fluctuating environmental conditions. Calcium (Ca2+) in plant cells is a versatile intracellular second messenger that is essential for stimulating short- and long-term responses to environmental stresses through changes in its concentration in the cytosol ([Ca2+]cyt). Increases in [Ca2+]cyt direct the strength and length of these stimuli. In order to terminate them, the cells must then remove the cytosolic Ca2+ against a concentration gradient, either taking it away from the cell or storing it in organelles such as the endoplasmic reticulum (ER) and/or vacuoles. Here, we review current knowledge about the biological roles of plant P-type Ca2+-ATPases as potential actors in the regulation of this cytosolic Ca2+ efflux, with a focus the IIA ER-type Ca2+-ATPases (ECAs) and the IIB autoinhibited Ca2+-ATPases (ACAs). While ECAs are analogous proteins to animal sarcoplasmic-endoplasmic reticulum Ca2+-ATPases (SERCAs), ACAs are equivalent to animal plasma membrane-type ATPases (PMCAs). We examine their expression patterns in cells exhibiting polar growth and consider their appearance during the evolution of the plant lineage. Full details of the functions and coordination of ECAs and ACAs during plant growth and development have not yet been elucidated. Our current understanding of the regulation of fluctuations in Ca2+ gradients in the cytoplasm and organelles during growth is in its infancy, but recent technological advances in Ca2+ imaging are expected to shed light on this subject.

Chloroplast Calcium Signaling in the Spotlight

“…Ca 2+ -permeable channels are grouped in five families: cyclic nucleotide-gated channels (CNGCs), glutamate receptors-like channels (GLRs), two-pore channels (TPCs), mechanosensitive channels (MCAs), hyperosmolality gated channels (OSCAs) (Demidchik et al, 2018). Ca 2+ transport off the cytosol to restore the resting [Ca 2+ ] cyt is mediated by energydriven pumps/transporters belonging to the P-type ATPases, such as P1B-type calcium/heavy metal cation-transporting ATPase (AtHMA1), P2A-type calcium cation-transporting ATPase (ECAs) and P2B-type calcium cation-transporting ATPase (ACAs) (García Bossi et al, 2020). Other Ca 2+ transporters are grouped in the CaCA family (CAX-type proton:calcium cation exchanger, CCX-type cation:calcium cation exchanger, MHX-type proton:magnesium cation exchanger, NCL/EF-CAX-type cation exchanger, EF-CAXtype cation exchanger) (Pittman and Hirschi, 2016) and CaCA2 family (PAM71-type manganese/calcium cation transporter).…”

Zoom in on Ca2+pattern and ion flux dynamics to decode spatial and temporal regulation of cotton fiber growth

“…ACA-type (plasma membrane-based) Ca 2+ -ATPases are essential component of the polarized cell growth. Four ACAs (ACA2, 7, 9, 11) are highly expressed during most of the pollen developmental stages (García Bossi et al, 2020), and insertional mutants of ACA9 show reduced pollen tube growth (Schiøtt et al, 2004). Ca 2+ -ATPases are also essential for a root hair growth.…”

Chlamydomonas reinhardtii cellular compartments and their contribution to intracellular calcium signalling

“…In plants, as in animals, Ca 2+ -ATPases are also crucial in maintaining Ca 2+ homeostasis within the different intracellular compartments, by controlling Ca 2+ efflux from the cytosol to organelles and/or to the extracellular space. Plants contain P-type ATPases, grouped as P-IIA ER-type Ca 2+ -ATPases (ECAs), mainly localized in the ER and Golgi apparatus, and P-IIB autoinhibited Ca 2+ -ATPases (ACAs), found mainly in the plasma membrane but also in the ER, vacuoles, and chloroplast membranes ( García Bossi et al , 2020 ). Three homologues of Arabidopsis ACAs and two for ECAs were found in C. reinhardtii , having a possible role in the reuptake of cytosolic Ca 2+ against its concentration gradient.…”

“…Three homologues of Arabidopsis ACAs and two for ECAs were found in C. reinhardtii , having a possible role in the reuptake of cytosolic Ca 2+ against its concentration gradient. ACA- and/or ECA-mediated Ca 2+ active transport could have a signalling function, removing this secondary messenger from the cell or storing it in organelles, such as the ER, vacuoles, chloroplast, or mitochondria ( García Bossi et al , 2020 ). The subcellular localization and characterization of these Ca 2+ -ATPases in C. reinhardtii needs to be elucidated, possibly clarifying their role in organellar Ca 2+ signalling and homeostasis.…”