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Proton Pinballs in Plant Growth
Novel molecular pinball machines of the plasma membrane control cytosolic Ca2+ levels that regulate plant metabolism. The essential components involve: 1. an auxin-activated proton pump; 2. arabinogalactan glycoproteins (AGPs); 3. Ca2+ channels; 4. auxin-efflux “PIN” proteins. Typical pinball machines release pinballs that trigger various sound and visual effects. However, in plants, “proton pinballs” eject Ca2+ bound by paired glucuronic acid residues of numerous glycomodules in periplasmic AGP-Ca2+. Freed Ca2+ ions flow down the electrostatic gradient through open Ca2+ channels into the cytosol, thus activating numerous Ca2+-dependent activities.
Sixty years ago , the discovery of hydroxyproline (Hyp) firmly bound to the cell wall was the “founder event” for a new field in plant biology. Proteins specific to the cell wall had not previously been considered as components of an otherwise polysaccharide structure, apart from occasional hints in the literature. Indeed, the Hill reaction defined the photolysis of water as the ancient source of atmospheric oxygen . On the evolutionary timescale, an increased atmospheric oxygen level eventually led to its use as a terminal electron acceptor but also a direct source of the hydroxyproline hydroxyl. The biosynthesis of hydroxyproline, first shown in sycamore cell suspensions, involved the direct incorporation of 18O2 into the hydroxyproline hydroxyl group . Hence, the first step in understanding the structural and dynamic roles of the Hyp-rich proteins unique to plants was taken. Quite remarkably, mammalian systems have recruited prolyl hydroxylase as an oxygen sensor for hypoxia inducible factor (HIF), which in turn plays a crucial role in foetal development .
The first analyses of TCA-soluble cytoplasmic protein–polysaccharide complexes purified by preparative isoelectric focusing  were subsequently identified as arabinogalactan proteins. Data from  show representative species across the plant kingdom included dicots, a gymnosperm and a bryophyte. These were the first AGP analyses notable for their high alanine and low tyrosine, with a high galactose and arabinose content.
Such proteins, later named arabinogalactan proteins (AGPs), located mainly between the plasma membrane and cell wall, were periplasmic, analogous to Peter Mitchell’s bacterial periplasm . However, they were not precursors to wall-bound proteins, based on their composition and absence of turnover in 14C-proline pulse-chase experiments .
2. The Origin of Ion Gradients
3. Plasma Membrane Dynamics
4. Proton Pumps
5. Indirect Evidence for the Role of AGPs in Ca2+ Homeostasis
An early indication of a connection between AGPs and Ca2+ appeared in 1991; the wound response of Acacia senegal and its secretory product, gum Arabic, consists of polysaccharides and glycoproteins related to AGPs . Significantly, gum Arabic contains glucuronic acid (~10%) and binds approximately ~1% by weight of Ca2+. In the same year , the analysis of isolated plasma membranes revealed a bound AGP content of ~10% w/w. These AGPs were hydroxyproline-rich, with a significant glucuronic acid content (~10%). However, the crucial connection between Hyp-glycosubstituents and the pH-dependent Ca2+ binding property of AGPs with Ca2+ homeostasis only appeared quite recently when a molecular model depicted paired glucuronic acid residues of a Hyp-glycomodule that bound Ca2+ in a molecular dynamics simulation, which was then confirmed through an in vitro assay .
6. Direct Evidence for AGP Regulation of Ca2+ Homeostasis—A New Paradigm
6.1. AGP Glucuronic Acid Is Essential for Growth
6.2. AGP Glucuronic Acid Enables AGP-Ca2+ Binding
6.3. AGP-Ca2+ Binding Is a Major Source of Cytosolic Ca2+
6.4. Auxin Increases Cytosolic Ca2+
6.5. Ca2+ ATPase Recycles Cytosolic Ca2+
6.6. Ca2+ Waves Are Essential for Root Growth
6.7. AGPs Respond to Salt Stress
The entry is from 10.3390/cells10081935
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