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Review
. 2021 Dec 4;187(4):1940-1972.
doi: 10.1093/plphys/kiab122.

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

Jie He  1 , Nico Rössner  1 , Minh T T Hoang  1 , Santiago Alejandro  1 , Edgar Peiter  1
Affiliations
Review

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

Jie He et al. Plant Physiol. .

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, pre-vacuolar compartment), 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 (GLR), cyclic nucleotide-gated channels (CNGC), mitochondrial conductivity units (MCU), and two-pore channel1 (TPC1)], transporters (e.g. natural resistance-associated macrophage proteins (NRAMP), Ca2+ exchangers (CAX), metal tolerance proteins (MTP), and bivalent cation transporters (BICAT)], and pumps [autoinhibited Ca2+-ATPases (ACA) and ER Ca2+-ATPases (ECA)] 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.

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Figures

Figure 1
Figure 1
Transport proteins for Ca2+ and Mn2+ discussed in this review. Pumps (triangles), transporters (ellipses), and channels (rectangles) that were experimentally shown to permeate Ca2+ (blue), Mn2+ (magenta), or both (blue/magenta) are displayed in a hypothetical plant cell containing the organelles discussed in this review. Only Arabidopsis proteins are shown, except for LjCASTOR and MtCNGC15s, for which a function of the Arabidopsis homologs as Ca2+ channels has not been examined yet. Characterized orthologs of Arabidopsis proteins described in the text are listed in Table 1. Note that the absence of an experimentally confirmed substrate, for example, Mn2+ in the case of Ca2+ channels (GLR, CNGC, and TPC1) does not exclude its permeation. Conductance of Mn2+ by (c)MCUs is inferred from their mammalian homologs. The permeation of Ca2+ by NRAMPs can be excluded on a structural basis, as discussed in the text. ER, endoplasmic reticulum; NE, nuclear envelope; PVC, pre-vacuolar compartment; TGN, trans-Golgi network.
Figure 2
Figure 2
Mn2+ and Ca2+ dependence of glycosylation in the Golgi. Enzymes are either marked in magenta for those experimentally confirmed to require Mn2+ or in gray for those predicted to be Mn2+-dependent. Enzymes that are also activated by Ca2+ are framed in blue. An enzyme that does not absolutely depend on Mn2+ is marked in brown. A, Schematic representation of enzymes involved in synthesis of O-glycans attached to plant AGPs and EXTs, and specific complex-type N-glycans attached to plant glycoproteins. The glycan models presented are modified from Nguema-Ona et al. (2014) and Showalter and Basu (2016). Among those core enzymes of deglycosylation (insert) and glycosylation, MNS1, MNS2, MNS3 (Liebminger et al., 2009), and FUT11 (Both et al., 2011) are activated by Ca2+ or Mn2+. XYLT (Pagny et al., 2003), GALT1 (Strasser et al., 2007), and GALT2 to 6 (Basu et al., 2015a, 2015b) are reported to coordinate Mn2+ for their catalytic activity. Activity of XYLT is stimulated or inhibited by Mn2+ (Bencúr et al., 2005). Based on the Uniprot database (www.uniprot.org), some further Arabidopsis GTs involved in N- or O-glycosylation are predicted to contain a DxD motif or to bind Mn2+ by sequence similarity, that is, β-1,2-N-acetylglucosaminyltransferase (GNT1 and 2), β-1,2-arabinosyltransferase (RRA1,2,3 and XEG113), hydroxyproline-O-galactosyltransferase (HPGT1,2,3), β-1,3-galactosyltransferase (B3GALT7), β-1,6-galactosyltransferase (GALT31A), and β-arabinofuranosyltransferase (RAY1). B, Schematic representation of enzymes involved in the synthesis of matrix sugars of the plant cell wall. The structures of matrix sugars are modified from Burton et al. (2010). Enzymes shown to require Mn2+ are galactan synthase 1 (AtGALS1) that catalyzes the addition of galactose from UDP-α-D-Gal to β-1,4-galactan chains of rhamnogalacturonan I and the transfer of an arabinopyranose from UDP-β-L-Arap to galactan chains (Ebert et al., 2018; Laursen et al., 2018); a polygalacturonate (1,4)-α-D-galacturonosyltransferase complex (GAUT1:GAUT7) that catalyzes the transfer of galacturonic acid onto homogalacturonan (Amos et al., 2018); (1,3)-α-D-xylosyltransferases (AtRGXT1 and 2) that synthesize rhamnogalacturonan-II (RG II; Egelund et al., 2006; Petersen et al., 2009); xyloglucan xylosyltransferases (XXT1 and 2) that are involved in xyloglucan biosynthesis (Culbertson et al., 2016; 2018); and GUX1 that adds GlcA to xylan (Rennie et al., 2012). In addition, based on the Uniprot database (www.uniprot.org), further Arabidopsis GTs involved in matrix sugar biosynthesis are predicted to contain a DxD motif or to bind Mn2+ by sequence similarity, that is, rhamnogalacturonan α-1,3-D-xylosyltransferase (MGP4 and RGXT3) for RGII biosynthesis, and UDP-GlcA:xylan glucuronyltransferase (GUX2,3,4,5) for heteroxylan biosynthesis.
Figure 3
Figure 3
Synchrotron µXRF analyses visualize the allocation of Ca2+ and Mn2+ in Arabidopsis seeds by vacuolar transporters. A, High-resolution SXRF maps of Ca2+ distribution in endodermal layers of the hypocotyl (a and c) and single endodermal cells (b and d; positions indicated by rectangles in a and c, respectively) in seeds from Col-0 and cax1cax3 plants. Colors indicate normalized fluorescence (logarithmic scale). Figure taken from Punshon et al. (2012), modified. B, High-resolution SXRF maps of Mn distribution in whole seeds of Col-0 and cax1cax3 plants. Figure taken from Punshon et al. (2012), modified. C, Distribution of Mn in intact seeds from Col-0, vit1-1, mtp8-1, and mtp8-1vit1-1 plants determined by µSXRF tomography. The color scale ranges from 0 to 1,100 µg g−1 Mn. Figure taken from Eroglu et al. (2017), modified.
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