Annexins as overlooked regulators of membrane transport in plant cells. - Free PDF Download (2023)

International Journal of

Review of Molecular Science

Annexins as overlooked regulators of membrane transport in plant cells Dorota Konopka-Postupolska 1, * and Greg Clark 2 1 2


Department of Plant Biochemistry, Department of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw 02-106, Poland Molecular, Cellular and Developmental Biology, University of Texas, Austin, TX 78712, USA;[email protected]Correspondence:[email protected]; Tel.: +48-22-592-5716; Fax: +48-22-658-4804

Academic editors: Received: 31 December 2016; Accepted: April 6, 2017; Released: April 19

Summary: Annexins are an evolutionarily conserved superfamily of proteins that can bind to membrane phospholipids in a calcium-dependent manner. Their physiological role is still intensively studied, and it appears that individual proteins are specialized for specific functions despite their general structural similarity. However, due to their general ability to coordinate membranes in a calcium-sensitive manner, they are thought to be involved in membrane flux. In this review, we present a summary of the current understanding of cellular transport in plant cells and consider the possible roles of annexin at different stages of vesicular transport. Keywords: annexin; vesicular transport; membrane trade; stress response; Rab protein; LOOP

1. Introduction Annexins are a multigene, evolutionarily conserved family of calcium- and phospholipid-binding proteins with a highly conserved tertiary structure among subfamilies from different kingdoms [1]. They are found in almost all eukaryotes, and prototypical proteins of this family are found in some prokaryotes [2–5]. The genomes of all plant and vertebrate species encode multiple annexins, and expression levels of certain annexins can be very high [3]. Annexins were first purified as minor contaminants of calmodulin purifications and were proposed as novel targets of Ca 2+ signaling in animal cells. The contribution of annexins to the adaptation of plant cells to adverse environmental conditions is well documented [3,6-10]. Analyzes confirmed that annexin 1 (ANNAT1) from Arabidopsis thaliana (Arabidopsis) and its homologs from different species (e.g. the stress tolerance of tobacco, cotton and Arabidopsis [3,10]. In transgenic plants expressing higher levels of this annexin Moreover, degradation of photosynthetic pigments and reduction in photosynthetic activity were slower and less pronounced than in wild-type plants, and their productivity in response to various stress factors was better. In some cases, ectopic expression of this annexin resulted in multistress tolerance [10-12]. certain annexins are also able to alleviate oxidative stress in prokaryotic (bacterial) and animal cells, strongly suggesting that annexins may act via very basic mechanisms common to all kingdoms [1]. So far, the exact molecular mechanisms of these biological phenomena unknown.

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Annexins are also believed to be involved in membrane-related processes such as intracellular vesicle transport, endo- and exocytosis, phagocytosis and autophagy due to their inherent ability to bind and position the membrane structures relative to each other in a calcium-dependent manner [3:13]. The growing body of data indicates that cell trafficking plays a significant role in plant stress response and adaptation to changes in the environment. In Arabidopsis, unperturbed vesicle transport is required for proper signaling during growth and development [14], maintenance of ion homeostasis [15,16] and tolerance to salt stress [17], water deficit [18] or during defensive responses [19], 20]. Tolerance to osmotic stress has been shown to be dependent on both transcriptional and non-transcriptional responses. The latter involves regulation of stomatal movements [21] and membrane permeability [22] by coordinating endo-/exocytosis of plasma membrane ion channels and transport of water channels, respectively. Similarly, the non-transcriptional responses of stress-related phytohormones such as abscisic acid or methyl jasmonate are triggered at least in part by changes in the polar distribution of PIN family auxin transporters [ 23 ]. Abscisic acid is an important regulator of abiotic stress resistance and promotes endocytosis [24] as well as sequestration of auxin transporters in endosomal recycling compartments [25], whereas the effects of methyl jasmonate (MeJA) on subcellular PIN2 distribution vary with concentration, at higher levels endocytosis is induced, at lower values ​​endocytosis is induced [26]. Auxin was previously thought to be exclusively involved in developmental processes, but recent transcriptome analysis revealed a partial overlap in expression profiles between auxin-responsive genes and stress-response genes, suggesting that auxins are also involved in stress/defense responses [27]. We speculate that plant annexins are among the possible Ca2+ effectors that regulate intracellular membrane flux either through direct interaction with membrane structures or indirectly, e.g. by rearranging the actin cytoskeleton [28]. In this regard, the strongest evidence supporting this hypothesis came from the early work on mammalian annexins [29]. In this study, the annexins A1, A4, A5, A6, A7 (ANXA1, ANXA4, ANXA5, ANXA6, and ANXA7) were expressed in wild-type and 13 secretory yeast mutants (sec) [ 30 ]. The latter included the ten-second mutants involved in the late secretory pathway (LSC; sec 1, sec 2, sec 3, sec 4, sec 5, sec 6, sec 8, sec 9, sec 10 and sec 15), two mutants with defective endoplasmic reticulum (ER) to Golgi complex (Golgi) transport (Section 17 and Section 18), and a mutant with pleiotropic defects (Section 14). Yeast lacks endogenous annexins, therefore the observed effects were due to non-specific interactions between annexins and the secretion machinery and not complementation. None of the annexins provided full complementation of any of the sec mutants, but specific interactions for ANXA1, ANXA6 and ANXA7 with the sec2 mutant and between ANXA7 and sec4 and sec15 were observed. While annexin A7 inhibited the growth of exocytosis-defective sec2, sec4, and sec15 mutants, ANXA1 and ANXA6 reduced the lag time associated with adaptation of sec2 mutants to galactose-containing medium. The latter could be due to an annexin-mediated correction of the defective insertion of galactose permease into the plasma membrane (PM). In conclusion, certain annexins may affect specific steps in membrane transport associated with growth, secretion, and remodeling of the plasma membrane (PM) of yeast cells. The purpose of this review is to highlight recent advances in plant membrane trafficking and to consider recent data indicating a role for annexins in membrane trafficking. New insights into our understanding of the complex network of membrane transport in plant cells as well as new insights into the function of plant annexins will be discussed. 2. Annexin properties Although the primary amino acid sequences of annexins differ significantly, the overall structure of the proteins of this superfamily is good with four well-known repeats (I-IV) of about 70 amino acids (PFAM domain (database of curated protein) families) ). received PF00191, 66 aa).

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Each of these repeats may have a type II Ca 2+ -binding bipartite motif located on two different α-helices (GxGT-(38-40 residues)-D/E), but typically some of them are non-functional. In plant annexins, the Ca2+ binding motif is highly conserved in repeat I, is generally lost in repeats II and III, and is only moderately conserved in repeat IV [3,13]. For example, Arabidopsis ANNAT1 and ANNAT2 have conserved Ca 2+ -binding motifs in repeats I and IV, but not in repeats II and III, while ANNAT4 is more divergent ( Figure 1A ). In contrast, three repeats (I, II and IV) are well conserved in vertebrate annexins [1,3,13]). Each individual annexin domain consists of 5 α-helices (AE). Four of them (A, B, D and E) are arranged in parallel and form a tightly packed helix-loop-helix bundle. In contrast, Helix C is almost vertical and covers the remaining four on the surface [13]. The core of the helix bundle consists mainly of hydrophobic residues, while hydrophilic residues are exposed on the surface of the protein and between domains. The tertiary structure of annexins is evolutionarily conserved; A single molecule resembles a slightly curved disc, with calcium and phospholipid binding sites on the more convex surface and the more concave surface facing the cytoplasm. Despite the considerable structural similarities that explain their central property of Ca 2+ -dependent lipid binding, individual eukaryotic annexins are considerably specific; For example, they differ significantly in their calcium binding affinity and thus also in their membrane binding. In smooth muscle cells, annexins function as intracellular Ca2+ sensors and have been shown to migrate sequentially to the PM according to their decreasing calcium affinity [31,32]. A mechanism of membrane binding has been proposed which assumes that calcium ions are jointly coordinated by the Ca 2+ binding site and membrane phospholipids (membrane bridging mechanism) [33]. Consequently, the calcium binding affinity of individual annexins should only be considered in the context of the composition of the interacting membrane. Membrane binding leads to conformational changes and the slightly curved annexin molecule is converted into a more planar disk [34]. Such a modification can visualize the secondary phospholipid binding sites on the concave surface and allow the attachment of membrane structures [35] (Figure 1B). Annexins are classified into five families according to the evolutionary classification of eukaryotes: A (ANXA, vertebrates, including humans), B (ANXB, invertebrates), C (ANXC, fungi), D (ANXD, true plants), E ( ANXE, protists) [36]. The best characterized is the monophyletic A family, where 12 different subfamilies are encoded by 12 paralogous genes (ANXA1-ANXA11 and ANXA13). The second, truly monophyletic group is the Archaeplastida, which consists of green and red algae and modern green land plants [2]. In contrast, neither fungi nor protists are considered a monophyletic clade, and different groups within this group may possess or lack these proteins [2]. The possible role of annexins in membrane transport and secretion was originally suggested based on their ability to “annex” membranes and possibly assist in secretory vesicle fusion with the PM (Figure 1B) [3,13]. Annexins not only bind to abundant phospholipids in membranes such as phosphatidylserine, but also interact with minor membrane phospholipids such as negatively charged phosphatidylinositols, phosphatidylglycerol and phosphatidic acid. The paradigm for annexin function is based on their Ca2+-dependent membrane-binding property, which enables them to move from the cytosol to the membranes when the level of Ca2+ in the cytosol rises in response to a stimulus. Therefore, annexins are considered to be dynamic signaling proteins that provide important links between intracellular Ca2+ signaling and the regulation of various membrane functions such as lateral membrane organization, the interaction of the cytoskeleton with cell membranes and membrane flux.

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Figure 1. Predicted structure of three Arabidopsis annexins and proposed mechanism

Figure 1. Predicted structure of three Arabidopsis annexins and proposed mechanism for annexin-annexin membrane coordination. (A) Predicted structure of three Arabidopsis annexins, ANNAT1, membrane ANNAT3, coordination. (A) Predicted structure of three Arabidopsis annexins, ANNAT1 and ANNAT4. The structure was created by ANNAT3, Nicolas Guex, Alexandre Diemand, Manuel C. Peitsch and Torsten Schwede based on Swiss-PdbViewer, DeepView v4.1 and ANNAT4. The structure was created with Swiss-PdbViewer, DeepView v4.1 from the existing Nicolas Guex crystal structures. The overall structure of the annexins is evolutionarily conserved. The molecule Alexandre Annexin Diemand, Manuel C. Peitsch, Torsten Schwede based on the existing annexin crystal consists of four repeats (I-IV) of about 70 amino acids (PFAM domain PF00191, 66 aa). In structures. The overall structure of the annexins is evolutionarily conserved. The molecule consists of four plant annexins. The type II Ca2+ and phospholipid binding motif (GxGT-(38-40 residues)-D/E) consists of repeats (I-IV) of approx. conserved amino (PFAM 66 aa only). moderate In plant annexins with high repeat content70 I (in gray), acids are generally lost in domain repeats IIPF00191 and III, and type II conserved Ca2+ and binding motif in phospholipids repeats IV (in red). In Arabidopsis, (GxGT-(38-40 canonical motif residues)-D/E) present in repeat 1 of highly conserved annexin 1 is 3 and generally modified motif IV of IIAnnexin 1 and in annexin 4 is in repeat I and (in gray) ), lostin repeats and III, and3. only moderate in repeat IV calcium and phospholipid binding motifs; (B) Possible mechanism of membrane coordination by (in red). In Arabidopsis, according to [34,37] the canonical motif is present in repeat 1 of annexins 1 and 3 as well as in modified annexins. Two opposing membranes can be coordinated by dimerization of the annexin motif in repat IV of annexin and membrane 3. No detectable calcium and phospholipid molecules are present in annexin. Binding to 1 leads to 4 changes in molecular conformation and a flattening of the binding motif; Possible mechanism of membrane coordination of annexins according to protein (B) disc. This creates secondary calcium and membrane binding sites on the concave surface [34,37]. describes enables positioning of the various membrane structures. Two opposing membranes are coordinated by dimerizing annexin molecules. Binding to the membrane leads to changes in molecular conformation and flattening of the protein disc. This exposes secondary calcium and membrane binding sites on the concave surface, allowing cells to be partitioned into a number of distinct locations by the various membrane structures of an endomembrane system.

Subjects. The diversification of the internal cell environment enables the simultaneous performance of different functions, such as B. Synthesis, sorting and degradation of macromolecules 3. Membrane flow lipids in eukaryotes (proteins and cell wall cell precursors) and secondary metabolism. The morphology, functions, lipid and protein compositions of the individual organelles are specifically designed to support the functions of eukaryotic cells. An endomembrane is divided into a number of discrete compartments. Although individual cell compartments are a system that is not continuous, they remain connected to each other. The diversification of the internal cell environment enables the performance of different functions of vesicle transport systems and proteins. Lipids are constantly exchanged between different

simultaneously, such as synthesis, sorting and degradation of macromolecules (proteins, lipids and cell wall precursors) and secondary metabolism. The individual organelles' morphology, functions, lipid and protein compositions are specifically designed to support individual functions. Although cell basins are not continuous, they remain connected by vesicle transport systems and proteins. Lipids are constantly exchanged between different structures. In addition, membrane transport systems allow cells to maintain contact with their environment and exchange information by supporting the uptake (endocytosis) and export (exocytosis) of macromolecules, particles, and other chemical compounds.

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In plant cells, the main organelles of the endomembrane system are the ER [38], the Golgi, which is composed of several distributed Golgi stacks called dictyosomes [39], and the trans-Golgi network (TGN) [40], multivesicular bodies/prevacuolar compartments (MVB/PVC ) [41] , lytic and protein storage vacuoles (LV and PSV, respectively) [42,43] , the PM and the endocytic compartment [44,45] . Based on rapid labeling with the fluorescent endocytic tracer FM4-64 and morphological similarities, it is generally assumed that the TGN in plants functions like the early endosome (EE) compartment in animal cells [41,46,47]. The next structure labeled by FM4-64 is the MVB/PVC, suggesting that it is the plant equivalent of the late endosomal compartment (LE) in animal cells. In plant cells, acidic vacuoles function like lysosomes. Membrane compartments constantly communicate with each other via transport vesicles. As in all other eukaryotes, there are two main pathways of membrane flux in plant cells: secretory and endocytic pathways [48,49]. Within the early secretory pathway (ESP), which includes the ER and Golgi [ 47 ], vesicle transport occurs in two opposite directions. In forward transport (anterograde trafficking), all newly synthesized proteins destined for secretion are exported from their site of synthesis in the ER to the standard targets. In the Golgi, cargo and membrane molecules are sorted between the PM/apoplast and tonoplast/vacuole lumen, which together form the late secretory pathway (LSP) [47]. At each step of their transport, proteins can be diverted from their forward path by reverse (retrograde) transport. Transport within the ESP is mediated by Coat Protein Complex II (COPII)-coated vesicles emerging from the ER membranes and by COPI-coated vesicles released from Golgi cisternae [50,51] . COPII-coated vesicles are involved in anterograde ER-to-Golgi transport, while two types of COPI-coated vesicles mediate retrograde Golgi-to-ER transport (COPIa) and inter-Golgi cisternae transport (COPIb) [ 50 ]. A third type of vesicle, clathrin-coated vesicles (CCV), functions in the LSP and assists in both forward transport and delivery of endocytic material to the endosomes. The second distinct secretory pathway supports the delivery of the precursors to the cell wall polysaccharides synthesized in the Golgi canal [52,53]. Cellulose is the only cell wall component produced in situ on the cell surface by the PM-localized enzymes, whereas hemicelluloses and pectin precursors are synthesized in the Golgi and only then transported to the cell surface and assembled into polymers [54–56]. It is estimated that up to 80% of Golgi metabolic activity in plant cells is involved in polysaccharide synthesis. In ESP, retrograde traffic balances the continuous forward flow, allowing the cell to maintain the size of the various compartments, return components of the resident transport machinery to the appropriate compartment, and prevent the loss of resident proteins accidentally captured by the donor compartment [57]. Much less is known about LSP. The TGN is the first site where the biosynthetic/secretory and endocytic pathways cross [49]. At the TGN, secretory transport could possibly branch to the various post-Golgi compartments, i.e. H. PM or PVCs/MVBs [40,57,58]. Proteins without one or more sorting signals are transported by default to the PM. Other proteins carrying vacuole sorting signals (VSSs) are recognized by the corresponding vacuole sorting receptor and transported in PVCs, although there is also some evidence that cargo recognition by VSRs may already occur in the ER [59- 62]. Receptors and membranes are returned to the TGN for the next delivery cycle. Trafficking within the LSP is primarily mediated by clathrin-coated vesicles (CCVs). These vesicles are formed on the PM during endocytosis and on the surface of the trans-Golgi network and support receptor-mediated post-Golgi traffic and endocytic protein transport. The transport of soluble cargo to the vacuoles occurs not only through the TGN, but also through other recently described routes. There is evidence that vacuolar proteins can bypass the Golgi (non-conventional secretory pathways) [63] or reach the PM first and only then return to the vacuole, as undisturbed endocytosis is required for the proper development of the vacuolar system [64]. . Furthermore, a space between the PVC and LV has been described in the leaf epidermis of tobacco (Nicotiana tabacum) [65], where proteins can be stored for different times before reaching their final destination. In addition, there are other non-Golgi secretion pathways

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international J. Mol. Science. 2017, 18, 863 6 of 34 system [64]. Furthermore, in the tobacco leaf epidermis ( Nicotiana tabacum ), a space between the PVC and LV has been described [ 65 ] where proteins can be stored for different lengths of time before reaching their final state [ 66 ]. Goal. In addition, several leaderless proteins that are not part of Golgi secretion are still being discovered. [66] A schematic representation of the transport of membrane plant cells is shown in Figure 2. The cells are shown in Figure 2.

Figure 2. Model representing intracellular transport in plant cells.

Figure 2. Model representing intracellular transport in plant cells. In silico analyzes predict that more than 17% of all Arabidopsis proteins enter the endomembrane system to be transported across the Golgi to the various standard labels [67]. In silico analyzes predict that more than 17% of all Arabidopsis proteins pass through the endomembrane. Pore-complex proteins undergo N-glycosylation. This modification required the correct folding of an incipient N-terminal leader enzyme sequence by the machinery responsible for co-translational delivery of the polypeptide to the ER lumen and through the SEC61 pore and responsible for quality control [69]. Correctly folded proteins are retained either in the ER or in the complex [68], where they subsequently undergo N-glycosylation. This modification recruits enzymes concentrated in discrete domains of the ER exit sites (ERES), which are specialized for secretion and then required for the actual formation of a nascent polypeptide and the Golgi machinery that folds in on itself, coated with COPII vesicles to delivery to [ 70]. In the Golgi, quality control proteins are responsible [69]. Correctly folded proteins are retained or concentrated in the ER, undergo final maturation and are sorted based on the presence of the short amino acid domains from the ER exit into the vesicles, which are located in the appropriate standard location (apoplast/PM or tonoplast/vacuole) migrate to specialized secretion sites (ERES) and then incorporated into newly emerged signal sequences (sorting motifs). Transport between the ER and Golgi requires energy and COPII-coated vesicles for delivery to the Golgi [70]. In the Golgi, proteins undergo final maturation by small, monomeric GTPases of the ARF family. The very last Golgi cisterna in the TGN is also a site and is sorted to the appropriate site, and vesicles migrate to the appropriate sites (apoplast/PM or where forward retrograde protein streams meet. It acts as a sorting and localization station at the junction using standard tonoplast/ vacuole) on the paths . Presence of the short amino acid signal sequences (sorting motifs). The endo-based and exocytic endocytic retrograde pathway enables both recovery of the transport machinery and ER degradation of already expendable membrane proteins. Proper targeting of vesicles Transport between the Golgi and the Golgi region requires energy, and small monomeric GTPases from the ARF depend on the presence of specific tags in the donor compartment and matching tags on the vesicles. Family. The very last Golgi cisterna of the TGN is also a site where forward and backward protein fusion from Golgi-derived vesicles carrying newly synthesized vacuole proteins and from rivers meet. It acts as a sorting station generating at the multivesicular junction of (prevacuolar endo- and exocytic pathways, early/recyclable endosomal compartments, body compartment, endocytic MVB/PVP). RetrogradeWithin RouteMVB/PVC, both recycling of transport machinery and dismantling of two types of sorting processes can take place – recycling of vacuolar cargo

dispensable membrane proteins. Correct targeting of vesicles depends on the presence of specific tags in the donor compartment and matching tags on the vesicles. A multivesicular body (prevacuolar compartment, MVB/PVP) results from the fusion of Golgi-derived vesicles carrying newly synthesized vacuolar proteins derived from early/recyclable endosomal compartments. Two types of sorting processes occur within the MVB/PVC: recycling of vacuolar cargo receptors, mediated by the retromer complex, and sorting of PM protein into internal vesicles by the ESCRT machinery. Unperturbed membrane transport is essential for maintaining homeostasis and stress responses in all eukaryotic organisms. Mutations in membrane transport proteins that block secretion are often lethal. Many annexin loss-of-function mutants, although not lethal, are sensitive to stress, and their corresponding gain-of-function mutants are stress-tolerant. These phenotypes may be due to their antioxidant activity, Ca2+ transport activity and/or their role in membrane regulation

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Act. In yeast ( Saccharomyces cerevisae ), vacuoleless mutants are viable despite severe biogenesis defects [71,72] . In contrast, vacuoles in plants are essential for development, and annexins can associate with the vacuole membrane at physiologically relevant Ca 2+ concentrations. Usually, mutations that disrupt their development and/or morphology, such as in Arabidopsis vacuoleless (vcl)/vps16, are lethal to the embryo [71,73]. Moreover, mutations that disrupt individual syntaxin genes (proteins that form a SNARE complex that performs membrane fusion) are often lethal at the stage of gametophyte or seedling development [14,74–77] . The role of calcium in transport across plant membranes The role of Ca2+ in transport across intracellular membranes is poorly characterized. It has long been known that in animal cells, a transient increase in cytosolic Ca2+ ions triggers the fusion of secretory granules and synaptic vesicles with the PM. In fact, membrane fusion often occurs during the secretory pathway, not only at the PM, so Ca2+ can potentially affect all these steps. The best known model for the Ca 2+ -regulated membrane transport event is neuronal SNARE-mediated exocytosis, which supports quantitative neurotransmitter release. Therefore, SNAREs are not Ca 2+ -sensitive proteins, and the assembly of trans -SNARE complexes at the synaptic vesicle-plasma membrane interface and the subsequent fusion of bilayers are fundamentally not calcium-dependent processes. Calcium reactivity is conferred by additional interactions with Ca 2+ -binding proteins, such as synaptotagmins or calmodulins [78–80] , which are activated in distinct but overlapping ranges of [Ca 2+ ]. Synaptotagmins ensure the synchronization of Ca2+-dependent exocytosis with the presynaptic action potential [78]. The action of calmodulins is much more complex as they interact with several target proteins involved in exocytosis, e.g. B. single soluble NSF binding protein receptors (SNAREs; e.g., VAMP2, AtSYP13 [79,81], Ca2+ channels, Ca2+/calmodulin kinase II [82–84], Rab3A [82,84,85] and Munc13 [85 .86] ). Thereby, calmodulin and synaptotagmin can work together to define the concentration range in which exocytosis occurs. As more data accumulated, it became clear that Ca 2+ is a fundamental cofactor required for the fusion of various biological membranes [87–93]. The constitutive secretory pathway appears to be a mosaic of Ca 2+ -dependent and Ca 2+ -independent processes. The addition of membrane-permeable chelators to intact, live cells results in inhibition of both anterograde and retrograde transport, but subsequent transport steps were affected to varying degrees [94]. The first step in the secretory pathway, i.e. H. COPII vesicle fusion, was not inhibited by Ca2+ chelators, while the second step, transport between the ER and Golgi intermediate compartment (ERGIC) and inside the Golgi, was inhibited. Downstream of the Golgi, there were no attachment points between the PM. Endocytosis was also unaffected, while endosome-to-Golgi and Golgi-to-ER transport was blocked [89]. Overall, the data described above strongly suggest that one of the possible mechanisms of calcium action is modulation of the activity of transport-related proteins, such as annexins, small RAB family GTPases or vesicle coat proteins. In addition to Rab3A in neurons, it has been shown that the activity of Rab11a in contractile vacuoles of Dictyostelium discoideum is controlled by the targeted release of Ca2+ via an ion channel P2XA [95]. In pneumocytes, Ca2+ entry via vesicular P2X4 channels has been reported to promote fusion pore opening and release of vesicle contents [96]. Therefore, calcium-dependent regulation of Rab proteins may be a common phenomenon, but the extent of this mechanism remains an open question. P2X receptors are also expressed on intracellular membranes in some cell types of multicellular organisms, although they are not found in higher plants [97]. However, treatment of plants with extracellular ATP (eATP) induces Ca2+ influx in plants [98–102], and eATP regulates growth in a variety of plant cells and tissues [103]. A lectin kinase receptor was recently identified as the first plant eATP receptor [104]. Interestingly, eATP-mediated Ca 2+ release in response to salt treatment was impaired in an Arabidopsis annexin mutant [105]. Calcium has also been shown to stabilize the COPI/COPII vesicle envelope. ALG-2 (Apoptosis-linked gene 2) is a Ca2+-binding protein that acts as a Ca2+ sensor on the membrane of ER export sites where COPII-coated vesicles are formed and the presence of the Ca2+ association of the sec31 subunit with of the membrane

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stabilized [106]. The Ca 2+ sensor for COPI retention on the Golgi has not yet been identified, but the yeast equivalent of the COPI coat that binds to the Golgi membranes requires Rab GTPase, ScYPT1 and the USO1 protein, among other proteins [107]. The latter is a homologue of Golgin p115 [108], which binds Rab1 to COPI vesicles at the cis-Golgi. A single point mutation in ScYPT1 (YPT1Ile121) results in a temperature-dependent dominant lethal phenotype in mutant cells. A mutation in SLY1 leads to an increase in the level of Ca2+ in the cytosol and suppresses this phenotype [109,110]. Ca2+ does not replace the specific USO1- or YPR1-dependent attachment process, but instead bypasses the need for efficient vesicle attachment. Another possible mechanism for Ca 2+ action on membrane fusion can be attributed to the physical interaction of the ions with acidic phospholipids, such as phosphatidylinositol phosphates, resulting in a change in the physical properties of the bilayer. In model membrane fusion systems, calcium ions increased the rate of lipid mixing and promoted the formation of fusion pores [111]. Interaction can also lower the energy barrier for membrane clusters to produce a hemifusion state (fusion of only the outer leaflets of two lipid bilayers) and then stabilize a highly curved membrane. Depending on lipid composition and [Ca2+]cyt, their interaction can promote negative or positive membrane curvature, which in turn affects the fusogenicity of many biological membranes [112]. Finally, Ca 2+ -mediated regulation of membrane fusion events can have an indirect effect, such as stabilization of COPI and COPII caps [113] or rearrangement of actin microfilaments [114–117] . Proper sheath assembly is required for the formation of the vesicles themselves and selection of cargo as well as biogenesis of the ESP compartments [89,118,119]. Actin microfilaments generate pathways for secretory vesicle movement, and actin polymerization-driven processes can control vesicle budding and movement of endosomes, so Ca 2+ can also regulate endocytosis [120]. In animal cells, endosome–lysosome fusion is controlled by transient increases in cytosolic Ca 2+ ions and the action of two downstream effectors, calmodulins [88,90] and Rab-GAP proteins [95] . Less is known about such processes in plant cells, but the high degree of evolutionary conservation of the entire tertiary structure strongly supports the likelihood that annexins also act as Ca2+ effectors and regulate intracellular membrane flux in plants. Furthermore, direct measurements of vesicle fusion using patch-clamp techniques in a single aleurone protoplast revealed that exocytosis in plants is also a Ca 2+ -dependent process [111]. It has also been shown that secretion of individual proteins is a Ca2+-dependent process (eg, inducible secretion of peroxidases to loosen the cell wall and allow cell elongation) [121]. Finally, a Ca2+ gradient in polarized cells helps control the shedding of cell wall material [122]. However, some differences in the way plant annexins regulate membrane flux can be expected due to different cytoarchitecture and physiology. In plant cells, the ER is not an important intracellular Ca2+ store as in animal cells. Since the large central vacuole and the apoplast in plants are also involved in Ca2+ storage [123], Ca2+ signaling in plant cells is spatially diverse [87]. Plant secretory pathways also exhibit several unique properties that distinguish them from comparable pathways in animal cells. Therefore, in the following section, we will summarize the current knowledge about plant membrane transport. 4. Annexins in membrane trafficking 4.1. What is known about vertebrate annexins: Ever since their discovery in animal cells, one of the earliest and most suspected roles for this family of proteins has been involvement in the secretion process. Since the function of annexin in plants may be consistent with its function in animals, it is worth considering the reports of animal annexin involvement in membrane transport and endocytosis. In the early studies, ANXA7, originally known as synexin, provided the best evidence for a role in secretion. It has been postulated to be involved in secretion due to its Ca 2+ and GTP promoted membrane fusion properties [124,125]. Unlike ANXA2, it promoted very strong aggregation of yeast secretory vesicles in vitro.

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which was only weakly active in the yeast vesicle aggregation assay [29]. Another annexin, ANXA13b, was shown to play a role in apical secretion through association with lipid microdomains [126]. Besides PM, there are also all other membrane compartments in BHK cells, such as nuclear envelope, ER, Golgi, plasma membrane, early endosomes (EE), late endosomes (LE) and lysosomes, which have been clearly identified as a target of annexin binding [127] . Later, annexins also play a role in the endocytic pathway [128], including intracellular positioning of recycling endosomes [129] and multivesicular body (MVB) biogenesis [130,131]. It has also been shown that ANXA2 is required for the establishment of cell polarity, cytokinesis and endocytosis in HeLa cells []. In addition to these original studies, evidence has continued to show that certain animal annexins function at different stages of membrane transport. Over a dozen annexins can be expressed in a single mammalian cell, form a sophisticated Ca2+ sensory network and can bind to membranes in a concentration-dependent manner, starting with the most sensitive ANXA2, followed by ANXA6, ANXA4 and ANXA1 [132,133] . . In addition, they are translocated to different membranes after induction [31,32]. ANXA1 and ANXA2 were translocated to the endosomal membrane, where ANXA2 was also involved in intracellular vesicle movement. ANXA5 was associated with LE and Golgi, ANXA6 with Golgi, vacuolar membranes and ER. ANXA1 and ANXA5 are located in the cell nucleus. These results suggest that a particular annexin is functionally specialized to control individual sets of subcellular membranes in response in a variety of ways. Ca2+ is known to regulate various aspects of secretion and vesicle transport, starting with the very first stages - transport from the ER to the Golgi through fusion with the PM and endocytosis. However, the role of Ca2+ in the early stages of secretion is still poorly understood, especially when compared to the rather extensive knowledge of its function in the various phases of the LSP beyond the Golgi-Golgi channel, such as B. vacuolar transport, exocytosis, endocytosis, and membrane recycling components. There is now evidence that Ca2+ contributes to the regulation of secretion and vesicle transport at the various stages of vesicle transport through the interaction with annexins. Within the ESP, ANXA11 has been shown to regulate ER-to-Golgi transport by stabilizing the SEC31A protein (a component of an outer cage of COPII-coated vesicles) at the ER [ 113 ]. ANXA2 is found at exocytotic sites in chromaffin granules and is required for Ca 2+ -dependent formation of lipid microdomains essential for exocytosis in these cells [ 134 ]. Reduced expression of ANXA2 leads to inhibited exocytosis in chromaffin granules. Recently, another study found that the binding of ANXA2 to membranes induces the formation of microdomains enriched in cholesterol and phosphatidylinositol-4,5-bisphosphate [PtdIns(4,5)P2] and also the budding of vesicles inward into giant unilamellar vesicles [135] ]. Finally, ANXA2 was shown to be able to partially restore Ca 2+ -dependent secretion in digitonin-permeabilized chromaffin cells [ 136 ]. A key role in the events leading to exocytosis has been attributed to a 16 amino acid peptide (P16) corresponding to the C-terminal end of ANXA2 (shared with 14-3-3 proteins). The partial effect of P16 on secretion under different experimental conditions suggests that annexin is not essential for exocytosis but only regulates its extent, possibly by establishing calcium-dependent protein-protein interactions [137]. There is evidence, both in vitro and in vivo, that ANXA7 regulates catecholamine release from stimulated chromaffin cells and that BoNT type C-mediated inhibition of membrane fusion is due to cleavage of ANXA7 [138]. Animal annexins have also recently been found to be involved in endocytosis trafficking [139]. ANXA2 facilitates endocytic trafficking of antisense oligonucleotides used as tools in this research [140]. Recent studies also showed an involvement of ANXA1 in membrane trafficking [141,142]. ANXA1 and ANXA2 have been shown to be involved in retrograde trafficking [143,144], and annexin A2 has been suggested to play a role in the biogenesis of MVBs [131]. A similar study showed that ANXA1 is required for EGF-stimulated inward vesiculation in multivesicular endosomes [ 145 ]. Two mechanisms of endosome fusion have been proposed, one that is dependent on calcium and annexins and another that is calcium independent [146]. Finally, numerous studies suggest that annexins are important for membrane repair. This process is induced by the uncontrolled influx of extracellular Ca2+ and requires intact membrane transport [147]. Depending on the type of membrane damage, there are different mechanisms for membrane repair

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including: (i) Ca 2+ -activated homotypic vesicle fusion and patch formation undergoing exocytosis [ 148 ]; (ii) endocytosis of membrane regions permeabilized by pore-forming toxins or mechanically damaged [149,150]; (iii) Blistering, formation of protrusions from the damaged membrane segments that detach locally from the cortical cytoskeleton with adjacent cytoplasm [151]. Annexins are able to induce aggregation and fusion of intracellular vesicles/lysosomes and thus can support exocytosis and provide a scaffold for endosome formation. ANXA1 and ANXA2 contribute to membrane repair through the aggregation and fusion of intracellular vesicles [152]. The vesicles are sealed from the cell body by plugs of ANXA1 [151]. ANXA5, in turn, can form a two-dimensional network under the damaged plasma membrane [153]. Finally, ANXA6 assembles a “cap” on the membrane repair patch [154]. 4.2. Plant Annexins All modern families of plant annexins descend from one to three founders in mosses and ferns [3]. The major expansion of annexin genes in plants occurred about 450 million years ago during the colonization of the more demanding drought-prone terrestrial environment, before the divergence between monocots and dicots [155]. To date, more than 400 plant annexins have been identified and classified into 17 phylogenetically related subfamilies based on primary amino acid sequence. Like their animal counterparts, plant annexins form families with multiple members within a respective species (8 in Arabidopsis [156]; 9 in rice Oryza sativa [157]; 12 in maize Zea mays [158] and potato Solanum tuberosum [10]; 11 in Solanum lycopersicum [159] and 23 in soybean [158]). Plant annexins were first purified based on their ability to bind phospholipids/membranes in a Ca 2+ -dependent manner. They have been shown to be associated with vacuole, nuclear and plasma membranes and the Golgi and Golgi-derived vesicles [160–162]. Results suggesting an involvement of annexin in plant secretory processes originally came from early localization studies. Using immunological approaches, annexins were localized at the tip of polar growing cells, such as pollen tubes and fern rhizoids [163,164]. In addition, immunolocalization studies in peas found high levels of annexin immunostaining in other highly secretory cell types, such as B. young, developing xylem cells and cells of the outer root sheath [160]. In this study, immunogold localization showed annexin association with the trans-Golgi membranes, Golgi-derived secretory vesicles, and the PM. Notably, the degree of immunogold labeling of annexin in root cap cells increased sharply as the root cap cell advanced toward the periphery and transitioned into highly secretory outer root cap cells. Another early study also showed that plant annexins, like animal annexins, can induce aggregation of secretory vesicles in vitro [165]. The results of the early studies showed only a role for plant annexins in secretory processes. However, in two pioneering studies it was shown that a maize annexin induces secretory vesicle aggregation [165] and has a direct positive effect on exocytosis in root sheath protoplasts [166]. Addition of annexin protein promoted Ca 2+ -dependent secretion of polysaccharides from root sheath cells, while anti-annexin antibodies blocked this ability. Interestingly, addition of GTP inhibited secretion in the protoplast cells of the root sheath. The results of recent studies have shown that plant annexins play an important role in abiotic and biotic stress responses. Ectopic expression of Arabidopsis ANNAT1 and its homologs confers tolerance to drought, osmotic and saline treatments, and tolerance to pathogen attack. These observed stress-tolerant phenotypes are likely due to the antioxidant activity associated with this annexin. This protein activity continues in all biological kingdoms [12,167–172]. For example, expression of ANNAT1 homologues can limit lipid peroxidation induced by stress treatments. The exact mechanism of action of the antioxidant activity of plant annexins is still unclear, however, certain animal and plant annexins have conserved redox-sensitive cysteine ​​residues, such as Cys-8 in mammalian ANXA2 [173,174]. Irreversible inhibition of this cysteine ​​by treatment with N-ethylmaleimide did not affect phospholipid binding but abolished in vitro liposome aggregation. Cys-8 can potentially undergo repeated redox cycling, and after oxidation by ROS is possible

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subsequently reduced by the thioredoxin system [174]. Indeed, compared to the control cells, ANXA2-depleted cell lines accumulated higher amounts of ROS and showed increased activation of oxidative stress-induced proapoptotic kinases (p38, JNK, AKT) and a higher degree of cell death [174]. Plant annexins may use a similar mechanism, possibly even more so as they have more reactive cysteines [6]. Interestingly, ectopic expression or overexpression of certain plant annexins also induces changes in gene expression [ 12 ]. This observation suggests the possible Ca 2+ -induced translocation of annexin into the nucleus [161,174–177] . However, as previously mentioned, annexins may also play a role in stress responses by regulating endocytosis and exocytosis, which are known to play a crucial role in plant stress responses. There are also a number of biochemical properties in plant annexins that may be important for the regulation of endocytic and exocytic processes, including F-actin binding, modulation of Ca2+ influx activity, and association with lipid microdomains. Plant annexins of various species have been shown to bind F-actin in vitro [178–180] and some have an IRI motif in their fourth repeat that may be responsible for actin binding. There is a review that highlights the importance of annexins in the regulation of the organization and dynamics of actin filaments in plants [181]. Ca 2+ is a critical signal controlling polarity in plant cells, and membrane transport is an important component in establishing and maintaining cell polarity [182]. Although it is still controversial whether some plant annexins act directly as Ca 2+ -permeable channels, it is clear that certain plant annexins modulate Ca 2+ influx. For example, ANNAT1 has been shown to facilitate Ca2+ influx in response to H2O2, which may regulate growth [9,183]. Certainly, their presence at the apex of polar growing cells suggests a possible role in regulated Ca2+ influx during cell expansion. Association with lipid microdomains is an important component of annexin-mediated exocytosis in animal cells. These microdomains are detergent-resistant membrane fractions, and plant annexins have recently been identified in such fractions [184]. Although these in vitro findings do not necessarily indicate that annexins function in membrane microdomains in vivo, some initial experiments with the transient expression of ANNAT1 in Nicotiana benthamiana showed that it colocalizes in situ with a lipidated fluorescent protein specific for sterol-enriched proteins are membrane microdomains. [185]. In vivo, however, there may be exceptions to this paradigm for annexin function, as certain annexins can bind to membranes in a Ca 2+ -independent manner and some annexins are also found in the apoplast, e.g. B. ANNAT1 [186]. 4.3. Plant annexins in membrane trafficking - where we are now In the model plant Arabidopsis (ANNAT1-8) there are eight members of the annexin family. Studies of these annexins have shown that different annexins have different and overlapping tissue- and development-specific expression patterns as well as different subcellular localization [156]. There are also data suggesting that certain plant annexins are multifunctional. The best example of such a protein is ANNAT1, the most abundant and well-studied annexin in Arabidopsis. It and its homologues in other plant species have been shown to promote Ca2+ influx and have antioxidant effects. It also appears to play an important role in seed germination and in abiotic and biotic stress responses [3,7,187]. Data collected so far showed that in Arabidopsis cells, individual annexins have the potential to regulate membrane events in different cell compartments (Figure 2). ANNAT1 was found in the PM proteome [188], while ANNAT3 was found in the tonoplast proteome [189]. Another Arabidopsis annexin, ANNAT4, has been shown to interact with two sets of Qa SNAREs located on the PM (AtSYP121, AtSYP122, AtSYP123) and the PVC/tonoplast (AtSYP21 and AtSYP22) [190]. Localization studies suggest that ANNAT1 may also play a role in secretion. There is a strong correlation between the immunolocalization patterns of ANNAT1 and ANNAT2 and the secretion of polysaccharides as determined using 3H-galactose in young seedlings [164]. There are also marked differences between ANNAT1 and ANNAT2 in their localization patterns: ANNAT1 is localized in the cell periphery of root epidermal cells, root hairs and root sheath cells, while ANNAT2 is localized in the cell periphery of

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Hypocotyl and cotyledon epidermal cells. These results suggest that ANNAT1 and ANNAT2 may regulate Golgi-mediated secretion of polysaccharide precursors to the PM. Two other Arabidopsis annexins, ANNAT3 and ANNAT5, are also involved in membrane trafficking. In the case of ANNAT3, recent evidence suggests that it plays a direct role in vacuolar post-Golgi transport [191]. Another study using RNAi showed that suppression of ANNAT5 expression in Arabidopsis pollen resulted in severe sterility [192]. In the case of ANNAT5, gain-of-function mutants expressing higher levels of this annexin were resistant to brefeldin A (BFA)-induced inhibition of pollen germination and pollen tube elongation [193]. Indeed, there was a positive correlation between the level of ANNAT5 expression and its ability to block BFA action on pollen. This finding may be related to the observation that BFA treatment of pollen has multiple effects on membrane transport. It promotes Golgi-mediated secretion but inhibits endocytosis [194], disrupts endomembrane transport by negatively affecting the formation of a specific subset of endosomes, and indirectly blocks actin polymerization at the tip of the pollen tube [195]. As ANNAT5 was also shown to bind actin, pollen from the ANNAT5 gain-of-function mutant was treated with lactrunculin B (LatB) [193], which blocks actin polymerization and thus inhibits pollen germination and pollen tube elongation. Their results showed that higher ANNAT5 levels could not overcome LatB-mediated effects on pollen. Although ANNAT5 appears to regulate pollen endomembrane transport in a Ca 2+ -dependent manner, the exact mechanisms have yet to be determined. The elongation of cotton fibers is mediated by both diffuse and polar growth. The first annexin identified in cotton has been shown to associate with callose synthase and possibly regulate the activity of this enzyme [196]. Recently, two cotton fiber annexins, GHANN2 and GHFANNX, have been shown to be important in fiber elongation. GHANN2 RNAi silencing inhibits fiber growth as well as Ca2+ influx at the tip of expanding fibers, which may be necessary for Ca2+-driven maintenance of polar secretion [197]. The GFP-tagged GHFANNX was located on the peripheral and cytoplasmic side of the cotton fiber tip tip, and the authors suggested that this annexin might be associated with Golgi-derived vesicles in this region [ 198 ]. GHFANNXA was found to promote Ca2+ influx and cause reorganization of actin filaments in cotton fibers, two mechanisms that could potentially affect the delivery of cell wall components necessary for expansion [199]. 5. The secretory transport pathway The secretory transport pathway in eukaryotic cells has been the subject of intensive research for decades. The current knowledge of these processes in plant cells is summarized in Figure 2. Despite intensive efforts, many aspects are still unclear. In plants, protein transport between the ER and Golgi is not dependent on the cytoskeleton, but is energy dependent. Two mechanisms for ER-to-Golgi transport of newly synthesized proteins have been proposed: non-selective mass flow and charge trapping [200,201] . In principle, they are not mutually exclusive, but instead cooperate to varying degrees depending on the type of protein [202]. For bulk flow, the basic protein machinery for ongoing vesicle traffic is sufficient and no additional factors are required. In plant cells, it is efficient enough to maintain the transport rate of soluble proteins through the secretory pathway [203]. In contrast, cargo trapping is a selective process and requires both the presence of sorting signals on proteins and dedicated protein machinery to perform the separation and cargo concentration in the donor compartment. In this case, the charge is concentrated before it leaves the donor space. Protein loading and vesicle transport between different membrane compartments is based on the action of small monomeric GTPases. The Arabidopsis genome contains 93 genes encoding small GTPases [204]. The high degree of evolutionary conservation of GTPases in eukaryotes suggests their importance in cellular signaling processes [205]. Among them, the Rab, Rho and Arf GTPase families act in different steps of membrane transport, from the formation of vesicles on donor membranes, to controlling transport specificity, to facilitating the docking and fusion of vesicles with the target membranes [206–208]. The Arabidopsis Arf GTPase family consists of 21 proteins and its members mediate

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the assembly of several sets of coat protein complexes [204]. For example, AtARF1 facilitates assembly of COPI envelopes and AtSAR1 mediates ER-to-Golgi transport through COPII-coated vesicles. The second family of proteins that determine organelle identity and provide specificity for targeted membrane fusion events, SNARE families [83,208,209]. RAB GTPases promote initial docking, while subsequent fusions of vesicles and target membranes are performed by SNAREs. SNAREs form a complex in which three glutamine-carrying proteins (Qa, Qb, Qc) and an arginine component (R) are required to drive membrane fusion [210]. In vivo, a functional SNARE complex is formed only by the related SNARE partners, although in vitro, as long as a member of each subclass is present, there is no distinction between related and unrelated sets [211]. Apparently, the specificity in plant cells is achieved through the presence of additional mechanisms, possibly through the effect of proofreading proteins such as SM proteins and/or through lateral separation of SNAREs at the junction of fusing organelles [212]. In Arabidopsis, there are 54 SNARE genes, including 18 Qa SNAREs (syntaxins), 11 Qb SNAREs, 8 Qc SNAREs, 14 R SNAREs (VAMPs), and 3 SNAPs (Qb/Qc ) [213]. Most of them are located in specific intracellular compartments: 6 in ER, 9 in Golgi, 4 in TGN, 2 in endosomes, 17 in PM, 7 in PVC/vacuoles, 2 in TGN/PVC/vacuoles and 1 in TGN/PVC / PM. Post-Golgi transport is directed to the PM for secretion or to the tonoplast for vacuolar deposition. Alongside the secretory pathways, there is endocytic trafficking, and both extraction of the transport machinery and degradation of already dispensable proteins are underway. Therefore, tightly regulated molecular mechanisms are required to coordinate multidirectional vesicle movement. Correct vesicle targeting depends on the presence of specific tags in the donor compartment and matching tags on the vesicles. The first selection step is performed by selective charge sorting according to the different vesicle types in the donor compartment. This is achieved through interactions of specific sorting signals from cargo molecules with membrane receptors and coat proteins in the cytosol. Immunolocalization data suggest that annexins are good candidates to participate in the final secretory pathway in plant cells. After budding and removal of the vesicles, the molecular mechanisms that enable the precise transport direction of the vesicles to their respective target sites are based on the differential labeling of the target membranes. This is achieved through a specific lipid composition, e.g. B. the aforementioned increased sterol content and thickness along the secretory pathway, as well as by accumulation of specific molecular species in situ synthesized smaller lipid components such as B. Phosphatidylinositol (PtdIns). ANXA2 has been shown to be important for membrane domain formation at the site of exocytosis in animal cells, has also been found on clathrin-coated vesicles [214] and contains two motifs for interaction with clathrin-recruiting proteins [215] . These observations led to the hypothesis that ANXA2 may be responsible for the coupling of exo- and endocytic events [216]. Based on these results, it can be expected that plant annexins also modulate exo- and endocytosis via the lateral organization of membrane microdomains. Endo- and exocytosis must be in balance, and negatively charged phosphoinositides (PIs, phosphorylated derivatives of phosphatidylinositol) regulate both processes. As discussed later in this review, there are other transport proteins besides annexins that can bind PIs, such as certain epsin and clathrin adapter proteins. Phosphatidylinositol and its phosphorylated forms are minor non-structural components of biological membranes, mainly found on the cytoplasmic fold of the PM. Their transient occurrence due to a high rate of metabolic turnover is suitable for the regulation of a number of cellular processes, including various aspects of membrane transport [28,217]. In mammalian cells, PIs are involved in both exocytosis [218] and endocytosis [219,220]. PIs appear to exert their functions through different mechanisms. First, they are able to recruit specific cytosolic proteins that, via dedicated protein domains, recognize specific headgroups that protrude from the plane of the membrane into the cytosol [221–223] . A number of proteins regulated by PI binding have been identified. During clathrin-mediated endocytosis (CME), PIs-binding proteins such as AP-2, AP180, epsin and dynamin coordinate the recruitment of vesicle coat proteins [224]. Second, due to the inverted conical shape [225], the local accumulation of PIs can affect the biophysical properties of membranes and facilitate the development of areas of increased membrane curvature [226,227]. Therefore, PIs are able to work simultaneously

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stabilize transient stages of fusion of secretory vesicles with the plasma membrane during Ca2+-triggered exocytosis and vesicle budding towards the cytosol during endocytosis [228]. The level of phosphatidylinositol-4,5-bisphosphate (PtdIns(4,5)P2) has been shown to determine the rate of vesicle priming, the size of the readily releasable vesicle pool and ongoing rates of exocytosis in stimulated cells [227] . and regulate SNARE-dependent fusion [229]. Third, PIs can serve as precursors for the formation of soluble inositol polyphosphates. There are notable differences in the spectrum of phosphorylated PI-based species between plants and other eukaryotes. Only five of the seven known PI species have been detected, namely the phosphatidylinositol monophosphates: PtdIns3P, PtdIns4P and PtdIns5P, and the phosphidyloinositol bisphosphates: PtdIns(3,5)P2 and PtdPIns(4,5) common [230], while PtdIns(3 ,4)P2 and PtdIns(3,4,5)P3 have not yet been detected in plants. Detailed information on the molecular targets of PIs is not yet available. The results obtained so far indicate that PtdIns is involved in the regulation of the central machinery of membrane transport and protein sorting. Analysis using fluorescent probes specific for certain types of PtdIns revealed that PtdIns(4,5)P2 is predominantly present in the PM at the tip of growing root hairs under salt stress, PtdIns3P in motile membrane structures or tonoplasts, and PtdIns4P in TGN. PM [231-233]. These distribution patterns are at least partially consistent with the subcellular localization of the individual kinases that catalyze PI synthesis and the phenotypes of the respective knockout mutants [234,235] . Overall, the general conclusion is that delivery/withdrawal of vesicles to and from the PM is accompanied by a progressively increasing degree of phosphorylation (PtdIns→PtdIns4P→PtdIns(4,5)P2) in subsequent membranes [234]. It appears that PIs are also involved in the control of the central machinery for membrane transport and protein sorting in plants. Thus, they affect essential processes such as establishment of cell polarity or cell wall deposition during plant growth, plant development [234] and environmental responses [236]. Although phosphitidylserine is the preferred phospholipid ligand of annexins in biological membranes, certain annexins also have an affinity for other anionic phospholipids, particularly PI. For example, ANXA2, ANXA8 and possibly ANXA1 show calcium-enhanced affinity for phosphatidylinositol-4,5-bisphosphate, although data for the latter are conflicting [237–240] . Despite the lack of a well-defined PtdIns-binding domain in annexins, this interaction is direct and specific. Binding of ANXA2 to PtdIns(4,5)P2 induces the formation or stabilization of actin assembly sites on cell membranes [238,239]. PtdIns(4,5)P2 is localized to cholesterol-rich membrane microdomains in the PM [241], and ANXA2 has been shown to bind cooperatively to cholesterol and PtdIns(4,5)P2-containing bilayers [135], suggesting that ANXA2 may also be involved in the lateral organization of membranes [242]. The selectivity of plant annexins over PIs has not yet been experimentally analyzed, but the similarity in overall structure between plant and animal annexins strongly suggests that there may be similarities in their mode of action. 5.1. Between Golgi and plasma membrane: forward pathway and exocytosis Soluble secretory proteins without sorting signals are secreted by default [243,244]. Similarly, membrane proteins entering the secretory pathway are targeted to the PM unless they have some tags that export them to the vacuoles [66,245]. Analysis of the transport of fluorescently labeled protein revealed that the traffic between the Golgi and the PM is direct and rapid without specific compartments in between [246]. Departure from the Golgi occurs by mass flow, with no further delay en route to the cell periphery. Secretory vesicles of different sizes, capable of transporting mixed amounts of polysaccharides or polysaccharides/glycoproteins, mediate the transport of polysaccharide precursors to the cell surface [246]. After release from the Golgi, the secretory vesicles can undergo maturation, which can result in final charge modifications such as esterification of pectins or further polymerization of polysaccharides [52]. However, recent experiments in mammalian and yeast cells [247,248] suggest that this picture of the signaling pathway is oversimplified and that secretion is an active process regulated by Ca 2+ -binding proteins and sequestering secretory cargo

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Proteins and a TGN-localized Ca2+ pump. Similar mechanisms may also exist in plants [62], which have long been thought to lack Ca 2+ -regulated exocytosis, similar to yeast. Exocytosis is a general term for the final step in the secretory pathway, where secretory vesicles fuse with the PM. The donor compartments for exocytosis are largely (but not exclusively) TNG, but secretory vesicles can also originate from the ER, cis-Golgi and MVB/PVC. The actin cytoskeleton provides a mechanism for vesicle delivery to the PM [249]. After arriving at the membrane, vesicles adhere to the membrane, and after the fusion of these two membranes mediated by a SNARE complex, the contents of the vesicle lumen are released to the apoplast. Through tethering, exocytotic vesicles localize to specific PM domains enriched in PtdIns(4,5)P2 and with a specific lipid content that favors membrane fusion. [250] This process is mediated by a multisubunit complex called the exocyst. In plants, homologs of all eight exocyst subunits identified in animals and yeast (SEC3, SEC5, SEC6, SEC8, SEC10, SEC15, EXO70, EXO84) have been identified [250]. Since the fusion of vesicles and PMs results in a net increase in membrane surface area, endocytosis must balance exocytosis to maintain stable cell volume. For example, when guard cells open, their volume and PM area increase by up to about 50% due to coordinated vesicle fusion and fission [251–254] . Knowledge of the mechanisms of exocytosis in plant cells is much less advanced compared to knowledge of endocytosis. Exocytosis in plants appears to be a regulated, inducible process. The previously proposed distinction between "constitutive" and "regulated" exocytosis is misleading, at least with regard to the molecular mechanism, which appears to be fundamentally the same in different secretory events. It is now assumed that plant secretion is always regulated, but that fusion with PM is not the rate-limiting step. Thus, plant secretion is regulated on different time scales and co-regulated by Ca 2+ , which is the main trigger for regulated exocytosis in animals [249]. Thus, Ca2+-binding proteins such as annexins may have an influence on secretion and regulate this process. There is compelling evidence that some annexins are involved in exocytosis. For example, ANXA2 is able to promote the formation of GM1/cholesterol-containing lipid microdomains corresponding to active sites of exocytosis [134]. Transmission electron microscopy (TEM) has shown that ANXA2 crosslinks secretory granules to the PM in stimulated neuroendocrine cells [255,256]. In permeabilized chromaffin cells, exogenous ANXA2 can restore activity in response to Ca2+ [257,258]. Exocytosis appears to be controlled by different secretory pathways. One of the best known is SNARE-mediated exocytosis. The Arabidopsis PM contains a defined set of 23 SNAREs [259]. Among them are nine Qa syntaxins (AtSYP111/AtKNOLLE-SYP112, AtSYP121-AtSYP125, AtSYP131-AtSYP132). They can form combinatorial complexes with the other Qb SNAREs also found in the PM (AtVTI12, AtNPSN11-AtNPSN13). There are also PM-specific R-SNAREs (AtVAMP721-AtVAMP722, AtVAMP724-AtVAMP726) [259]. Certain animal annexins have also been shown to interact with SNAREs, either indirectly by affecting the organization of sterol-enriched membrane subdomains or directly by interacting with SNARE members of complexes. In neuroendocrine adrenergic chromaffin cells, stimulation induces membrane translocation of cytosolic ANXA2 to the PM, where it forms a heterotetramer with S100A10. S100A10, in turn, can interact with VAMP2. Enzymatic cleavages of VAMP2 release S100A10 from the plasma membrane and inhibit translocation of ANXA2 to the plasma membrane [260]. ANXA7 associates with SNAP23 both in vitro and in vivo during surfactant secretion in alveolar cells, and this process is calcium dependent [261,262]. Furthermore, ANXA2 has been shown to regulate pulmonary surfactant secretion in type II alveolar epithelial cells through physical interaction with SNAP23 [263]. Cholesterol and sphingolipids are thought to be concentrated in cells of the PM. Fluorescence polarization studies showed that almost half of the plasma membrane exists in ordered domains at 37 °C, and about 70–80% of the surface of several cell types is resistant to solubilization by cold Triton X-100 [264]. In polarized epithelial cells, the apical membranes are specialized for secretion

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is almost completely in the liquid ordered state [265]. It has been shown that ANXA2 can induce the formation of PI(4,5)P2-enriched domains in the plasma membrane, which can affect the local membrane curvature of the lipid bilayer [128]. As previously mentioned, the Arabidopsis annexin ANNAT4 was recently shown to interact with AtSYP121, AtSYP122, AtSYP123, AtSYP21 and AtSYP22 [190]. The functional relevance of these interactions remains to be determined, but this annexin may regulate vesicle fusion via its ability to interact with specific SNARE complexes. It is tempting to speculate that other plant annexins may interact with specific SNARE proteins, and this is an important hypothesis to be tested. 5.2. Between Golgi and Plasma Membrane: Reversal Pathway and Endocytosis As in animal and yeast cells, endosomes in plants exchange both biosynthetic and endocytic cargo. While l plays a fundamental role in the function of clathrin in cell polarity, growth, structuring and organogenesis in plants. In recent decades, endocytosis in plant cells has been shown to play a fundamental role in determining cell polarity, growth, patterning and organogenesis [266,267]. Endocytosis allows cells to dynamically control the composition and functional properties of the PM, for example by internalizing receptors that would control signaling at the PM [268]. Localization of auxin efflux transporters (PINs) is also partially regulated by endocytic recycling [269], and asymmetric localization of PINs determines cell polarity and promotes directional intercellular auxin flux [23]. Interestingly, the expression of ANNAT2 in Arabidopsis root cap columella cells is altered in pin2 mutants in response to hypergravity [270]. The authors of this study hypothesize that PIN2 may be responsible for the normal expression and localization of ANNAT2 during gravitational responses. In plant cells, endocytosis is also involved in cell plate formation [271]. Membrane proteins and apoplastic fluids are constantly obtained through budding, cleavage and formation of endocytic vesicles, which fuse with endosomes, giving rise to early endosomes (EE). In plants, the TGN function as early endosomes that take up the exocytosed cargo [ 46 ]. The TGN functions as an early endosome and receives internalized endocytic vesicles [48,272,273]. Endocytosis is a precisely regulated process whose molecular mechanisms are tightly controlled and isolated from other transport pathways. An Arabidopsis mutant lacking the TGN-localized component and defective in the secretory pathway shows no apparent impairment of endocytic transport [ 274 ]. The elements of the endocytic machinery, viz. H. Lipids and corresponding receptors are recycled to the PM by recycling endosomes, while other cargo proteins undergo sorting and are released from late endosomes to the lytic vacuole for degradation [275,276]. Endosomes can be classified into tubular or multivesicular endosomes according to structural features, or into sorting (SE) or recycling (RE) according to functional criteria [277,278]. In general, transport through the endosomal system depends on maturation, which is achieved through the exchange of components. This process involves removing the remnants of the previous phase of trafficking and introducing new phases in parallel, thereby gaining the competence to take the next step in human trafficking. Furthermore, endosomal maturation is accompanied by acidification of the internal lumen due to increasing levels and activity of membrane V-ATPase (vesicular H + -ATPase subunit a1) [279–281] . In humans, disturbances in this process appear to be a major cause of several neurodegenerative diseases [180]. As in animal and yeast (Saccharomyces cerevisiae) cells, different types of endocytosis have also been described in plants. The major difference in endocytosis between plant and animal cells is the mechanism of vesicle formation, which affects both the vesicle size and the material incorporated into the vesicles. These differences include fluid phase uptake, bacterial phagocytosis and lipid raft-mediated endocytosis [182]. Two types of endocytosis have been documented: clathrin-mediated and membrane microdomain-associated [44,282,283]. Regardless of the type of endocytosis, vesicles are fused into an inner membrane compartment.

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5.3. Multivesicular body/prevacuolar compartment MVBs are formed by fusion of Golgi-derived vesicles carrying newly synthesized vacuolar proteins and from early/recyclable endosomal compartments. Two types of sorting processes occur within the MVB/PVC: recycling of vacuolar cargo receptors mediated by the retromer complex and sorting of PM protein into internal vesicles by the ESCRT machinery [284]. Fusion of MVBs/PVCs with the vacuole results in the release of soluble vacuolar proteins and MVB vesicles into the lumen of the vacuole [191,274]. Thus, MVBs/PVCs serve as gaps that allow proteins to recycle before their fusion with the vacuole. The characteristic feature of MVB/PVC is the presence of intraluminal vesicles (ILV). In yeast and mammals, these vesicles are thought to function as late endosomes. The generation of ILVs is coordinated by the conserved ESCRT machinery (ESCRT-0, -I, -II, -III and the VPS4 complexes) [285]. Plant genomes encode orthologs of three ESCRT-I, II and III complexes, but lack ESCRT-0 [286–289]. Therefore, the other proteins, e.g. B. FREE1 (plant-specific and PVC-localized FYVE domain protein required for endosomal sorting) [290] and TOM1 (target of MYB), for cargo recognition by [41]. RAB-GTPase-mediated MVB/PVC maturation occurs through component exchange. In Arabidopsis, MVB/PVC maturation is associated with the gradual replacement of Rab5 by Rab7 to form a Rab7-positive MVB/PVC. In addition, a fusion between MVB/PVC and autophagosomes was observed [291]. ANNAT3 has been shown to be required for TGN-to-MVB transport in Arabidopsis. In protoplasts of plants with suppressed expression of ANNAT3 by RNAi, MVB maturation was disrupted, resulting in increased co-localization of TGN and MVB markers (YFP-AtSYP61 and mRFP-AtVSR2). Moreover, RNA interference-mediated knockdown plants (∆annat3) had the same phenotype as the dominant-negative mutant of VPS2, a member of the ESCRT-III complex required for internal vesicle cleavage in MVBs. Taken together, these results suggest that ANNAT3 is required for the final step in the release of MVBs as a transport vehicle to the vacuole [191]. 5.4. Between plasma membrane and vacuoles Another peculiarity of the plant endomembrane system, which further increases the complexity of the transport system, is the presence of different types of vacuoles in the same cells. In most mature plant cells, the majority of the cell volume is occupied by a large central vacuole. It provides structural support to plant cells by exerting turgor pressure on the cell wall and drives cell expansion without the need to produce more cytosol. Several early studies characterized a vacuole-specific annexin, VCaB42. This annexin binds calcium in the low nanomolar range [162], co-localizes with a Rop-GTPase, and is thought to play a role in vacuolar biogenesis during cell expansion [292]. Central vacuoles also serve as a site for intracellular storage of water and nutrients, wastes and toxins, as well as sequestration of inactive progenitor forms of proteins/secondary compounds essential for interactions with the environment or other organisms [42]. Vacuoles can also support other highly specialized functions, such as in guard cells, where the rapid fission and fusion of vacuoles allows for rapid changes in cell volume and stomata movement [293]. In young cells, especially during seed development, there are at least two functionally distinct types of vacuoles [294,295]—PSVs and -LVs. PSVs are pH neutral and are responsible for storing nutrients and proteins essential for germination and early seedling growth, while LVs are acidic and serve for protein degradation [49,296,297]. PSV and LV are thought to be separate organelles [294,298–300]. During seed germination, cell type-specific transformation of PSV to LV can occur, and PSVs are rapidly replaced by a central LV to enable rapid elongation of embryo cells [301]. In vegetative cells, e.g. B. in a growing root tip, the fusion of PSV and LV seems to take place [294]. The transport of proteins to vacuoles occurs predominantly from the TGN, but can also start directly from the ER. Such a shortcut may represent a rapid mechanism required for continuous adaptation to a changing environment and adaptation to stress [302]. LV and PSV are the terminal stations for vesicular traffic. Unperturbed post-Golgi trafficking is required for their proper design.

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In general, researchers are just beginning to understand how the plant TGN recognizes and distributes the proteins in different vacuoles [62,303]. During cell transport, proteins are targeted to defined compartments based on the presence of specific integral motifs recognized by compatible receptors. Vacuolar sorting signals (VSS) operating in plants can be divided into three main groups. The first is the sequence-specific vacuolar sorting signal (ssVSR), which is common in the LV targeting protein; i.e. H. the N-terminal NPIR consensus sequence (Asn-Pro-Ile-Arg), which is very strict and does not tolerate any variation. This sequence is usually part of longer propeptides that are cleaved off during protein maturation in the PVC or in the vacuoles. A non-sequence-specific cleavable C-terminal propeptide (CTPP) has been described for a PSV target protein. It is a C-terminal sequence with no clear consensus as to sequence or length, but is usually enriched in hydrophobic amino acids. Finally, there are signals that depend on the tertiary structure of the molecule and are most common in storage proteins. These tertiary structures can be distributed throughout the molecule and achieve their functionality only when the protein adopts its native conformation [297,304]. The VSSs are recognized by sorting receptors responsible for directing proteins to the vacuoles. Two types of such receptors have been described so far: vacuole-sorting receptors (VSRs) [305,306] and receptor homology transmembrane RING H2 domain proteins (RMRs) [307,308] . The major pathway for transport of soluble cargo from the Golgi to the LV requires recognition of ssVSS by VSRs at the TGN and transport to the PVC/MVB [306] of clathrin-coated vesicles before reaching the vacuoles [302] . When vesicles fuse with the PVC/MVB, the VSRs are returned to the TGN for the next round of delivery. When the PVC/MVB fuses with the tonoplast, cargo molecules are released into the vacuole [65]. This stepwise trafficking is aided by the sequential action of Rab GTPases, with Rab11 mediating early transport events and cargo arrival at the PVC, while Rab7 mediates final delivery to the vacuole and increases cargo levels in PVCs [207]. Unlike soluble proteins, the sorting signals for tonoplast-spanning proteins are largely unknown. There are at least three different pathways, and membrane proteins can reach the vacuoles even when Golgi and post-Golgi transport is blocked [63,66,309,310], possibly using the autophagy machinery [311,312]. In plants, proteins with the single TMD in the PVC contain the Yxxφ motif at their C-terminal cytosolic domain [313]. However, the sorting motifs of multi-TMD proteins are still completely unknown. The transport of VSS-VSR complexes from the TGN is currently believed to be a passive process dependent on the release of the TGN from the Golgi stack and its subsequent maturation into an MVB/PVC, similar to endosomes. Therefore, only one type of CCV is produced that recycles membrane proteins back to the PM [60–62,314]. In Arabidopsis, 9 SNAREs localize to the tonoplast, namely AtSYP21 and AtSYP22 (Qa), AtVTI11 and AtVTI13 (Qb), AtSYP51 and AtSYP52 (Qc), and AtVAMP711, AtVAMP712 and AtVAMP713(R). ANNAT4 interacts with two of these SNARES, AtSYP21 and AtSYP22, and is therefore a candidate for regulating vesicle fusion with vacuole membranes. Only one complete SNARE complex has been identified and confirmed to be involved in vacuole transport, and it is of an endosomal type, namely (Qa/Qb/Qc/R) AtSYP22/AtVTI11/AtSYP51/AtVAMP727 [315]. SYP5 subgroup members (AtSYP51 and AtSYP52) interact specifically with SYP2 subgroup syntaxins as well as AtVTI11 and form a SNARE complex involved in TGN-to-PVC trafficking [316]. 5.5. Guideless secretion The secretion of proteins lacking the N-terminal signal sequence and which do not enter the classical ER-mediated secretory pathway in animals is well established. Four general mechanisms have been proposed: (i) direct translocation across the PM (eg, fibroblast growth factor 1, interleukin 1α); (ii) endolysosomal pathways, where cytosolic proteins are transported into intracellular vesicles called endolysosomes via protein conducting channels (IL-1β and HMBG1); the fusion of endolysosomes with the cell membrane and the release of the proteins in the apoplast; (iii) exosome-mediated secretion; and (iv) membrane blebbing or microvesicle release [317].

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Annexins do not contain N-terminal signal sequences in their primary amino acid sequence that direct their secretion, but they have been detected in the phloem sap and in the extracellular matrix of plants [318–321]. Extracellular vesicles/exosomes have been identified in plants and, like animal exosomes, have been suggested to act in part as a novel pathway for the secretion of proteins lacking signal peptides [322]. Interestingly, the presence of ANNAT1 and other membrane transport proteins, including AtSYP121 and AtSYP122, was recently documented in Arabidopsis exosomes [323]. Recently, non-classical secretion has been shown to change rapidly in response to biotic stress. Upon induction with salicylic acid, a large number of normally cytosolic enzymes lack a classic signal peptide, such as e.g. B. superoxide dismutases [321,324,325]. 6. Future perspectives – possible mechanisms for the effect of annexins on cell transport Although there is strong evidence for the involvement of annexins in plant membrane transport, little is known about the details of annexin function in specific membrane transport events, with the notable exception of evidence that ANNAT3 is involved in vesicular transport of soluble vacuolar proteins after the TGN [191]. In general, plant annexins appear to play important roles in both ESP and LSP, including post-Golgi trafficking (Figure 3). Because annexins bind to membranes in response to an increase in cytosolic Ca 2+ levels, they may act similarly to the Ca 2+ sensor calmodulin, with the main difference being that they transduce Ca 2+ signaling to membrane structures and thus may function as Ca 2+ -dependent activators of secretion. international J. Mol. Science. 2017, 18, 863

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Figure 3. Possible targets for annexin involvement in intracellular transport in plant cells. There is evidence that annexins are involved in both early and late intracellular secretory pathways, including endo- and endocellular secretory pathways. Figure 3. Possible targets for transport of annexins into plant cells. There is exocytosis. Annexins have also been proposed to function in conventional constitutive secretion, and there is evidence that annexins are involved in the green Botharrow-forward route and late secretory pathways, including endotonic-conventional secretion; Arrow - reverse route; yellow arrow - endocytic pathway. and exocytosis. Annexins are also thought to act on conventional constitutive secretion. Acknowledgments: We thank Grażyna Dobrowolska, Olga Sztatelman and Stanley Roux for critical reading of the non-conventional secretion; green arrow - forward route, red arrow - back route; the script. This work was supported by the National Science Centre, Poland (grant 2012/06/M/NZ3/00156 to Dorota Konopka-Postupolska) and the National Science Foundation, USA (grant IOS-1027514 to Stanley J., yellow arrow - endocytic route). . Roux and Greg Clark) and National Aeronautics and Space Administration, USA (assignment NNX13AM54G to Stanley J. Roux and Greg Clark). Author Contributions: Dorota Konopka-Postupolska and Greg Clark contributed to manuscript preparation; Greg Clark edited the text. Conflicts of interest: The authors declare that there are no conflicts of interest.

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It is also possible that certain plant annexins may modulate specific endomembrane vesicle fusion events by modifying the pH and membrane potential of endomembrane vesicles. Future research should test the specific membrane and protein interactions of individual annexins to better understand the contribution of annexins to plant membrane transport. ˙ Acknowledgments: We thank Grazyna Dobrowolska, Olga Sztatelman, and Stanley Roux for critical reading of the manuscript. This work was supported by the National Science Center, Poland (Grant 2012/06/M/NZ3/00156 to Dorota Konopka-Postupolska) and the National Science Foundation, USA (Grant IOS-1027514 to Stanley J. Roux and Greg Clark). and National Aeronautics and Space Administration, USA (grant NNX13AM54G to Stanley J. Roux and Greg Clark). Author Contributions: Dorota Konopka-Postupolska and Greg Clark contributed to manuscript preparation; Greg Clark edited the text. Conflicts of interest: The authors declare that there are no conflicts of interest.

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