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Suppression of Arabidopsis GGLT1 affects growth by reducing the L-galactose content and borate cross-linking of rhamnogalacturonan-II.

ABSTRACT: Boron is a micronutrient that is required for the normal growth and development of vascular plants, but its precise functions remain a subject of debate. One established role for boron is in the cell wall where it forms a diester cross-link between two monomers of the low-abundance pectic polysaccharide rhamnogalacturonan-II (RG-II). The inability of RG-II to properly assemble into a dimer results in the formation of cell walls with abnormal biochemical and biomechanical properties and has a severe impact on plant productivity. Here we describe the effects on RG-II structure and cross-linking and on the growth of plants in which the expression of a GDP-sugar transporter (GONST3/GGLT1) has been reduced. In the GGLT1-silenced plants the amount of L-galactose in side-chain A of RG-II is reduced by up to 50%. This leads to a reduction in the extent of RG-II cross-linking in the cell walls as well as a reduction in the stability of the dimer in the presence of calcium chelators. The silenced plants have a dwarf phenotype, which is rescued by growth in the presence of increased amounts of boric acid. Similar to the mur1 mutant, which also disrupts RG-II cross-linking, GGLT1-silenced plants display a loss of cell wall integrity under salt stress. We conclude that GGLT1 is probably the primary Golgi GDP-L-galactose transporter, and provides GDP-L-galactose for RG-II biosynthesis. We propose that the L-galactose residue is critical for RG-II dimerization and for the stability of the borate cross-link.

SUBMITTER: Sechet J

PROVIDER: S-EPMC6263843 | biostudies-literature |

REPOSITORIES: biostudies-literature

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The gene responsible for borate cross-linking of pectin Rhamnogalacturonan-II is required for plant reproductive tissue development and fertilization.

Project description:Deficiencies in boron, a microelement that is essential for the growth and development of higher plants, often cause problems in reproductive growth. Rhamnogalacturonan-II (RG-II) in cell wall pectin acts as the sole receptor for boron in plant cells, forming a borate cross-linked RG-II dimer (dRG-II-B), but the physiological functions of dRG-II-B remain unknown. We have previously shown that the pectin glucuronyltransferase 1 gene NpGUT1, which is involved in the biosynthesis of RG-II sugar chains, is essential for the formation of the RG-II-B complex, resulting in tight intercellular attachment in meristematic tissues. Because NpGUT1 expression was found to be abundant in reproductive organs in addition to meristematic tissues, we analyzed the expression and functions of NpGUT1 in more detail in tobacco reproductive tissues. Specific NpGUT1 expression was detected in the tapetum of flower buds and in the pollen, pollen tube tips, and transmitting tissue of the pistils of flowers. Dexamethasone-induced expression of the NpGUT1 antisense gene in flower buds resulted in the formation of sterile flowers with aberrant development of pollen and transmitting tissue. Pollen tubes could not pass through pistils with aborted transmitting tissue, and expression of an NpGUT1 antisense gene in germinating pollen inhibited pollen tube elongation, accompanied by the absence of pectin RG-II and boron in the pollen tube tip. These results indicate that expression of NpGUT1 is required for the development and functions of male and female tissues.

| S-EPMC1637626 | biostudies-literature

Arabinogalactan-Proteins as Boron-Acting Enzymes, Cross-Linking the Rhamnogalacturonan-II Domains of Pectin.

Project description:Most pectic rhamnogalacturonan-II (RG-II) domains in plant cell walls are borate-bridged dimers. However, the sub-cellular locations, pH dependence, reversibility and biocatalyst involvement in borate bridging remain uncertain. Experiments discussed here explored these questions, utilising suspension-cultured plant cells. In-vivo pulse radiolabelling showed that most RG-II domains dimerise extremely quickly (<4 min after biosynthesis, thus while still intraprotoplasmic). This tallies with the finding that boron withdrawal causes cell wall weakening within 10-20 min, and supports a previously proposed biological role for boron/RG-II complexes specifically at the wall/membrane interface. We also discuss RG-II monomer ↔ dimer interconversion as monitored in vitro using gel electrophoresis and a novel thin-layer chromatography method to resolve monomers and dimers. Physiologically relevant acidity did not monomerise dimers, thus boron bridge breaking cannot be a wall-loosening mechanism in 'acid growth'; nevertheless, recently discovered RG-II trimers and tetramers are unstable and may thus underpin reversible wall loosening. Dimerising monomers in vitro by B(OH)3 required the simultaneous presence of RG-II-binding 'chaperones': co-ordinately binding metals and/or ionically binding cationic peptides. Natural chaperones of the latter type include highly basic arabinogalactan protein fragments, e.g., KHKRKHKHKRHHH, which catalyse a reaction [2 RG-II + B(OH)3 → RG-II-B-RG-II], suggesting that plants can 'enzymically' metabolise boron.

| S-EPMC10707938 | biostudies-literature

Identification of putative rhamnogalacturonan-II specific glycosyltransferases in Arabidopsis using a combination of bioinformatics approaches.

Project description:Rhamnogalacturonan-II (RG-II) is a complex plant cell wall polysaccharide that is composed of an ?(1,4)-linked homogalacturonan backbone substituted with four side chains. It exists in the cell wall in the form of a dimer that is cross-linked by a borate di-ester. Despite its highly complex structure, RG-II is evolutionarily conserved in the plant kingdom suggesting that this polymer has fundamental functions in the primary wall organisation. In this study, we have set up a bioinformatics strategy aimed at identifying putative glycosyltransferases (GTs) involved in RG-II biosynthesis. This strategy is based on the selection of candidate genes encoding type II membrane proteins that are tightly coexpressed in both rice and Arabidopsis with previously characterised genes encoding enzymes involved in the synthesis of RG-II and exhibiting an up-regulation upon isoxaben treatment. This study results in the final selection of 26 putative Arabidopsis GTs, including 10 sequences already classified in the CAZy database. Among these CAZy sequences, the screening protocol allowed the selection of ?-galacturonosyltransferases involved in the synthesis of ?4-GalA oligogalacturonides present in both homogalacturonans and RG-II, and two sialyltransferase-like sequences previously proposed to be involved in the transfer of Kdo and/or Dha on the pectic backbone of RG-II. In addition, 16 non-CAZy GT sequences were retrieved in the present study. Four of them exhibited a GT-A fold. The remaining sequences harbored a GT-B like fold and a fucosyltransferase signature. Based on homologies with glycosyltransferases of known functions, putative roles in the RG-II biosynthesis are proposed for some GT candidates.

| S-EPMC3522684 | biostudies-literature

Golgi-localized membrane protein AtTMN1/EMP12 functions in the deposition of rhamnogalacturonan II and I for cell growth in Arabidopsis.

Project description:Appropriate pectin deposition in cell walls is important for cell growth in plants. Rhamnogalacturonan II (RG-II) is a portion of pectic polysaccharides; its borate crosslinking is essential for maintenance of pectic networks. However, the overall process of RG-II synthesis is not fully understood. To identify a novel factor for RG-II deposition or dimerization in cell walls, we screened Arabidopsis mutants with altered boron (B)-dependent growth. The mutants exhibited alleviated disorders of primary root and stem elongation, and fertility under low B, but reduced primary root lengths under sufficient B conditions. Altered primary root elongation was associated with cell elongation changes caused by loss of function in AtTMN1 (Transmembrane Nine 1)/EMP12, which encodes a Golgi-localized membrane protein of unknown function that is conserved among eukaryotes. Mutant leaf and root dry weights were lower than those of wild-type plants, regardless of B conditions. In cell walls, AtTMN1 mutations reduced concentrations of B, RG-II specific 2-keto-3-deoxy monosaccharides, and rhamnose largely derived from rhamnogalacturonan I (RG-I), suggesting reduced RG-II and RG-I. Together, our findings demonstrate that AtTMN1 is required for the deposition of RG-II and RG-I for cell growth and suggest that pectin modulates plant growth under low B conditions.

| S-EPMC8096605 | biostudies-literature

AtHKT1 drives adaptation of Arabidopsis thaliana to salinity by reducing floral sodium content.

Project description:Arabidopsis thaliana high-affinity potassium transporter 1 (AtHKT1) limits the root-to-shoot sodium transportation and is believed to be essential for salt tolerance in A. thaliana. Nevertheless, natural accessions with 'weak allele' of AtHKT1, e.g. Tsu-1, are mainly distributed in saline areas and are more tolerant to salinity. These findings challenge the role of AtHKT1 in salt tolerance and call into question the involvement of AtHKT1 in salinity adaptation in A. thaliana. Here, we report that AtHKT1 indeed drives natural variation in the salt tolerance of A. thaliana and the coastal AtHKT1, so-called weak allele, is actually hyper-functional in reducing flowers sodium content upon salt stress. Our data showed that AtHKT1 positively contributes to saline adaptation in a linear manner. Forward and reverse genetics analysis established that the single AtHKT1 locus is responsible for the variation in the salinity adaptation between Col-0 and Tsu-1. Reciprocal grafting experiments revealed that shoot AtHKT1 determines the salt tolerance of Tsu-1, whereas root AtHKT1 primarily drives the salt tolerance of Col-0. Furthermore, evidence indicated that Tsu-1 AtHKT1 is highly expressed in stems and is more effective compared to Col-0 AtHKT1 at limiting sodium flow to the flowers. Such efficient retrieval of sodium to the reproductive organ endows Tsu-1 with stronger fertility compared to Col-0 upon salt stress, thus improving Tsu-1 adaptation to a coastal environment. To conclude, our data not only confirm the role of AtHKT1 in saline adaptation, but also sheds light on our understanding of the salt tolerance mechanisms in plants.

| S-EPMC5679648 | biostudies-literature

Angiotensin II reduces mitochondrial content in skeletal muscle and affects glycemic control.

Project description:OBJECTIVE: Blockade of angiotensin (Ang) II has been shown to prevent new-onset type 2 diabetes. We focused on the effects of AngII on muscle mitochondria, especially on their biogenesis, as an underlining mechanism of type 2 diabetes. RESEARCH DESIGN AND METHODS: C2C12 cells and C57bl/6 mice were used to examine roles for AngII in the regulation of muscle mitochondria and to explore whether the effect was mediated by type 1 AngII receptor (AT1R) or type 2 receptor (AT2R). RESULTS: C2C12 cells treated with 10(-8)-10(-6) mol/l AngII reduced the mitochondrial content associated with downregulation of the genes involved in mitochondrial biogenesis. The action of AngII was diminished by blockade of AT2R but not AT1R, whereas overexpression of AT2R augmented the effect. AngII increased mitochondrial ROS and decreased mitochondrial membrane potential, and these effects of AngII were significantly suppressed by blockade of either AT1R or AT2R. Chronic AngII infusion in mice also reduced muscle mitochondrial content in association with increased intramuscular triglyceride and deteriorated glycemic control. The AngII-induced reduction in muscle mitochondria in mice was partially, but significantly, reversed by blockade of either AT1R or AT2R, associated with increased fat oxidation, decreased muscle triglyceride, and improved glucose tolerance. Genes involved in mitochondrial biogenesis were decreased via AT2R but not AT1R under these in vivo conditions. CONCLUSIONS: Taken together, these findings imply the novel roles for AngII in the regulation of muscle mitochondria and lipid metabolism. AngII reduces mitochondrial content possibly through AT1R-dependent augmentation of their degradation and AT2R-dependent direct suppression of their biogenesis.

| S-EPMC2646070 | biostudies-literature

Polarized localization and borate-dependent degradation of the Arabidopsis borate transporter BOR1 in tobacco BY-2 cells.

Project description:In Arabidopsis the borate transporter BOR1, which is located in the plasma membrane, is degraded in the presence of excess boron by an endocytosis-mediated mechanism. A similar mechanism was suggested in rice as excess boron decreased rice borate transporter levels, although in this case whether the decrease was dependent on an increase in degradation or a decrease in protein synthesis was not elucidated. To address whether the borate-dependent degradation mechanism is conserved among plant cells, we analyzed the fate of GFP-tagged BOR1 (BOR1-GFP) in transformed tobacco BY-2 cells. Cells expressing BOR1-GFP displayed GFP fluorescence at the plasma membrane, especially at the membrane between two attached cells. The plasma membrane signal was abolished when cells were incubated in medium with a high concentration of borate (3 to 5 mM). This decrease in BOR1-GFP signal was mediated by a specific degradation of the protein after internalization by endocytosis from the plasma membrane. Pharmacological analysis indicated that the decrease in BOR1-GFP largely depends on the increase in degradation rate and that the degradation was mediated by a tyrosine-motif and the actin cytoskeleton. Tyr mutants of BOR1-GFP, which has been shown to inhibit borate-dependent degradation in Arabidopsis root cells, did not show borate-dependent endocytosis in tobacco BY-2 cells. These findings indicate that the borate-dependent degradation machinery of the borate transporter is conserved among plant species.

| S-EPMC3954168 | biostudies-literature

Mutation of Arabidopsis Copper-Containing Amine Oxidase Gene AtCuAO? Alters Polyamines, Reduces Gibberellin Content and Affects Development.

Project description:Polyamines (PAs) are essential metabolites in plants performing multiple functions during growth and development. Copper-containing amine oxidases (CuAOs) catalyse the catabolism of PAs and in Arabidopsis thaliana are encoded by a gene family. Two mutants of one gene family member, AtCuAO?, showed delayed seed germination, leaf emergence, and flowering time. The height of the primary inflorescence shoot was reduced, and developmental leaf senescence was delayed. Siliques were significantly longer in mutant lines and contained more seeds. The phenotype of AtCuAO? over-expressors was less affected. Before flowering, there was a significant increase in putrescine in AtCuAO? mutant leaves compared to wild type (WT), while after flowering both spermidine and spermine concentrations were significantly higher than in WT leaves. The expression of GA (gibberellic acid) biosynthetic genes was repressed and the content of GA1, GA7, GA8, GA9, and GA20 was reduced in the mutants. The inhibitor of copper-containing amine oxidases, aminoguanidine hydrochloride, mimicked the effect of AtCuAO? mutation on WT seed germination. Delayed germination, reduced shoot height, and delayed flowering in the mutants were rescued by GA3 treatment. These data strongly suggest AtCuAO? is an important gene regulating PA homeostasis, and that a perturbation of PAs affects plant development through a reduction in GA biosynthesis.

| S-EPMC7589035 | biostudies-literature

A High-Pressure Praseodymium Fluoride Borate Linking Multiple Structural Features of Apatite-Type Compounds.

Project description:Pr5 (BO4 )3-x (BO3 )x (F,OH)2.67 O0.28 (x?1.6), a boron-containing fluoride-oxoapatite-like compound, was obtained by the application of high-pressure/high-temperature synthesis. It exhibits a superstructure of the apatite type with a tripled c lattice parameter (space group P63 /m) and shows complex anion disorder along the 63 screw axis and occupation of distorted octahedra, as well as almost trigonal planar sites, by oxygen and fluorine atoms. Furthermore, a distinct BO4 /(BO3 +F) group disorder is found; 46?% of the sites being occupied by BO4 groups and 54?% by BO3 groups, with a fluoride ion located near the missing oxygen atom. The rare earth cations in the 4f sites exhibit a specific distorted tricapped trigonal prismatic coordination with a mean metaprism twist angle of 21.3°. The crystal structure of Pr5 (BO4 )3-x (BO3 )x (F,OH)2.67 O0.28 (x?1.6) shows much "flexibility" resulting in split and off-site positions of all other rare earth cations. The title compound therefore combines many structural features of apatite-like compounds, for example biologically highly-important carbonated apatites, shedding more light onto the complex structural chemistry of apatites.

| S-EPMC6392139 | biostudies-literature

Tetra-pyrazine-platinum(II) bis-(tetra-fluoro-borate) acetonitrile hemisolvate.

Project description:The improved synthesis and characterization of tetra-pyrazine-platinum(II) bis-(tetra-fluoro-borate) acetonitrile hemisolvate, [Pt(C(4)H(4)N(2))(4)](BF(4))(2)·0.5CH(3)CN, is reported. The unit cell contains a half equivalent of an acetonitrile solvent mol-ecule per tetra-pyrazine-platinum(II) ion. The coordination geometry of the Pt(II) ion is almost square-planar, with the Pt atom residing on an inversion center. The BF(4) (-) counter-anion, located at a general position, has an idealized tetra-hedral geometry and an acetonitrile solvent mol-ecule, the methyl group of which is disordered over two equal positions, sits on a twofold rotation axis.

| S-EPMC2959766 | biostudies-literature

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