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Displaying results 1 to 10 of 11.

Publications

He, J.; Yang, B.; Hause, G.; Rössner, N.; Peiter-Volk, T.; Schattat, M. H.; Voiniciuc, C.; Peiter, E.; The trans-Golgi-localized protein BICAT3 regulates manganese allocation and matrix polysaccharide biosynthesis Plant Physiol. 190, 2579-2600, (2022) DOI: 10.1093/plphys/kiac387

Abstract Manganese (Mn2+) is essential for a diversity of processes, including photosynthetic water splitting and the transfer of glycosyl moieties. Various Golgi-localized glycosyltransferases that mediate cell wall matrix polysaccharide biosynthesis are Mn2+ dependent, but the supply of these enzymes with Mn2+ is not well understood. Here, we show that the BIVALENT CATION TRANSPORTER 3 (BICAT3) localizes specifically to trans-cisternae of the Golgi. In agreement with a role in Mn2+ and Ca2+ homeostasis, BICAT3 rescued yeast (Saccharomyces cerevisiae) mutants defective in their translocation. Arabidopsis (Arabidopsis thaliana) knockout mutants of BICAT3 were sensitive to low Mn2+ and high Ca2+ availability and showed altered accumulation of these cations. Despite reduced cell expansion and leaf size in Mn2+-deficient bicat3 mutants, their photosynthesis was improved, accompanied by an increased Mn content of chloroplasts. Growth defects of bicat3 corresponded with an impaired glycosidic composition of matrix polysaccharides synthesized in the trans-Golgi. In addition to the vegetative growth defects, pollen tube growth of bicat3 was heterogeneously aberrant. This was associated with a severely reduced and similarly heterogeneous pectin deposition and caused diminished seed set and silique length. Double mutant analyses demonstrated that the physiological relevance of BICAT3 is distinct from that of ER-TYPE CA2+-ATPASE 3, a Golgi-localized Mn2+/Ca2+-ATPase. Collectively, BICAT3 is a principal Mn2+ transporter in the trans-Golgi whose activity is critical for specific glycosylation reactions in this organelle and for the allocation of Mn2+ between Golgi apparatus and chloroplasts.
Publications

Yang, B.; Hofmann, F.; Usadel, B.; Voiniciuc, C.; Seed hemicelluloses tailor mucilage properties and salt tolerance New Phytol. 229, 1946-1954, (2021) DOI: 10.1111/nph.17056

While Arabidopsis seed coat epidermal cells have become an excellent genetic system to study the biosynthesis and structural roles of various cell wall polymers, the physiological function of the secreted mucilaginous polysaccharides remains ambiguous. Seed mucilage is shaped by two distinct classes of highly substituted hemicelluloses along with cellulose and structural proteins, but their interplay has not been explored.We deciphered the functions of four distinct classes of cell wall polymers by generating a series of double mutants with defects in heteromannan, xylan, cellulose, or the arabinogalactan protein SALT-OVERLY SENSITIVE 5 (SOS5), and evaluating their impact on mucilage architecture and seed germination during salt stress.We discovered that muci10 seeds, lacking heteromannan branches, had elevated tolerance to salt stress, while heteromannan elongation mutants exhibited reduced germination in calcium chloride (CaCl2). By contrast, xylan made by MUCILAGE-RELATED21 (MUCI21) was found to be required for the adherence of mucilage pectin to microfibrils made by CELLULOSE SYNTHASE5 (CESA5) as well as to a SOS5-mediated network.Our results indicate that the substitution of xylan and glucomannan in seeds can fine-tune mucilage adherence and salt tolerance, respectively. The study of germinating seeds can thus provide insights into the synthesis, modification and function of complex glycans.
Publications

Verhertbruggen, Y.; Bouder, A.; Vigouroux, J.; Alvarado, C.; Geairon, A.; Guillon, F.; Wilkinson, M. D.; Stritt, F.; Pauly, M.; Lee, M. Y.; Mortimer, J. C.; Scheller, H. V.; Mitchell, R. A.; Voiniciuc, C.; Saulnier, L.; Chateigner-Boutin, A.-L.; The TaCslA12 gene expressed in the wheat grain endosperm synthesizes wheat-like mannan when expressed in yeast and Arabidopsis Plant Sci. 302, 110693, (2021) DOI: 10.1016/j.plantsci.2020.110693

Mannan is a class of cell wall polysaccharides widespread in the plant kingdom. Mannan structure and properties vary according to species and organ. The cell walls of cereal grains have been extensively studied due to their role in cereal processing and to their beneficial effect on human health as dietary fiber. Recently, we showed that mannan in wheat (Triticum aestivum) grain endosperm has a linear structure of β-1,4-linked mannose residues. The aim of this work was to study the biosynthesis and function of wheat grain mannan. We showed that mannan is deposited in the endosperm early during grain development, and we identified candidate mannan biosynthetic genes expressed in the endosperm. The functional study in wheat was unsuccessful therefore our best candidate genes were expressed in heterologous systems. The endosperm-specificTaCslA12 gene expressed in Pichia pastoris and in an Arabidopsis thaliana mutant depleted in glucomannan led to the production of wheat-like linear mannan lacking glucose residues and with moderate acetylation. Therefore, this gene encodes a mannan synthase and is likely responsible for the synthesis of wheat endosperm mannan.
Publications

Yang, B.; Voiniciuc, C.; Fu, L.; Dieluweit, S.; Klose, H.; Usadel, B.; TRM 4 is essential for cellulose deposition in Arabidopsis seed mucilage by maintaining cortical microtubule organization and interacting with CESA 3 New Phytol. 221, 881-895, (2019) DOI: 10.1111/nph.15442

The differentiation of the seed coat epidermal (SCE) cells in Arabidopsis thaliana leads to the production of a large amount of pectin‐rich mucilage and a thick cellulosic secondary cell wall. The mechanisms by which cortical microtubules are involved in the formation of these pectinaceous and cellulosic cell walls are still largely unknown.Using a reverse genetic approach, we found that TONNEAU1 (TON1) recruiting motif 4 (TRM4) is implicated in cortical microtubule organization in SCE cells, and functions as a novel player in the establishment of mucilage structure.TRM4 is preferentially accumulated in the SCE cells at the stage of mucilage biosynthesis. The loss of TRM4 results in compact seed mucilage capsules, aberrant mucilage cellulosic structure, short cellulosic rays and disorganized cellulose microfibrils in mucilage. The defects could be rescued by transgene complementation of trm4 alleles. Probably, this is a consequence of a disrupted organization of cortical microtubules, observed using fluorescently tagged tubulin proteins in trm4 SCE cells. Furthermore, TRM4 proteins co‐aligned with microtubules and interacted directly with CELLULOSE SYNTHASE 3 in two independent assays.Together, the results indicate that TRM4 is essential for microtubule array organization and therefore correct cellulose orientation in the SCE cells, as well as the establishment of the subsequent mucilage architecture.
Publications

Pauly, M.; Gawenda, N.; Wagner, C.; Fischbach, P.; Ramírez, V.; Axmann, I. M.; Voiniciuc, C.; The Suitability of Orthogonal Hosts to Study Plant Cell Wall Biosynthesis Plants 8, 516, (2019) DOI: 10.3390/plants8110516

Plant cells are surrounded by an extracellular matrix that consists mainly of polysaccharides. Many molecular components involved in plant cell wall polymer synthesis have been identified, but it remains largely unknown how these molecular players function together to define the length and decoration pattern of a polysaccharide. Synthetic biology can be applied to answer questions beyond individual glycosyltransferases by reconstructing entire biosynthetic machineries required to produce a complete wall polysaccharide. Recently, this approach was successful in establishing the production of heteromannan from several plant species in an orthogonal host—a yeast—illuminating the role of an auxiliary protein in the biosynthetic process. In this review we evaluate to what extent a selection of organisms from three kingdoms of life (Bacteria, Fungi and Animalia) might be suitable for the synthesis of plant cell wall polysaccharides. By identifying their key attributes for glycoengineering as well as analyzing the glycosidic linkages of their native polymers, we present a valuable comparison of their key advantages and limitations for the production of different classes of plant polysaccharides.
Publications

Polko, J. K.; Barnes, W. J.; Voiniciuc, C.; Doctor, S.; Steinwand, B.; Hill, J. L.; Tien, M.; Pauly, M.; Anderson, C. T.; Kieber, J. J.; SHOU4 Proteins Regulate Trafficking of Cellulose Synthase Complexes to the Plasma Membrane Curr. Biol. 28, 3174-3182.e6, (2018) DOI: 10.1016/j.cub.2018.07.076

Cell walls play critical roles in plants, regulating tissue mechanics, defining the extent and orientation of cell expansion, and providing a physical barrier against pathogen attack [1]. Cellulose microfibrils, which are synthesized by plasma membrane-localized cellulose synthase (CESA) complexes, are the primary load-bearing elements of plant cell walls [2]. Cell walls are dynamic structures that are regulated in part by cell wall integrity (CWI)-monitoring systems that feed back to modulate wall properties and the synthesis of new wall components [3]. Several receptor-like kinases have been implicated as sensors of CWI [3, 4, 5], including the FEI1/FEI2 receptor-like kinases [4]. Here, we characterize two genes encoding novel plant-specific plasma membrane proteins (SHOU4 and SHOU4L) that were identified in a suppressor screen of the cellulose-deficient fei1 fei2 mutant. shou4 shou4l double mutants display phenotypes consistent with elevated levels of cellulose, and elevated levels of non-crystalline cellulose are present in this mutant. Disruption of SHOU4 and SHOU4L increases the abundance of CESA proteins at the plasma membrane as a result of enhanced exocytosis. The SHOU4/4L N-terminal cytosolic domains directly interact with CESAs. Our results suggest that the SHOU4 proteins regulate cellulose synthesis in plants by influencing the trafficking of CESA complexes to the cell surface.
Publications

Voiniciuc, C.; Whole-seed Immunolabeling of Arabidopsis Mucilage Polysaccharides Bio Protoc. 7, e2323, (2017) DOI: 10.21769/BioProtoc.2323

In addition to synthesizing and secreting copious amounts of pectic polymers (Young et al., 2008), Arabidopsis thaliana seed coat epidermal cells produce small amounts of cellulose and hemicelluloses typical of secondary cell walls (Voiniciuc et al., 2015c). These components are intricately linked and are released as a large mucilage capsule upon hydration of mature seeds. Alterations in the structure of minor mucilage components can have dramatic effects on the architecture of this gelatinous cell wall. The immunolabeling protocol described here makes it possible to visualize the distribution of specific polysaccharides in the seed mucilage capsule.
Publications

Griffiths, J. S.; Šola, K.; Kushwaha, R.; Lam, P.; Tateno, M.; Young, R.; Voiniciuc, C.; Dean, G.; Mansfield, S. D.; DeBolt, S.; Haughn, G. W.; Unidirectional Movement of Cellulose Synthase Complexes in Arabidopsis Seed Coat Epidermal Cells Deposit Cellulose Involved in Mucilage Extrusion, Adherence, and Ray Formation Plant Physiol. 168, 502-520, (2015) DOI: 10.1104/pp.15.00478

CELLULOSE SYNTHASE5 (CESA5) synthesizes cellulose necessary for seed mucilage adherence to seed coat epidermal cells of Arabidopsis (Arabidopsis thaliana). The involvement of additional CESA proteins in this process and details concerning the manner in which cellulose is deposited in the mucilage pocket are unknown. Here, we show that both CESA3 and CESA10 are highly expressed in this cell type at the time of mucilage synthesis and localize to the plasma membrane adjacent to the mucilage pocket. The isoxaben resistant1-1 and isoxaben resistant1-2 mutants affecting CESA3 show defects consistent with altered mucilage cellulose biosynthesis. CESA3 can interact with CESA5 in vitro, and green fluorescent protein-tagged CESA5, CESA3, and CESA10 proteins move in a linear, unidirectional fashion around the cytoplasmic column of the cell, parallel with the surface of the seed, in a pattern similar to that of cortical microtubules. Consistent with this movement, cytological evidence suggests that the mucilage is coiled around the columella and unwinds during mucilage extrusion to form a linear ray. Mutations in CESA5 and CESA3 affect the speed of mucilage extrusion and mucilage adherence. These findings imply that cellulose fibrils are synthesized in an ordered helical array around the columella, providing a distinct structure to the mucilage that is important for both mucilage extrusion and adherence.
Publications

Voiniciuc, C.; Yang, B.; Schmidt, M. H.-W.; Günl, M.; Usadel, B.; Starting to Gel: How Arabidopsis Seed Coat Epidermal Cells Produce Specialized Secondary Cell Walls Int. J. Mol. Sci. 16, 3452-3473, (2015) DOI: 10.3390/ijms16023452

For more than a decade, the Arabidopsis seed coat epidermis (SCE) has been used as a model system to study the synthesis, secretion and modification of cell wall polysaccharides, particularly pectin. Our detailed re-evaluation of available biochemical data highlights that Arabidopsis seed mucilage is more than just pectin. Typical secondary wall polymers such as xylans and heteromannans are also present in mucilage. Despite their low abundance, these components appear to play essential roles in controlling mucilage properties, and should be further investigated. We also provide a comprehensive community resource by re-assessing the mucilage phenotypes of almost 20 mutants using the same conditions. We conduct an in-depth functional evaluation of all the SCE genes described in the literature and propose a revised model for mucilage production. Further investigation of SCE cells will improve our understanding of plant cell walls.
Publications

Griffiths, J. S.; Tsai, A. Y.-L.; Xue, H.; Voiniciuc, C.; Šola, K.; Seifert, G. J.; Mansfield, S. D.; Haughn, G. W.; SALT-OVERLY SENSITIVE5 Mediates Arabidopsis Seed Coat Mucilage Adherence and Organization through Pectins Plant Physiol. 165, 991-1004, (2014) DOI: 10.1104/pp.114.239400

Interactions between cell wall polymers are critical for establishing cell wall integrity and cell-cell adhesion. Here, we exploit the Arabidopsis (Arabidopsis thaliana) seed coat mucilage system to examine cell wall polymer interactions. On hydration, seeds release an adherent mucilage layer strongly attached to the seed in addition to a nonadherent layer that can be removed by gentle agitation. Rhamnogalacturonan I (RG I) is the primary component of adherent mucilage, with homogalacturonan, cellulose, and xyloglucan constituting minor components. Adherent mucilage contains rays composed of cellulose and pectin that extend above the center of each epidermal cell. CELLULOSE SYNTHASE5 (CESA5) and the arabinogalactan protein SALT-OVERLY SENSITIVE5 (SOS5) are required for mucilage adherence through unknown mechanisms. SOS5 has been suggested to mediate adherence by influencing cellulose biosynthesis. We, therefore, investigated the relationship between SOS5 and CESA5. cesa5-1 seeds show reduced cellulose, RG I, and ray size in adherent mucilage. In contrast, sos5-2 seeds have wild-type levels of cellulose but completely lack adherent RG I and rays. Thus, relative to each other, cesa5-1 has a greater effect on cellulose, whereas sos5-2 mainly affects pectin. The double mutant cesa5-1 sos5-2 has a much more severe loss of mucilage adherence, suggesting that SOS5 and CESA5 function independently. Double-mutant analyses with mutations in MUCILAGE MODIFIED2 and FLYING SAUCER1 that reduce mucilage release through pectin modification suggest that only SOS5 influences pectin-mediated adherence. Together, these findings suggest that SOS5 mediates adherence through pectins and does so independently of but in concert with cellulose synthesized by CESA5.
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