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Experimental Manipulation of Pectin Architecture in the Cell Wall of the Unicellular Charophyte, Penium Margaritaceum.

ABSTRACT: Pectins represent one of the main components of the plant primary cell wall. These polymers have critical roles in cell expansion, cell-cell adhesion and response to biotic stress. We present a comprehensive screening of pectin architecture of the unicellular streptophyte, Penium margaritaceum. Penium possesses a distinct cell wall whose outer layer consists of a lattice of pectin-rich fibers and projections. In this study, cells were exposed to a variety of physical, chemical and enzymatic treatments that directly affect the cell wall, especially the pectin lattice. Correlative analyses of pectin lattice perturbation using field emission scanning electron microscopy, confocal laser scanning microscopy, and transmission electron microscopy demonstrate that pectin lattice microarchitecture is both highly sensitive and malleable.

SUBMITTER: Palacio-Lopez K

PROVIDER: S-EPMC7360812 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Experimental Manipulation of Pectin Architecture in the Cell Wall of the Unicellular Charophyte, Penium Margaritaceum.

Palacio-Lopez Kattia K Sun Li L Reed Reagan R Kang Eric E Sørensen Iben I Rose Jocelyn K C JKC Domozych David S DS

Frontiers in plant science 20200708

Pectins represent one of the main components of the plant primary cell wall. These polymers have critical roles in cell expansion, cell-cell adhesion and response to biotic stress. We present a comprehensive screening of pectin architecture of the unicellular streptophyte, Penium margaritaceum. Penium possesses a distinct cell wall whose outer layer consists of a lattice of pectin-rich fibers and projections. In this study, cells were exposed to a variety of physical, chemical and ...[more]

PMID: 32733522

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Project description:Background and aimsPenium margaritaceum is a unicellular charophycean green alga with a unique bi-directional polar expansion mechanism that occurs at the central isthmus zone prior to cell division. This entails the focused deposition of cell-wall polymers coordinated by the activities of components of the endomembrane system and cytoskeletal networks. The goal of this study was to elucidate the structural organization of the cortical cytoskeletal network during the cell cycle and identify its specific functional roles during key cell-wall developmental events: pre-division expansion and cell division.MethodsMicrotubules and actin filaments were labelled during various cell cycle phases with an anti-tubulin antibody and rhodamine phalloidin, respectively. Chemically induced disruption of the cytoskeleton was used to elucidate specific functional roles of microtubules and actin during cell expansion and division. Correlation of cytoskeletal dynamics with cell-wall development included live cell labelling with wall polymer-specific antibodies and electron microscopy.Key resultsThe cortical cytoplasm of Penium is highlighted by a band of microtubules found at the cell isthmus, i.e. the site of pre-division wall expansion. This band, along with an associated, transient band of actin filaments, probably acts to direct the deposition of new wall material and to mark the plane of the future cell division. Two additional bands of microtubules, which we identify as satellite bands, arise from the isthmus microtubular band at the onset of expansion and displace toward the poles during expansion, ultimately marking the isthmus of future daughter cells. Treatment with microtubule and actin perturbation agents reversibly stops cell division.ConclusionsThe cortical cytoplasm of Penium contains distinct bands of microtubules and actin filaments that persist through the cell cycle. One of these bands, termed the isthmus microtubule band, or IMB, marks the site of both pre-division wall expansion and the zone where a cross wall will form during cytokinesis. This suggests that prior to the evolution of land plants, a dynamic, cortical cytoskeletal array similar to a pre-prophase band had evolved in the charophytes. However, an interesting variation on the cortical band theme is present in Penium, where two satellite microtubule bands are produced at the onset of cell expansion, each of which is destined to become an IMB in the two daughter cells after cytokinesis. These unique cytoskeletal components demonstrate the close temporal control and highly coordinated cytoskeletal dynamics of cellular development in Penium.

Project description:Background and aimsThe cell walls of charophytic algae both resemble and differ from those of land plants. Cell walls in early-diverging charophytes (e.g. Klebsormidiophyceae) are particularly distinctive in ways that might enable survival in environments that are incompatible with land-plant polymers. This study therefore investigates the structure of Klebsormidium polysaccharides.MethodsThe 'pectin' fraction (defined by extractability) of Klebsormidium fluitans, solubilized by various buffers from alcohol-insoluble residues, was digested with several treatments that (partly) hydrolyse land-plant cell-wall polysaccharides. Products were analysed by gel-permeation and thin-layer chromatography.Key resultsThe Klebsormidium pectic fraction made up ~30-50 % of its alcohol-insoluble residue, was optimally solubilized at pH 3-4 at 100 °C, and contained residues of xylose ≈ galactose > rhamnose > arabinose, fucose, mannose and glucose. Uronic acids were undetectable, and the pectic fraction was more readily solubilized by formate than by oxalate, suggesting a lack of chelation. Some land-plant-targeting hydrolases degraded the Klebsormidium pectic fraction: digestion by α-l-arabinanase, endo-β-(1→4)-d-xylanase and α-d-galactosidase suggests the presence of β-(1→4)-xylan with terminal α-l-arabinose, α-d-galactose and (unexpectedly) rhamnose. 'Driselase' released oligosaccharides of xylose and rhamnose (~1:1), and graded acid hydrolysis of these oligosaccharides indicated a 'rhamnoxylan' with rhamnose side-chains. Partial acid hydrolysis of Klebsormidium pectic fraction released rhamnose plus numerous oligosaccharides, one of which comprised xylose and galactose (~1:2 Gal/Xyl), suggesting a galactoxylan. Lichenase was ineffective, as were endo-β-(1→4)-d-galactanase, endo-β-(1→4)-d-mannanase, β-d-xylosidase and β-d-galactosidase.ConclusionsKlebsormidium pectic fraction possesses many land-plant-like linkages but is unusual in lacking uronic acid residues and in containing rhamnoxylan and galactoxylan domains. Uronic acids allow land-plant and late-diverging charophyte pectins to form Ca2+-bridges, facilitating cell-wall polymer association; their absence from Klebsormidium suggests that neutral heteroxylans rely on alternative cross-linking mechanisms. This lack of dependence on Ca2+-bridges might confer on Klebsormidium the ability to grow in the acidic, metal-rich environments that it tolerates.

Dataset Information

Experimental Manipulation of Pectin Architecture in the Cell Wall of the Unicellular Charophyte, Penium Margaritaceum.

Publications

Experimental Manipulation of Pectin Architecture in the Cell Wall of the Unicellular Charophyte, <i>Penium Margaritaceum</i>.

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