scholarly journals Callose deposition is essential for the completion of cytokinesis in the unicellular alga Penium margaritaceum

2020 ◽  
Vol 133 (19) ◽  
pp. jcs249599 ◽  
Author(s):  
Destiny J. Davis ◽  
Minmin Wang ◽  
Iben Sørensen ◽  
Jocelyn K. C. Rose ◽  
David S. Domozych ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Plate ◽  
Molecular Evidence ◽  
Callose Deposition ◽  
Division Plane ◽  
Unicellular Algae ◽  
A Cell ◽  
Division Cell ◽  
Wall Assembly ◽  
Cell Wall Deposition

ABSTRACTCytokinesis in land plants involves the formation of a cell plate that develops into the new cell wall. Callose, a β-1,3 glucan, accumulates at later stages of cell plate development, presumably to stabilize this delicate membrane network during expansion. Cytokinetic callose is considered specific to multicellular plant species, because it has not been detected in unicellular algae. Here we present callose at the cytokinesis junction of the unicellular charophyte, Penium margaritaceum. Callose deposition at the division plane of P. margaritaceum showed distinct, spatiotemporal patterns likely representing distinct roles of this polymer in cytokinesis. Pharmacological inhibition of callose deposition by endosidin 7 resulted in cytokinesis defects, consistent with the essential role for this polymer in P. margaritaceum cell division. Cell wall deposition at the isthmus zone was also affected by the absence of callose, demonstrating the dynamic nature of new wall assembly in P. margaritaceum. The identification of candidate callose synthase genes provides molecular evidence for callose biosynthesis in P. margaritaceum. The evolutionary implications of cytokinetic callose in this unicellular zygnematopycean alga is discussed in the context of the conquest of land by plants.This article has an associated First Person interview with the first author of the paper.

scholarly journals Callose deposition is essential for the completion of cytokinesis in the unicellular alga, Penium margaritaceum

2020 ◽  
Author(s):  
Destiny J. Davis ◽  
Minmin Wang ◽  
Iben Sørensen ◽  
Jocelyn K.C. Rose ◽  
David S. Domozych ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Plate ◽  
Molecular Evidence ◽  
Callose Deposition ◽  
Division Plane ◽  
Cell Wall Assembly ◽  
Unicellular Algae ◽  
A Cell ◽  
Division Cell ◽  
Wall Assembly

AbstractCytokinesis in land plants involves the formation of a cell plate that develops into the new cell wall. Callose is a β-1,3 glucan that transiently accumulates at later stages of cell plate development and is thought to stabilize the delicate membrane network of the cell plate as it expands. Cytokinetic callose deposition is currently considered specific to multicellular plant species as it has not been detected in unicellular algae. Here we present callose at the cytokinesis junction of the unicellular charophyte, Penium margaritaceum. Notably, callose deposition at the division plane of P. margaritaceum showed distinct, spatiotemporal patterns that could represent distinct roles of this polymer in cytokinesis and cell wall assembly. Pharmacological inhibition of cytokinetic callose deposition by Endosidin 7 treatment resulted in cytokinesis defects, consistent with the essential role for this polymer in P. margaritaceum cell division. Cell wall deposition and assembly at the isthmus zone was also affected by the absence of callose, demonstrating the dynamic nature of new wall assembly in P. margaritaceum. The identification of candidate callose synthase genes provides molecular evidence for callose biosynthesis in P. margaritaceum. The evolutionary implications of cytokinetic callose in this unicellular Zygnematopycean alga is discussed in the context of the conquest of land by plants.Summary StatementEvolutionarily conserved callose in Penium margaritaceum is essential for the completion of cytokinesis.

scholarly journals A Biophysical Model for Plant Cell Plate Development

2020 ◽  
Author(s):  
Muhammad Zaki Jawaid ◽  
Rosalie Sinclair ◽  
Daniel Cox ◽  
Georgia Drakakaki
Keyword(s):  
Cell Wall ◽  
Plant Cell ◽  
Late Stage ◽  
Cell Plate ◽  
Biophysical Model ◽  
Synthesis Rate ◽  
Spontaneous Curvature ◽  
Two Dimensional ◽  
A Cell

AbstractPlant cytokinesis, a fundamental process of plant life, involves de novo formation of a ‘cell plate’ that partitions the cytoplasm of the dividing cell. Cell plate formation is directed by orchestrated delivery, fusion of cytokinetic vesicles, and membrane maturation to the form the nascent cell wall by the timely deposition of polysaccharides such as callose, cellulose, and crosslinking glycans. In contrast to the role of endomembrane protein regulators the role of polysaccharides, in cell plate development is poorly understood. Callose, a β-1-3 glucan polymer, is transiently accumulated during cell plate expansion to be replaced by cellulose in mature stages. Based on the severity of cytokinesis defects in the absence of callose, it has been proposed that it stabilizes this membrane network structure. However, there is currently no theory to understand its role in cytokinesis.Here we extend the Helfrich free energy model for membranes including a phenomenological spreading force as an “areal pressure” generated by callose and/or other polysaccharides. Regular cell plate development in the model is possible, with suitable bending modulus, for a two-dimensional late stage spreading force parameter of between 2–6pN/nm, an osmotic pressure difference of 2–10kPa, and spontaneous curvature between 0–0.04nm−1. With these conditions, stable membrane conformation sizes and morphologies emerge in concordance with stages of cell plate development. With no spreading force, the cell plate fails to mature properly, corroborating experimental observations of cytokinesis arrest in the absence of callose. To reach a nearly mature cell plate, our model requires the late stage onset that the spreading force coupled with a concurrent loss of spontaneous curvature. A simple model based upon production of callose as a quasi-two-dimensional self-avoiding polymer produces the correct phenomenological form of the spreading force, which will be further refined, since matching to our numbers requires an exceptionally high callose synthesis rate.Significance StatementPlant cell division features the development of a unique membrane network called the cell plate that matures to a cell wall which separates the two daughter cells. During cell plate development, callose, a β-1-3 glucan polymer, is transiently synthesized at the cell plate only to be replaced by cellulose in mature stages. The role for this transient callose accumulation at the cell plate is unknown. It has been suggested that callose provides mechanical stability, as well as a spreading force that widens and expands tubular and fenestrated cell plate structures to aid the maturation of the cell plate. Chemical inhibition of callose deposition results in the failure of cell plate development supporting this hypothesis. This publication establishes the need for a spreading force in cell plate development using a biophysical model that predicts cell plate development in the presence and the absence of this force. Such models can potentially be used to decipher for the transition/maturation of membrane networks upon the deposition of polysaccharide polymers.

scholarly journals Phosphorylation-dependent activation of the cell wall synthase PBP2a in Streptococcus pneumoniae by MacP

2018 ◽  
Vol 115 (11) ◽  
pp. 2812-2817 ◽  
Author(s):  
Andrew K. Fenton ◽  
Sylvie Manuse ◽  
Josué Flores-Kim ◽  
Pierre Simon Garcia ◽  
Chryslène Mercy ◽  
...  
Keyword(s):  
Cell Wall ◽  
Streptococcus Pneumoniae ◽  
Drug Targets ◽  
Synthetic Activity ◽  
Bacterial Cells ◽  
Cell Wall Assembly ◽  
Division Site ◽  
A Cell ◽  
Wall Assembly

Most bacterial cells are surrounded by an essential cell wall composed of the net-like heteropolymer peptidoglycan (PG). Growth and division of bacteria are intimately linked to the expansion of the PG meshwork and the construction of a cell wall septum that separates the nascent daughter cells. Class A penicillin-binding proteins (aPBPs) are a major family of PG synthases that build the wall matrix. Given their central role in cell wall assembly and importance as drug targets, surprisingly little is known about how the activity of aPBPs is controlled to properly coordinate cell growth and division. Here, we report the identification of MacP (SPD_0876) as a membrane-anchored cofactor of PBP2a, an aPBP synthase of the Gram-positive pathogen Streptococcus pneumoniae. We show that MacP localizes to the division site of S. pneumoniae, forms a complex with PBP2a, and is required for the in vivo activity of the synthase. Importantly, MacP was also found to be a substrate for the kinase StkP, a global cell cycle regulator. Although StkP has been implicated in controlling the balance between the elongation and septation modes of cell wall synthesis, none of its substrates are known to modulate PG synthetic activity. Here we show that a phosphoablative substitution in MacP that blocks StkP-mediated phosphorylation prevents PBP2a activity without affecting the MacP–PBP2a interaction. Our results thus reveal a direct connection between PG synthase function and the control of cell morphogenesis by the StkP regulatory network.

scholarly journals SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Xiaohang Cheng ◽  
Magdalena Bezanilla
Keyword(s):  
Cell Expansion ◽  
Cell Biology ◽  
Cell Plate ◽  
Seed Plants ◽  
Planar Polarity ◽  
Callose Deposition ◽  
Division Plane ◽  
Open Questions ◽  
Catastrophic Failures ◽  
Division Plane Orientation

SABRE, which is found throughout eukaryotes and was originally identified in plants, mediates cell expansion, division plane orientation, and planar polarity in plants. How and where SABRE mediates these processes remain open questions. We deletedSABREinPhyscomitrium patens, an excellent model for cell biology.SABREnull mutants were stunted, similar to phenotypes in seed plants. Additionally, polarized growing cells were delayed in cytokinesis, sometimes resulting in catastrophic failures. A functional SABRE fluorescent fusion protein localized to dynamic puncta on regions of the endoplasmic reticulum (ER) during interphase and at the cell plate during cell division. WithoutSABRE, cells accumulated ER aggregates and the ER abnormally buckled along the developing cell plate. Notably, callose deposition was delayed in∆sabre, and in cells that failed to divide, abnormal callose accumulations formed at the cell plate. Our findings revealed a surprising and fundamental role for the ER in cell plate maturation.

Control of division plane in normal and griseofulvin-treated microsporocytes of Magnolia

1992 ◽  
Vol 103 (4) ◽  
pp. 1031-1038 ◽  
Author(s):  
R.C. Brown ◽  
B.E. Lemmon
Keyword(s):  
Cell Plate ◽  
Equatorial Region ◽  
Cell Periphery ◽  
Drug Induced ◽  
Spatial Control ◽  
Division Plane ◽  
Spindle Poles ◽  
Wall Deposition ◽  
A Cell ◽  
Multiple Poles

Meiotic cytokinesis in microsporocytes of Magnolia is an unusual form of the simultaneous type; phragmoplast expansion is not accompanied by a cell plate, wall deposition is centripetal, and infurrowing of the cytoplasm after first meiosis results in semicells connected by an isthmus. Dyad domains are further defined by interaction of extensive radial systems of microtubules emanating from the daughter nuclei and by a band of organelles polarized in the equatorial region. After second meiosis, phragmoplasts are organized in the interzonal regions between the sister nuclei in each semicell and also at the interfaces of microtubules forming secondary interzonals between non-sister nuclei. Wall deposition is not initiated until after phragmoplasts expand to the cell periphery and fuse in the isthmus. Centripetal wall deposition in boundaries of spore domains marked by radial arrays of microtubules results in simultaneous quadripartitioning of the microsporocyte into a tetrad of microspores. Treatment of microsporocytes with griseofulvin resulted in atypically placed nuclei and supernumerary nuclei. Abnormalities could be traced to displaced spindles and to spindles with multiple poles. Drug-induced multinucleate coenocytes were able to organize microtubules and initiate cytokinesis in altered patterns. The data suggest that spindle alignment and aggregation of spindle poles are two components of spatial control that are operative in determining the normal arrangement of nuclei, and that the final placement of walls is a function of the postmeiotic nuclear-based radial arrays of microtubules which define spore domains.

The Formation of the Generative Cell in the Pollen Grain of Endymion Non-Scriptus (L)

1968 ◽  
Vol 3 (4) ◽  
pp. 573-578
Author(s):  
R. E. ANGOLD
Keyword(s):  
Cell Wall ◽  
Somatic Cells ◽  
Generative Cell ◽  
Cell Plate ◽  
Pollen Grain ◽  
Generative Nucleus ◽  
A Cell ◽  
Generative Nuclei

The generative cell wall in the pollen grain of Endymion non-scriptus is formed, as in somatic cells, from a cell plate between the vegetative and generative nuclei. This wall curves around the generative nucleus, and fuses with the intine to enclose the generative cell. The generative cell is subsequently freed from the intine by the constriction of the generative cell wall between the generative nucleus and the intine.

scholarly journals SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

2020 ◽  
Author(s):  
Xiaohang Cheng ◽  
Magdalena Bezanilla
Keyword(s):  
Cell Expansion ◽  
Cell Biology ◽  
Cell Plate ◽  
Genetic Alterations ◽  
Callose Deposition ◽  
Division Plane ◽  
Cell Plate Formation ◽  
Tissue Patterning ◽  
Plate Formation ◽  
In Cells

AbstractThe SABRE protein, originally identified in plants, is found throughout eukaryotes. In plants, SABRE has been implicated in cell expansion, division plane orientation and planar polarity. However, how SABRE mediates these processes remains an open question. Here, we have taken advantage of the fact that the bryophyte Physcomitrium patens has a single copy of SABRE, is an excellent model for cell biology and is readily amenable to precise genetic alterations to investigate SABRE’s mechanism of action. We discovered that SABRE null mutants were stunted in both polarized growing and diffusely growing tissues, similar to reported phenotypes in seed plants. However, in polarized growing cells, we observed significant delays in cell plate formation and sometimes catastrophic failures in cell division. We generated a functional SABRE fluorescent fusion protein and determined that it forms dynamic puncta on regions of the endoplasmic reticulum (ER) both in the cytoplasm during interphase and at the new cell plate during division. In the absence of SABRE, ER morphology was severely compromised with large aggregates accumulating in the cytoplasm and abnormal buckling along the developing cell plate late in cytokinesis. In fact, SABRE and the ER maximally accumulated on the developing plate specifically during cell plate maturation, coincident with the timing of the onset of failures in cell plate formation in cells lacking SABRE. Further we discovered that callose deposition is delayed in Δsabre cells, and in cells that failed to divide, abnormal callose accumulations formed at the cell plate. Our findings demonstrated that SABRE functions by influencing the ER and callose deposition, revealing a surprising and essential role for the ER in cell plate maturation. Given that SABRE is conserved, understanding how SABRE influences cell and tissue patterning has profound significance across eukaryotes.

scholarly journals A novel rice fragile culm 24 mutant encodes a UDP-glucose epimerase that affects cell wall properties and photosynthesis

2020 ◽  
Vol 71 (10) ◽  
pp. 2956-2969 ◽  
Author(s):  
Ran Zhang ◽  
Huizhen Hu ◽  
Youmei Wang ◽  
Zhen Hu ◽  
Shuangfeng Ren ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cellulose Microfibril ◽  
Cellulose Microfibrils ◽  
Cell Wall Assembly ◽  
Cellulose Microfibril Orientation ◽  
Plant Photosynthesis ◽  
Altered Cell ◽  
Wall Assembly ◽  
Cell Wall Deposition ◽  
Cell Wall Properties

Abstract UDP-glucose epimerases (UGEs) are essential enzymes for catalysing the conversion of UDP-glucose (UDP-Glc) into UDP-galactose (UDP-Gal). Although UDP-Gal has been well studied as the substrate for the biosynthesis of carbohydrates, glycolipids, and glycoproteins, much remains unknown about the biological function of UGEs in plants. In this study, we selected a novel rice fragile culm 24 (Osfc24) mutant and identified it as a nonsense mutation of the FC24/OsUGE2 gene. The Osfc24 mutant shows a brittleness phenotype with significantly altered cell wall composition and disrupted orientation of the cellulose microfibrils. We found significantly reduced accumulation of arabinogalactan proteins in the cell walls of the mutant, which may consequently affect plant growth and cell wall deposition, and be responsible for the altered cellulose microfibril orientation. The mutant exhibits dwarfism and paler leaves with significantly decreased contents of galactolipids and chlorophyll, resulting in defects in plant photosynthesis. Based on our results, we propose a model for how OsUGE2 participates in two distinct metabolic pathways to co-modulate cellulose biosynthesis and cell wall assembly by dynamically providing UDP-Gal and UDP-Glc substrates.

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