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.

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 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 Proper division plane orientation and mitotic progression together allow normal growth of maize

2017 ◽  
Vol 114 (10) ◽  
pp. 2759-2764 ◽  
Author(s):  
Pablo Martinez ◽  
Anding Luo ◽  
Anne Sylvester ◽  
Carolyn G. Rasmussen
Keyword(s):  
Cell Cycle ◽  
Cell Biology ◽  
Cell Cycle Progression ◽  
Normal Growth ◽  
Mitotic Progression ◽  
Wild Type ◽  
Cycle Progression ◽  
Division Plane ◽  
Plane Orientation ◽  
Division Plane Orientation

How growth, microtubule dynamics, and cell-cycle progression are coordinated is one of the unsolved mysteries of cell biology. A maize mutant,tangled1, with known defects in growth and proper division plane orientation, and a recently characterized cell-cycle delay identified by time-lapse imaging, was used to clarify the relationship between growth, cell cycle, and proper division plane orientation. Thetangled1mutant was fully rescued by introduction of cortical division site localized TANGLED1-YFP. A CYCLIN1B destruction box was fused to TANGLED1-YFP to generate a line that mostly rescued the division plane defect but still showed cell-cycle delays when expressed in thetangled1mutant. Although an intermediate growth phenotype between wild-type and thetangled1mutant was expected, these partially rescued plants grew as well as wild-type siblings, indicating that mitotic progression delays alone do not alter overall growth. These data indicate that division plane orientation, together with proper cell-cycle progression, is critical for plant growth.

scholarly journals SCL28 promotes cell expansion and endoreplication in Arabidopsis by activating SIAMESE-RELATED cyclin-dependent kinase inhibitors.

2021 ◽  
Author(s):  
Camila Goldy ◽  
Virginia L Barrera ◽  
Isaiah Taylor ◽  
Celeste Buchensky ◽  
Rodrigo Vena ◽  
...  
Keyword(s):  
Cell Cycle ◽  
Cell Wall ◽  
Cell Expansion ◽  
Kinase Inhibitors ◽  
Mitotic Cell ◽  
Specific Cell ◽  
Mitotic Cell Cycle ◽  
Cyclin Dependent Kinase ◽  
Division Plane ◽  
Division Plane Orientation

The processes that contribute to plant organ morphogenesis are spatial-temporally organized. Within the meristem the mitotic cell cycle produces new cells that subsequently engage in specific cell expansion and differentiation programs once they exit the division competent zone. The latter is frequently accompanied by endoreplication, being an alternative cell cycle that replicates the DNA without nuclear division, causing a stepwise increase in somatic ploidy. We have previously shown that the Arabidopsis SCL28 transcription factor promotes progression through G2/M and modulates division plane orientation. Here, we demonstrate that SCL28 co-express and regulates genes specific to cell elongation and differentiation, including genes related to cell wall and cytoskeleton assembly. Consistently, this correlates with defects in post-mitotic cell expansion in a scl28 mutant. Strikingly, SCL28 controls expression of 6 members of the SIAMESE/SIAMESE-RELATED (SIM/SMR) family, encoding cyclin-dependent kinase inhibitors with a role in promoting mitotic cell cycle exit and endoreplication onset, both in response to developmental and environmental cues. Consistent with this role, scl28 mutants displayed reduced endoreplication, both in roots and leaves. Altogether, these results suggest that SCL28 controls cell expansion and differentiation by promoting endoreplication onset and by modulating aspects of the biogenesis, assembly and remodeling of the cytoskeleton and cell wall.

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 Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity

2013 ◽  
Vol 4 (1) ◽  
Author(s):  
Stefano Pietra ◽  
Anna Gustavsson ◽  
Christian Kiefer ◽  
Lothar Kalmbach ◽  
Per Hörstedt ◽  
...  
Keyword(s):  
Cell Division ◽  
Planar Polarity ◽  
Division Plane ◽  
Plane Orientation ◽  
Division Plane Orientation ◽  
Cell Division Plane

scholarly journals Multiscale mechanics of mucociliary clearance in the lung

2019 ◽  
Vol 375 (1792) ◽  
pp. 20190160 ◽  
Author(s):  
Janna C. Nawroth ◽  
Anne M. van der Does ◽  
Amy Ryan (Firth) ◽  
Eva Kanso
Keyword(s):  
Cell Biology ◽  
Mucociliary Clearance ◽  
Treatment Options ◽  
Diagnostic Tools ◽  
Regional Variability ◽  
Multiscale Mechanics ◽  
Airway Diseases ◽  
Open Questions ◽  
Human Lungs ◽  
The Relationship

Mucociliary clearance (MCC) is one of the most important defence mechanisms of the human respiratory system. Its failure is implicated in many chronic and debilitating airway diseases. However, due to the complexity of lung organization, we currently lack full understanding on the relationship between these regional differences in anatomy and biology and MCC functioning. For example, it is unknown whether the regional variability of airway geometry, cell biology and ciliary mechanics play a functional role in MCC. It therefore remains unclear whether the regional preference seen in some airway diseases could originate from local MCC dysfunction. Though great insights have been gained into the genetic basis of cilia ultrastructural defects in airway ciliopathies, the scaling to regional MCC function and subsequent clinical phenotype remains unpredictable. Understanding the multiscale mechanics of MCC would help elucidate genotype–phenotype relationships and enable better diagnostic tools and treatment options. Here, we review the hierarchical and variable organization of ciliated airway epithelium in human lungs and discuss how this organization relates to MCC function. We then discuss the relevancy of these structure–function relationships to current topics in lung disease research. Finally, we examine how state-of-the-art computational approaches can help address existing open questions. This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.

Division Plane Establishment and Cytokinesis

2019 ◽  
Vol 70 (1) ◽  
pp. 239-267 ◽  
Author(s):  
Pantelis Livanos ◽  
Sabine Müller
Keyword(s):  
Secretory Pathway ◽  
Preprophase Band ◽  
Cell Plate ◽  
Division Plane ◽  
Spatial Reference ◽  
Division Site ◽  
Eukaryotic Proteins ◽  
Plate Formation ◽  
Membrane Compartment ◽  
Cytoplasmic Content

Plant cells divide their cytoplasmic content by forming a new membrane compartment, the cell plate, via a rerouting of the secretory pathway toward the division plane aided by a dynamic cytoskeletal apparatus known as the phragmoplast. The phragmoplast expands centrifugally and directs the cell plate to the preselected division site at the plasma membrane to fuse with the parental wall. The division site is transiently decorated by the cytoskeletal preprophase band in preprophase and prophase, whereas a number of proteins discovered over the last decade reside continuously at the division site and provide a lasting spatial reference for phragmoplast guidance. Recent studies of membrane fusion at the cell plate have revealed the contribution of functionally conserved eukaryotic proteins to distinct stages of cell plate biogenesis and emphasize the coupling of cell plate formation with phragmoplast expansion. Together with novel findings concerning preprophase band function and the setup of the division site, cytokinesis and its spatial control remain an open-ended field with outstanding and challenging questions to resolve.

scholarly journals Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis

2001 ◽  
Vol 155 (2) ◽  
pp. 239-250 ◽  
Author(s):  
Maren Heese ◽  
Xavier Gansel ◽  
Liliane Sticher ◽  
Peter Wick ◽  
Markus Grebe ◽  
...  
Keyword(s):  
Cell Division ◽  
Membrane Fusion ◽  
Functional Characterization ◽  
Cell Plate ◽  
Yeast Two Hybrid ◽  
Division Plane ◽  
Plant Cytokinesis ◽  
Cell Plate Formation ◽  
Plate Formation ◽  
Two Hybrid

Cytokinesis requires membrane fusion during cleavage-furrow ingression in animals and cell plate formation in plants. In Arabidopsis, the Sec1 homologue KEULE (KEU) and the cytokinesis-specific syntaxin KNOLLE (KN) cooperate to promote vesicle fusion in the cell division plane. Here, we characterize AtSNAP33, an Arabidopsis homologue of the t-SNARE SNAP25, that was identified as a KN interactor in a yeast two-hybrid screen. AtSNAP33 is a ubiquitously expressed membrane-associated protein that accumulated at the plasma membrane and during cell division colocalized with KN at the forming cell plate. A T-DNA insertion in the AtSNAP33 gene caused loss of AtSNAP33 function, resulting in a lethal dwarf phenotype. atsnap33 plantlets gradually developed large necrotic lesions on cotyledons and rosette leaves, resembling pathogen-induced cellular responses, and eventually died before flowering. In addition, mutant seedlings displayed cytokinetic defects, and atsnap33 in combination with the cytokinesis mutant keu was embryo lethal. Analysis of the Arabidopsis genome revealed two further SNAP25-like proteins that also interacted with KN in the yeast two-hybrid assay. Our results suggest that AtSNAP33, the first SNAP25 homologue characterized in plants, is involved in diverse membrane fusion processes, including cell plate formation, and that AtSNAP33 function in cytokinesis may be replaced partially by other SNAP25 homologues.

Cell biology of early events in the plant resistance response to infection by pathogenic fungi

1995 ◽  
Vol 73 (S1) ◽  
pp. 418-425 ◽  
Author(s):  
I. Kobayashi ◽  
L. J. Murdoch ◽  
A. R. Hardham ◽  
H. Kunoh
Keyword(s):  
Plant Resistance ◽  
Cell Biology ◽  
Fungal Pathogens ◽  
Plant Defence ◽  
Pathogenic Fungi ◽  
Callose Deposition ◽  
Resistance Response ◽  
New Genes ◽  
Host Cell Wall ◽  
Plant Cytoskeleton

In addition to passive (or constitutive) defence mechanisms, plants have evolved a range of active (or inducible) responses that occur rapidly on infection with an incompatible (avirulent) pathogen and that are thought to play a major role in the expression of resistance. These defence reactions are only induced if the plant possesses the ability to recognize and respond to the pathogen. Signal reception by the host must initiate a cascade of events that lead to the expression of resistance. Some resistance responses, such as callose deposition, do not require the expression of new genes. Many responses, for example the synthesis and secretion of toxic compounds or molecules that enhance the strength of physical barriers, result from changes in the pattern of gene transcription. Other defence phenomena include hypersensitive cell collapse, intercellular signalling, and the induction of defence gene transcripts in surrounding cells. Changes in cell biochemistry and physiology are accompanied by characteristic structural modifications in the infected cells, such as the redeployment of selected organelles and dramatic modifications of the host cell wall. Recent evidence indicates that microtubules and microfilaments of the plant cytoskeleton facilitate the rapid localization of these and other plant defence responses to the region of infection. Key words: plant resistance, plant cytoskeleton, microtubules, microfilaments, fungal pathogens, polarity of defence response.

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