scholarly journals A Plant-Specific Polarity Module Establishes Cell Fate Asymmetry in the Arabidopsis Stomatal Lineage

2019 ◽  
Author(s):  
Matthew H. Rowe ◽  
Juan Dong ◽  
Annika K. Weimer ◽  
Dominique C. Bergmann
Keyword(s):  
Genetic Diversity ◽  
Cell Fate ◽  
Cell Polarity ◽  
Asymmetric Cell Division ◽  
Diverse Range ◽  
Asymmetric Cell Divisions ◽  
Cell Divisions ◽  
Collective Activity ◽  
Developmental Contexts ◽  
Stomatal Lineage

SUMMARYGenerating cell polarity in anticipation of asymmetric cell division is required in many developmental contexts across a diverse range of species. Physical and genetic diversity among major multicellular taxa, however, demand different molecular solutions to this problem. The Arabidopsis stomatal lineage displays asymmetric, stem cell-like and oriented cell divisions, which require the activity of the polarly localized protein, BASL. Here we identify the plant-specific BREVIS RADIX (BRX) family as localization and activity partners of BASL. We show that members of the BRX family are polarly localized to peripheral domains in stomatal lineage cells and that their collective activity is required for asymmetric cell divisions. We further demonstrate a mechanism for these behaviors by uncovering mutual, yet unequal dependencies of BASL and the BRX family for each other’s localization and segregation at the periphery of stomatal lineage cells.

scholarly journals Quantitative and dynamic cell polarity tracking in plant cells

2020 ◽  
Author(s):  
Yan Gong ◽  
Rachel Varnau ◽  
Eva-Sophie Wallner ◽  
Dominique C. Bergmann ◽  
Lily S. Cheung
Keyword(s):  
Cell Fate ◽  
Cell Polarity ◽  
Brachypodium Distachyon ◽  
Quantitative Information ◽  
Tissue Level ◽  
Asymmetric Cell Divisions ◽  
Cell Divisions ◽  
Versatile Tool ◽  
Dynamic Cell ◽  
Microscopy Techniques

ABSTRACTQuantitative information on the spatiotemporal distribution of polarized proteins is central for understanding cell-fate determination, yet collecting sufficient data for statistical analysis is difficult to accomplish with manual measurements. Here we present POME, a semi-automated pipeline for the quantification of cell polarity, and demonstrate its application to a variety of developmental contexts. POME analysis reveals that during asymmetric cell divisions in the Arabidopsis thaliana stomatal lineage, polarity proteins BASL and BRXL2 are more asynchronous and less mutually dependent than previously thought. While their interaction is important to maintain their polar localization and recruit other effectors to regulate asymmetric cell divisions, BRXL2 polarization precedes that of BASL and can be initiated in BASL’s absence. Uncoupling of polarization from BASL activity is also seen in Brachypodium distachyon, where we find that the MAPKKK BdYDA1 is segregated and polarized following asymmetric division. Our results demonstrate that POME is a versatile tool, which by itself or combined with tissue-level studies and advanced microscopy techniques can help uncover new mechanisms of cell polarity.

scholarly journals On the edge: Evolution of polarity protein BASL and the capacity for stomatal lineage asymmetric divisions

2021 ◽  
Author(s):  
Ido Nir ◽  
Gabriel O Amador ◽  
Yan Gong ◽  
Nicole K Smoot ◽  
Le Cai ◽  
...  
Keyword(s):  
Cell Fate ◽  
Cell Types ◽  
Cell Fates ◽  
Division Plane ◽  
Asymmetric Cell Divisions ◽  
Cell Divisions ◽  
Distinct Cell ◽  
Asymmetric Divisions ◽  
Stem Cell Divisions ◽  
Stomatal Lineage

Asymmetric and oriented stem cell divisions enable the continued production of patterned tissues. The molecules that guide these divisions include several polarity proteins that are localized to discrete plasma membrane domains, are differentially inherited during asymmetric divisions, and whose scaffolding activities can guide division plane orientation and subsequent cell fates. In the stomatal lineages on the surfaces of plant leaves, asymmetric and oriented divisions create distinct cell types in physiologically optimized patterns. The polarity protein BASL is a major regulator of stomatal lineage division and cell fate asymmetries in Arabidopsis, but its role in the stomatal lineages of other plants was unclear. Here, using phylogenetic and functional assays, we demonstrate that BASL is a dicot specific polarity protein. Among dicots, divergence in BASLs roles may reflect some intrinsic protein differences, but more likely reflects previously unappreciated differences in how asymmetric cell divisions are employed for pattern formation in different species. This multi-species analysis therefore provides insight into the evolution of a unique polarity regulator and into the developmental choices available to cells as they build and pattern tissues.

scholarly journals Tuning of self-renewing capacity in the Arabidopsis stomatal lineage by hormonal and nutrition regulation of asymmetric cell divisions

2020 ◽  
Author(s):  
Yan Gong ◽  
Julien Alassimone ◽  
Rachel Varnau ◽  
Nidhi Sharma ◽  
Lily S. Cheung ◽  
...  
Keyword(s):  
Cell Polarity ◽  
Molecular Mechanisms ◽  
Leaf Size ◽  
Negative Regulator ◽  
Environmental Signals ◽  
Glucose Signaling ◽  
Asymmetric Cell Divisions ◽  
Cell Divisions ◽  
Asymmetric Divisions ◽  
Stomatal Lineage

ABSTRACTAsymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis thaliana stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate the majority of cells on the leaf surface. These divisions can be fine-tuned by systemic and environmental signals to modify tissue development, but the molecular mechanisms by which plants incorporate such cues to regulate asymmetric divisions are largely unknown. In a screen for modulators of cell polarity and asymmetric divisions, we identified a mutation in CONSTITIUTIVE TRIPLE RESPONSE 1, a negative regulator of ethylene signaling. We subsequently revealed antagonistic impacts of ethylene and glucose signaling on the self-renewing capacity of stomatal lineage stem cells. Quantitative analysis of the impacts of these signaling systems on cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. Taken together, our results provide a framework for a mechanistic understanding of how systemic information such as nutritional status and environmental factors tune stem cell behavior in the stomatal lineage, ultimately enabling optimization of leaf size and cell-type composition.

scholarly journals Cytokine receptor-Eb1 interaction couples cell polarity and fate during asymmetric cell division

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Cuie Chen ◽  
Ryan Cummings ◽  
Aghapi Mordovanakis ◽  
Alan J Hunt ◽  
Michael Mayer ◽  
...  
Keyword(s):  
Stem Cells ◽  
Cell Division ◽  
Cell Fate ◽  
Cell Polarity ◽  
Adult Stem Cells ◽  
Asymmetric Cell Division ◽  
Cytokine Receptor ◽  
Spindle Orientation ◽  
Germline Stem Cells ◽  
Self Renewal

Asymmetric stem cell division is a critical mechanism for balancing self-renewal and differentiation. Adult stem cells often orient their mitotic spindle to place one daughter inside the niche and the other outside of it to achieve asymmetric division. It remains unknown whether and how the niche may direct division orientation. Here we discover a novel and evolutionary conserved mechanism that couples cell polarity to cell fate. We show that the cytokine receptor homolog Dome, acting downstream of the niche-derived ligand Upd, directly binds to the microtubule-binding protein Eb1 to regulate spindle orientation in Drosophila male germline stem cells (GSCs). Dome’s role in spindle orientation is entirely separable from its known function in self-renewal mediated by the JAK-STAT pathway. We propose that integration of two functions (cell polarity and fate) in a single receptor is a key mechanism to ensure an asymmetric outcome following cell division.

scholarly journals Emerging mechanisms of asymmetric stem cell division

2018 ◽  
Vol 217 (11) ◽  
pp. 3785-3795 ◽  
Author(s):  
Zsolt G. Venkei ◽  
Yukiko M. Yamashita
Keyword(s):  
Stem Cells ◽  
Stem Cell ◽  
Cell Division ◽  
Asymmetric Cell Division ◽  
Binary Outcomes ◽  
Cellular Mechanisms ◽  
Asymmetric Cell Divisions ◽  
Cell Divisions ◽  
Dividing Cells ◽  
Stem Cell Division

The asymmetric cell division of stem cells, which produces one stem cell and one differentiating cell, has emerged as a mechanism to balance stem cell self-renewal and differentiation. Elaborate cellular mechanisms that orchestrate the processes required for asymmetric cell divisions are often shared between stem cells and other asymmetrically dividing cells. During asymmetric cell division, cells must establish asymmetry/polarity, which is guided by varying degrees of intrinsic versus extrinsic cues, and use intracellular machineries to divide in a desired orientation in the context of the asymmetry/polarity. Recent studies have expanded our knowledge on the mechanisms of asymmetric cell divisions, revealing the previously unappreciated complexity in setting up the cellular and/or environmental asymmetry, ensuring binary outcomes of the fate determination. In this review, we summarize recent progress in understanding the mechanisms and regulations of asymmetric stem cell division.

Lineage, cell polarity and inscuteable function in the peripheral nervous system of the Drosophila embryo

Development ◽  
2001 ◽  
Vol 128 (5) ◽  
pp. 631-643 ◽  
Author(s):  
V. Orgogozo ◽  
F. Schweisguth ◽  
Y. Bellaiche
Keyword(s):  
Nervous System ◽  
Peripheral Nervous System ◽  
Cell Polarity ◽  
Asymmetric Cell Division ◽  
Drosophila Embryo ◽  
Sensory Organ ◽  
Chordotonal Organ ◽  
Cell Divisions ◽  
Ideal System ◽  
Asymmetric Divisions

The stereotyped pattern of the Drosophila embryonic peripheral nervous system (PNS) makes it an ideal system to use to identify mutations affecting cell polarity during asymmetric cell division. However, the characterisation of such mutations requires a detailed description of the polarity of the asymmetric divisions in the sensory organ lineages. We describe the pattern of cell divisions generating the vp1-vp4a mono-innervated external sense (es) organs. Each sensory organ precursor (SOP) cell follows a series of four asymmetric cell divisions that generate the four es organs cells (the socket, shaft, sheath cells and the es neurone) together with one multidendritic (md) neurone. This lineage is distinct from any of the previously proposed es lineages. Strikingly, the stereotyped pattern of cell divisions in this lineage is identical to those described for the embryonic chordotonal organ lineage and for the adult thoracic bristle lineage. Our analysis reveals that the vp2-vp4a SOP cells divide with a planar polarity to generate a dorsal pIIa cell and a ventral pIIb cell. The pIIb cell next divides with an apical-basal polarity to generate a basal daughter cell that differentiates as an md neurone. We found that Inscuteable specifically accumulated at the apical pole of the dividing pIIb cell and regulated the polarity of the pIIb division. This study establishes for the first time the function of Inscuteable in the PNS, and provides the basis for studying the mechanisms controlling planar and apical-basal cell polarities in the embryonic sensory organ lineages.

scholarly journals Regulating the regulator: Numb acts upstream of p53 to control mammary stem and progenitor cell

2015 ◽  
Vol 211 (4) ◽  
pp. 737-739 ◽  
Author(s):  
Marisa M. Faraldo ◽  
Marina A. Glukhova
Keyword(s):  
Stem Cells ◽  
Stem Cell ◽  
Cell Fate ◽  
Cell Expansion ◽  
Progenitor Cell ◽  
Asymmetric Cell Divisions ◽  
Stem Cell Expansion ◽  
Cell Divisions ◽  
Cell Fate Determinant ◽  
Mammary Stem

In this issue, Tosoni et al. (2015. J. Cell Biol. http://dx.doi.org/10.1083/jcb.201505037) report that cell fate determinant and tumor suppressor Numb imposes asymmetric cell divisions in mammary stem cells by regulating p53. Numb thereby restricts mammary stem cell expansion and controls the proliferation and lineage-specific characteristics of their progeny.

scholarly journals Arabidopsis stomatal polarity protein BASL mediates distinct processes before and after cell division to coordinate cell size and fate asymmetries

2021 ◽  
Author(s):  
Yan Gong ◽  
Julien Alassimone ◽  
Andrew Muroyama ◽  
Gabriel Amador ◽  
Rachel Varnau ◽  
...  
Keyword(s):  
Cell Size ◽  
Cell Fate ◽  
Quantitative Imaging ◽  
Cell Types ◽  
Division Plane ◽  
Asymmetric Cell Divisions ◽  
Genetic Manipulations ◽  
Before And After ◽  
Independent Effects ◽  
Stomatal Lineage

In many land plants, asymmetric cell divisions (ACDs) create and pattern differentiated cell types on the leaf surface. In the Arabidopsis stomatal lineage, BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) regulates multiple aspects of ACD including division plane placement and cell fate enforcement. Polarized subcellular localization of BASL is initiated before the ACD and persists for many hours after the division in one of the two daughters. Untangling the respective contributions of polarized BASL before and after division is essential to gain a better understanding of its roles in regulating stomatal lineage ACDs and to uncover the rules that guide leaf pattern. Here we combine quantitative imaging and lineage tracking with genetic tools that provide temporally-restricted BASL expression. We find that pre-division BASL is required for division orientation, whereas BASL polarity post-division ensures proper cell fate commitment. These genetic manipulations allowed us to uncouple daughter-cell size asymmetry from polarity crescent inheritance, revealing independent effects of these two asymmetries on subsequent cell behavior. Finally, we show that there is coordination between the division frequencies of sister cells produced by ACDs, and this coupling requires BASL as an effector of peptide signaling.

Sign in / Sign up

Export Citation Format

Share Document