scholarly journals Tuning self-renewal in the Arabidopsis stomatal lineage by hormone and nutrient regulation of asymmetric cell division

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Yan Gong ◽  
Julien Alassimone ◽  
Rachel Varnau ◽  
Nidhi Sharma ◽  
Lily S Cheung ◽  
...  

Asymmetric and self-renewing divisions build and pattern tissues. In the Arabidopsis stomatal lineage, asymmetric cell divisions, guided by polarly localized cortical proteins, generate most cells on the leaf surface. Systemic and environmental signals modify tissue development, but the mechanisms by which plants incorporate such cues to regulate asymmetric divisions are elusive. In a screen for modulators of cell polarity, we identified CONSTITUTIVE TRIPLE RESPONSE1, 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 cell polarity and fate dynamics showed that developmental information may be encoded in both the spatial and temporal asymmetries of polarity proteins. These results provide a framework for a mechanistic understanding of how nutritional status and environmental factors tune stem-cell behavior in the stomatal lineage, ultimately enabling flexibility in leaf size and cell-type composition.

2020 ◽  
Author(s):  
Yan Gong ◽  
Julien Alassimone ◽  
Rachel Varnau ◽  
Nidhi Sharma ◽  
Lily S. Cheung ◽  
...  

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.


Development ◽  
2001 ◽  
Vol 128 (5) ◽  
pp. 631-643 ◽  
Author(s):  
V. Orgogozo ◽  
F. Schweisguth ◽  
Y. Bellaiche

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.


2019 ◽  
Author(s):  
Matthew H. Rowe ◽  
Juan Dong ◽  
Annika K. Weimer ◽  
Dominique C. Bergmann

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.


2019 ◽  
Author(s):  
Pedro M Domingos ◽  
Andreas Jenny ◽  
David del Alamo ◽  
Marek Mlodzik ◽  
Hermann Steller ◽  
...  

ABSTRACTThe establishment of planar cell polarity (PCP) in the Drosophila eye requires correct specification of the R3/R4 pair of photoreceptor cells, determined by a Frizzled mediated signaling event that specifies R3 and induces Delta to activate Notch signaling in the neighboring cell, specifying it as R4. Here, we investigated the role of the Notch signaling negative regulator Numb in the specification of R3/R4 fates and PCP establishment in the Drosophila eye. We observed that Numb is transiently upregulated in R3 at the time of R3/R4 specification. This regulation of Numb levels in developing photoreceptors occurs at the post-transcriptional level and is dependent on Dishevelled, an effector of Frizzled signaling, and Lethal Giant Larva. We detected PCP defects in cells homozygous for numb15, but these defects were due to a loss of function mutation in fat (fatQ805*) being present in the numb15 chromosome. However, mosaic overexpression of Numb in R4 precursors (only) caused PCP defects and numb loss-of-function had a modifying effect on the defects found in a hypomorphic dishevelled mutation. Our results suggest that Numb levels are upregulated to reinforce the bias of Notch signaling activation in the R3/R4 pair, two post-mitotic cells that are not specified by asymmetric cell division.


2022 ◽  
Vol 13 (1) ◽  
Author(s):  
Lu Wang ◽  
Dongmeng Li ◽  
Kezhen Yang ◽  
Xiaoyu Guo ◽  
Chao Bian ◽  
...  

AbstractCell polarity is a fundamental feature underlying cell morphogenesis and organismal development. In the Arabidopsis stomatal lineage, the polarity protein BASL controls stomatal asymmetric cell division. However, the cellular machinery by which this intrinsic polarity site is established remains unknown. Here, we identify the PRAF/RLD proteins as BASL physical partners and mutating four PRAF members leads to defects in BASL polarization. Members of PRAF proteins are polarized in stomatal lineage cells in a BASL-dependent manner. Developmental defects of the praf mutants phenocopy those of the gnom mutants. GNOM is an activator of the conserved Arf GTPases and plays important roles in membrane trafficking. We further find PRAF physically interacts with GNOM in vitro and in vivo. Thus, we propose that the positive feedback of BASL and PRAF at the plasma membrane and the connected function of PRAF and GNOM in endosomal trafficking establish intrinsic cell polarity in the Arabidopsis stomatal lineage.


PLoS ONE ◽  
2013 ◽  
Vol 8 (10) ◽  
pp. e77097 ◽  
Author(s):  
Claudiane Guay ◽  
Érik Joly ◽  
Émilie Pepin ◽  
Annie Barbeau ◽  
Lisa Hentsch ◽  
...  

2021 ◽  
Author(s):  
Pénélope Darnat ◽  
Angelique Burg ◽  
Jérémy Sallé ◽  
Jérôme Lacoste ◽  
Sophie Louvet-Vallée ◽  
...  

Abstract Cell proliferation and cell polarity need to be precisely coordinated to orient the asymmetric cell divisions crucial for generating cell diversity in epithelia. In many instances, the Frizzled/Dishevelled planar cell polarity pathway is involved in mitotic spindle orientation, but how this is spatially and temporally coordinated with cell cycle progression has remained elusive. Using Drosophila sensory organ precursor cells as a model system, we show that Cyclin A, the main Cyclin driving the transition to M-phase of the cell cycle, is recruited to the apical-posterior cortex in prophase by the Frizzled/Dishevelled complex. This cortically localized Cyclin A then regulates the orientation of the division by recruiting Mud, a homologue of NuMA, the well-known spindle-associated protein. The observed non-canonical subcellular localization of Cyclin A reveals this mitotic factor as a direct link between cell proliferation, cell polarity and spindle orientation.


2005 ◽  
Vol 73 (3) ◽  
pp. 1377-1385 ◽  
Author(s):  
M. Aaron Baxter ◽  
Bradley D. Jones

ABSTRACT An important step in Salmonella enterica serovar Typhimurium virulence is the ability to invade the intestinal epithelium. The invasion process requires a large number of genes encoded on Salmonella pathogenicity island 1 (SPI-1) at centisome 63 as well as genes located in other positions throughout the chromosome. Expression of the invasive phenotype is tightly regulated by environmental cues that are processed by a complex regulatory scheme. A central player in the invasion regulatory pathway is the HilA protein, which is transcriptional activator belonging to the OmpR/ToxR family. A number of positive regulators (hilC, hilD, fis, sirA/barA, csrAB, phoBR, fadD, envZ/ompR, and fliZ) and negative regulators (hha, hilE, lon, ams, phoP c and pag) have been identified that are able to alter expression of hilA transcription. Recent work has found that hilA transcription requires the HilD protein for activation. Other work has emphasized the importance of HilE as a negative regulator of hilA. Overexpression of hilE superrepresses hilA transcription, as well as the invasive phenotype. Two-hybrid experiments suggest that HilE exerts its regulatory influence on hilA through protein-protein interactions with HilD as the protein does not bind to the hilA promoter nor does it affect hilD transcription. As it seems likely that hilE plays an important role in translating environmental signals into invasion gene regulation, we have attempted to identify how the hilE gene itself is regulated. Our results indicate that the fimYZ genes, response regulatory proteins involved in type 1 fimbrial gene expression and recently implicated in motility gene regulation, are important activators of hilE expression. These findings indicate that invasion gene expression is coregulated with motility and adherence and provide experimental evidence that the expression of these virulence phenotypes is a subset of the overall regulation of bacterial physiology.


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