Evolution of polarity protein BASL and the capacity for stomatal lineage asymmetric divisions

Differentiation of specialized cell types from self-renewing progenitors requires precise cell cycle control. Plant stomata are generated through asymmetric divisions of a stem-cell-like precursor meristemoid followed by the single symmetric division that creates an adjustable pore surrounded by paired guard cells. The stomatal-lineage-specific transcription factor MUTE terminates the asymmetric divisions and triggers differentiation. However, the role of cell cycle machinery in this transition remains unknown. Through time-lapse imaging, we discover that the symmetric division is slower than the asymmetric division. We identify a plant-specific cyclin-dependent kinase inhibitor, SIAMESE-RELATED4 (SMR4), as a molecular brake that decelerates cell cycle during this transition. SMR4 is directly induced by MUTE and transiently accumulates in differentiating meristemoids. SMR4 physically and functionally associates with CYCD3;1 and extends G1-phase of asymmetric divisions. By contrast, SMR4 fails to interact with CYCD5;1, a MUTE-induced G1 cyclin, and permits the symmetric division. Our work unravels a molecular framework of the proliferation-to-differentiation switch within the stomatal lineage and suggests that a timely proliferative cell cycle is critical for the stomatal fate specification.

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

10.1101/2021.08.05.455184 ◽

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.

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

10.1101/2020.09.16.300830 ◽

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.

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Lineage and stage-specific expressed CYCD7;1 coordinates the single symmetric division that creates stomatal guard cells

10.1101/207837 ◽

2017 ◽

Author(s):

Annika K. Weimer ◽

Juliana L. Matos ◽

Walter Dewitte ◽

James A.H. Murray ◽

Dominique C. Bergmann

Keyword(s):

Cell Division ◽

Developmental Trajectories ◽

Transcriptional Level ◽

Symmetric Division ◽

Distinct Cell ◽

Asymmetric Divisions ◽

Stomatal Guard Cells ◽

Cell Type Specific ◽

Rigid Walls ◽

Stomatal Lineage

AbstractPlants, with cells fixed in place by rigid walls, often utilize spatial and temporally distinct cell division programs to organize and maintain organs. This leads to the question of how developmental regulators interact with the cell cycle machinery to link cell division events with particular developmental trajectories. In Arabidopsis leaves, the development of stomata, two-celled epidermal valves that mediate plant-atmosphere gas exchange, relies on a series of oriented stem-cell-like asymmetric divisions followed by a single symmetric division. The stomatal lineage is embedded in a tissue whose cells transition from proliferation to post-mitotic differentiation earlier, necessitating stomatal lineage-specific factors to prolong competence to divide. We show that the D-type cyclin, CYCD7;1 is specifically expressed just prior to the symmetric guard-cell forming division, and that it is limiting for this division. Further, we find that CYCD7;1 is capable of promoting divisions in multiple contexts, likely through RBR-dependent promotion of the G1/S transition, but that CYCD7;1 is regulated at the transcriptional level by cell-type specific transcription factors that confine its expression to the appropriate developmental window.

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

eLife ◽

10.7554/elife.63335 ◽

2021 ◽

Vol 10 ◽

Author(s):

Yan Gong ◽

Julien Alassimone ◽

Rachel Varnau ◽

Nidhi Sharma ◽

Lily S Cheung ◽

...

Keyword(s):

Cell Polarity ◽

Asymmetric Cell Division ◽

Leaf Size ◽

Negative Regulator ◽

Nutrient Regulation ◽

Environmental Signals ◽

Glucose Signaling ◽

Type Composition ◽

Asymmetric Divisions ◽

Stomatal Lineage

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.

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