Misregulation of MYB16 causes stomatal cluster formation by disrupting polarity in asymmetric cell division

Stomata and leaf cuticle regulate water evaporation from the plant body and balance the trade-off between photosynthesis and water loss. We identified MYB16, a key transcription factor controlling cutin biosynthesis, from previous stomatal lineage ground cell (SLGC)-enriched transcriptome study. The preferential localization of MYB16 in SLGCs but not meristemoids suggests a link between cutin synthesis and stomatal development. Here, we showed that downregulation of MYB16 in meristemoids was directly mediated by the stomatal master transcription factor, SPEECHLESS (SPCH). The suppression of MYB16 before asymmetric division was crucial for stomatal patterning because overexpression or ectopic expression of MYB16 in meristemoids increased impermeability and elevated stomatal density and clusters. The aberrant pattern of stomata was due to reduced and disrupted establishment of polarity during asymmetric cell division. Manipulating polarity by growing seedlings on hard agar rescued stomatal clusters and polarity defects in MYB16 ectopic lines. By expressing a cutinase in MYB16 ectopic lines, stomatal clustering was reduced, which suggests that the ectopic accumulation of cuticle affects the polarity in asymmetrically dividing cells and causes clustered stomata. Taken together, inhibiting MYB16 expression by SPCH in early stomatal lineage is required to correctly place the polarity complex for proper stomatal patterning during leaf morphogenesis.

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Activation of ACC synthase 2/6 increases stomatal density and cluster on the Arabidopsis leaf epidermis during drought

10.1101/2021.04.27.441570 ◽

2021 ◽

Author(s):

Ming-zhu Jia ◽

Ling-yun Liu ◽

Chen Geng ◽

Chun-peng Song ◽

Jing Jiang

Keyword(s):

Transcription Factor ◽

Drought Stress ◽

Stomatal Density ◽

Acc Synthase ◽

Individual Development ◽

Leaf Epidermis ◽

Stomatal Development ◽

Drought Conditions ◽

The Relationship ◽

Stomatal Lineage

AbstractIt is known that the transcription factor SPEECHLESS (SPCH) drives entry of epidermal cells into stomatal lineage, and that the activation of subtilisin-like protease SDD1 reduces stomatal density and cluster on the epidermis. However, there is still a big gap in our understanding of the relationship between stomatal development and the establishment of stomatal density and pattern, especially during drought. Interestingly, 1-aminocyclopropane-1-carboxylic acid (ACC) not only promotes stomatal development, but also is involved in the establishment of stomatal density and pattern. ACC generation comes from the activity of ACC synthase (ACS), while ACS activity could be mediated by drought. This work showed that the Arabidopsis SPCH activated ACS2/6 expression and ACC-dependent stomatal generation with an increase of stomatal density and cluster under drought conditions; and the possible mechanisms were that ACC-induced Ca2+ shortage in stomatal lineage reduced the inhibition of the transcription factor GT-2 Like 1 (GTL1) on SDD1 expression. These suggest that ACS2/6-dependent ACC accumulation integrated stomatal development with the establishment of stomatal density and pattern by mediating Ca2+ levels in stomatal lineage cells on the leaf epidermis, and this integration is directly related to the growth or survival of plants under escalated drought stress.HighlightACC synthase ACS2/6 activation integrated stomatal individual development with space setting between stomata by mediating Ca2+ levels in stomatal lineage on the leaf epidermis in response to drought.

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The transcription factor ZmNAC49 reduces stomatal density and improves drought tolerance in maize

Journal of Experimental Botany ◽

10.1093/jxb/eraa507 ◽

2020 ◽

Author(s):

Yang Xiang ◽

Xiujuan Sun ◽

Xiangli Bian ◽

Tianhui Wei ◽

Tong Han ◽

...

Keyword(s):

Transcription Factor ◽

Drought Stress ◽

Stomatal Conductance ◽

Drought Tolerance ◽

Transpiration Rate ◽

Transcriptional Activation ◽

Stomatal Density ◽

Stomatal Development ◽

Expression Of Genes ◽

Growth Development

Abstract Drought stress severely limits the growth, development, and productivity of crops, and therefore understanding the mechanisms by which plants respond to drought is crucial. In this study, we cloned a maize NAC transcription factor, ZmNAC49, and identified its function in response to drought stress. We found that ZmNAC49 is localized in the nucleus and has transcriptional activation activity. ZmNAC49 expression is rapidly and strongly induced by drought stress, and overexpression enhances stress tolerance in maize. Overexpression also significant decreases the transpiration rate, stomatal conductance, and stomatal density in maize. Detailed study showed that ZmNAC49 overexpression affects the expression of genes related to stomatal development, namely ZmTMM, ZmSDD1, ZmMUTE, and ZmFAMA. In addition, we found that ZmNAC49 can directly bind to the promoter of ZmMUTE and suppress its expression. Taken together, our results show that the transcription factor ZmNAC49 represses ZmMUTE expression, reduces stomatal density, and thereby enhances drought tolerance in maize.

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The FACT complex and cell cycle progression are essential to maintain asymmetric transcription factor partitioning during cell division

10.1101/075135 ◽

2016 ◽

Author(s):

Eva Herrero ◽

Sonia Stinus ◽

Eleanor Bellows ◽

Peter H Thorpe

Keyword(s):

Cell Cycle ◽

Transcription Factor ◽

Cell Division ◽

Cell Cycle Progression ◽

Asymmetric Cell Division ◽

Cycle Progression ◽

Cellular Processes ◽

Daughter Cells ◽

Cycle Arrest ◽

Reverse Genetic Screen

AbstractThe polarized partitioning of proteins in cells underlies asymmetric cell division, which is an important driver of development and cellular diversity. Like most cells, the budding yeast Saccharomyces cerevisiae divides asymmetrically to give two distinct daughter cells. This asymmetry mimics that seen in metazoans and the key regulatory proteins are conserved from yeast to human. A well-known example of an asymmetric protein is the transcription factor Ace2, which localizes specifically to the daughter nucleus, where it drives a daughter-specific transcriptional network. We performed a reverse genetic screen to look for regulators of asymmetry based on the Ace2 localization phenotype. We screened a collection of essential genes in order to analyze the effect of core cellular processes in asymmetric cell division. This identified a large number of mutations that are known to affect progression through the cell cycle, suggesting that cell cycle delay is sufficient to disrupt Ace2 asymmetry. To test this model we blocked cells from progressing through mitosis and found that prolonged cell cycle arrest is sufficient to disrupt Ace2 asymmetry after release. We also demonstrate that members of the evolutionary conserved FACT chromatin-remodeling complex are required for both asymmetric and cell cycle-regulated localization of Ace2.

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Activation of 1-Aminocyclopropane-1-Carboxylic Acid Synthases Sets Stomatal Density and Clustered Ratio on Leaf Epidermis of Arabidopsis in Response to Drought

Frontiers in Plant Science ◽

10.3389/fpls.2021.758785 ◽

2021 ◽

Vol 12 ◽

Author(s):

Ming-zhu Jia ◽

Ling-yun Liu ◽

Chen Geng ◽

Jing Jiang

Keyword(s):

Transcription Factor ◽

Stomatal Density ◽

Acc Synthase ◽

Drought Response ◽

Leaf Epidermis ◽

Stomatal Development ◽

Growth And Survival ◽

Drought Conditions ◽

Moderate Drought

The adjustment of stomatal density and clustered ratio on the epidermis is the important strategy for plants to respond to drought, because the stoma-based water loss is directly related to plant growth and survival under drought conditions. But the relevant adjustment mechanism still needs to be explored. 1-Aminocyclopropane-1-carboxylate (ACC) is disclosed to promote stomatal development, while in vivo ACC levels depend on activation of ACC synthase (ACS) family members. Based on the findings of ACS expression involving in drought response and several ACS activity inhibitors reducing stomatal density and cluster in drought response, here we examined how ACS activation is involved in the establishment of stomatal density and cluster on the epidermis under drought conditions. Preliminary data indicated that activation of ACS2 and/or ACS6 (ACS2/6) increased stomatal density and clustered ratio on the Arabidopsis leaf epidermis by accumulating ACC under moderate drought, and raised the survival risk of seedlings under escalated drought. Further exploration indicated that, in Arabidopsis seedlings stressed by drought, the transcription factor SPEECHLESS (SPCH), the initiator of stomatal development, activates ACS2/6 expression and ACC production; and that ACC accumulation induces Ca2+ deficiency in stomatal lineage; this deficiency inactivates a subtilisin-like protease STOMATAL DENSITY AND DISTRIBUTION 1 (SDD1) by stabilizing the inhibition of the transcription factor GT-2 Like 1 (GTL1) on SDD1 expression, resulting in an increases of stomatal density and cluster ratio on the leaf epidermis. This work provides a novel evidence that ACS2/6 activation plays a key role in the establishment of stomatal density and cluster on the leaf epidermis of Arabidopsis in response to drought.

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A Spatiotemporal Molecular Switch Governs Plant Asymmetric Cell Division

10.1101/2020.09.05.284380 ◽

2020 ◽

Author(s):

Xiaoyu Guo ◽

Chan Ho Park ◽

Zhi-Yong Wang ◽

Bryce E. Nickels ◽

Juan Dong

Keyword(s):

Cell Division ◽

Cell Fate ◽

Mother Cell ◽

Asymmetric Cell Division ◽

Molecular Switch ◽

Cell Fate Determination ◽

Stomatal Development ◽

Division Plane ◽

Daughter Cells ◽

Commitment To Cell Division

SummaryAsymmetric cell division (ACD) often requires protein polarization in the mother cell to produce daughter cells with distinct identities (“cell-fate asymmetry”). Here, we define a previously undocumented mechanism for establishing cell-fate asymmetry in Arabidopsis stomatal stem cells. In particular, we show that polarization of BSL protein phosphatases promotes stomatal ACD by establishing a “kinase-based signaling asymmetry” in the two daughter cells. BSL polarization in the stomatal ACD mother cell is triggered upon commitment to cell division. Polarized BSL is inherited by the differentiating daughter cell where it suppresses cell division and promotes cell-fate determination. Plants lacking BSL exhibit stomatal over-proliferation, demonstrating BSL plays an essential role in stomatal development. Our findings establish that BSL polarization provides a spatiotemporal molecular switch that enables cell-fate asymmetry in stomatal ACD daughter cells. We propose BSL polarization is triggered by an ACD “checkpoint” in the mother cell that monitors establishment of division-plane asymmetry.

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Altered stomatal patterning accompanies a trichome dimorphism in a natural population of Arabidopsis

10.1101/710889 ◽

2019 ◽

Author(s):

Noriane M. L. Simon ◽

Jiro Sugisaka ◽

Mie N. Honjo ◽

Sverre Aarseth Tunstad ◽

George Tunna ◽

...

Keyword(s):

Natural Population ◽

Stomatal Density ◽

Natural Populations ◽

Experimental Manipulation ◽

Stomatal Development ◽

Cell Fates ◽

Trichome Formation ◽

Stomatal Guard Cells ◽

Growth And Reproduction ◽

Stomatal Patterning

AbstractTrichomes are large epidermal cells on the surface of leaves that are thought to deter herbivores, yet the presence of trichomes can also negatively impact plant growth and reproduction. Stomatal guard cells and trichomes have shared developmental origins, and experimental manipulation of trichome formation can lead to changes in stomatal density. The influence of trichome formation upon stomatal development in natural populations of plants is currently unknown. Here, we show that a natural population of Arabidopsis halleri that includes hairy (trichome-bearing) and glabrous (no trichomes) morphs has differences in stomatal density that are associated with this trichome dimorphism. We found that glabrous morphs had significantly greater stomatal density and stomatal index than hairy morphs. One interpretation is that this arises from a trade-off between the proportions of cells that have trichome and guard cell fates during leaf development. The differences in stomatal density between the two morphs might have impacts upon environmental adaptation, in addition to herbivory deterrence caused by trichome development.

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Asymmetric Transcription Factor Partitioning During Yeast Cell Division Requires the FACT Chromatin Remodeler and Cell Cycle Progression

Genetics ◽

10.1534/genetics.120.303439 ◽

2020 ◽

Vol 216 (3) ◽

pp. 701-716 ◽

Cited By ~ 1

Author(s):

Eva Herrero ◽

Sonia Stinus ◽

Eleanor Bellows ◽

Lisa K. Berry ◽

Henry Wood ◽

...

Keyword(s):

Cell Cycle ◽

Transcription Factor ◽

Cell Division ◽

Cell Cycle Progression ◽

Asymmetric Cell Division ◽

Cycle Progression ◽

Cell Cycle Delay ◽

Cellular Processes ◽

Evolutionarily Conserved ◽

Ram Network

The polarized partitioning of proteins in cells underlies asymmetric cell division, which is an important driver of development and cellular diversity. The budding yeast Saccharomyces cerevisiae divides asymmetrically, like many other cells, to generate two distinct progeny cells. A well-known example of an asymmetric protein is the transcription factor Ace2, which localizes specifically to the daughter nucleus, where it drives a daughter-specific transcriptional network. We screened a collection of essential genes to analyze the effects of core cellular processes in asymmetric cell division based on Ace2 localization. This screen identified mutations that affect progression through the cell cycle, suggesting that cell cycle delay is sufficient to disrupt Ace2 asymmetry. To test this model, we blocked cells from progressing through mitosis and found that prolonged metaphase delay is sufficient to disrupt Ace2 asymmetry after release, and that Ace2 asymmetry is restored after cytokinesis. We also demonstrate that members of the evolutionarily conserved facilitates chromatin transcription (FACT) chromatin-reorganizing complex are required for both asymmetric and cell cycle-regulated localization of Ace2, and for localization of the RAM network components.

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Centromere assembly and non-random sister chromatid segregation in stem cells

Essays in Biochemistry ◽

10.1042/ebc20190066 ◽

2020 ◽

Vol 64 (2) ◽

pp. 223-232 ◽

Cited By ~ 1

Author(s):

Ben L. Carty ◽

Elaine M. Dunleavy

Keyword(s):

Stem Cells ◽

Cell Division ◽

Cell Fate ◽

Sister Chromatid ◽

Asymmetric Cell Division ◽

Protein A ◽

Germline Stem Cells ◽

Sister Chromatids ◽

Centromere Protein A ◽

Oocyte Meiosis

Abstract Asymmetric cell division (ACD) produces daughter cells with separate distinct cell fates and is critical for the development and regulation of multicellular organisms. Epigenetic mechanisms are key players in cell fate determination. Centromeres, epigenetically specified loci defined by the presence of the histone H3-variant, centromere protein A (CENP-A), are essential for chromosome segregation at cell division. ACDs in stem cells and in oocyte meiosis have been proposed to be reliant on centromere integrity for the regulation of the non-random segregation of chromosomes. It has recently been shown that CENP-A is asymmetrically distributed between the centromeres of sister chromatids in male and female Drosophila germline stem cells (GSCs), with more CENP-A on sister chromatids to be segregated to the GSC. This imbalance in centromere strength correlates with the temporal and asymmetric assembly of the mitotic spindle and potentially orientates the cell to allow for biased sister chromatid retention in stem cells. In this essay, we discuss the recent evidence for asymmetric sister centromeres in stem cells. Thereafter, we discuss mechanistic avenues to establish this sister centromere asymmetry and how it ultimately might influence cell fate.

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