Requirement for A-type cyclin-dependent kinase and cyclins for the terminal division in the stomatal lineage of Arabidopsis

Yang, Kezhen; Wang, Hongzhe; Xue, Shan; Qu, Xiaoxiao; Zou, Junjie; Le, Jie

doi:10.1093/jxb/eru139

Cited by 43 publications

(48 citation statements)

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“…To determine whether other cell parameters were also affected by the enhancer mutation during cotyledon growth, we analyzed cell images collected from 3-to 6-d-old cotyledons (SI Appendix, Fig. S1A) using a different cell-clearing method (30). We found that CA1-1 cells at day 6 also had a slightly smaller area on average than WT and that cae2-1 CA1-1 had the smallest cells at all stages (SI Appendix, Fig.…”

Section: Resultsmentioning

confidence: 99%

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C-terminal domain (CTD) phosphatase links Rho GTPase signaling to Pol II CTD phosphorylation in Arabidopsis and yeast

Zhang

Yang

Chen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Rho GTPases, including the Rho, Cdc42, Rac, and ROP subfamilies, act as pivotal signaling switches in various growth and developmental processes. Compared with the well-defined role of cytoskeletal organization in Rho signaling, much less is known regarding transcriptional regulation. In a mutant screen for phenotypic enhancers of transgenic Arabidopsis plants expressing a constitutively active form of ROP2 (designated CA1-1), we identified RNA polymerase II (Pol II) C-terminal domain (CTD) phosphatase-like 1 (CPL1) as a transcriptional regulator of ROP2 signaling. We show that ROP2 activation inhibits CPL1 activity by promoting its degradation, leading to an increase in CTD Ser5 and Ser2 phosphorylation. We also observed similar modulation of CTD phosphorylation by yeast Cdc42 GTPase and enhanced degradation of the yeast CTD phosphatase Fcp1 by activated ROP2 signaling. Taken together, our results suggest that modulation of the Pol II CTD code by Rho GTPase signaling represents an evolutionarily conserved mechanism in both unicellular and multicellular eukaryotes.Rho GTPase | ROP GTPase | Pol II | CTD code | CPL1

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Section: Resultsmentioning

confidence: 99%

“…Images of cotyledon cells were collected using either agarose gel imprinting (60) or an ethanol/acetic acid treatment-based method (30). The Shape Factor was determined using the equation (4π × area/perimeter 2 ) as described (29).…”

Section: Methodsmentioning

confidence: 99%

C-terminal domain (CTD) phosphatase links Rho GTPase signaling to Pol II CTD phosphorylation in Arabidopsis and yeast

Zhang

Yang

Chen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Therefore, the expression of SPCH is under tight and dynamic control, which is crucial for defining stomatal pattern and density. SPCH has been shown to be regulated through phosphorylation by MITOGEN ACTIVATED PROTEIN KINASE (MAPKs), GLYCOGEN SYNTHASE 3 KINASE (GSK3) and CYCLIN DEPENDENT KINASE (CDK) families at the post-translational level (Gudesblat et al, 2012;Lampard et al, 2009;Yang et al, 2014). Phosphorylation by MAPKs or GSK3 targets SPCH for degradation, leading to decreased entry divisions and ultimately a lower stomatal density (Lampard et al, 2009;Gudesblat et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

IDD16 negatively regulates stomatal initiation via trans‐repression of SPCH in Arabidopsis

Lin

Feng

et al. 2019

Plant Biotechnology Journal

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Summary In Arabidopsis , the initiation and proliferation of stomatal lineage cells is controlled by SPEECHLESS ( SPCH ). Phosphorylation of SPCH at the post‐translational level has been reported to regulate stomatal development. Here we report that IDD 16 acts as a negative regulator for stomatal initiation by directly regulating SPCH transcription. In Arabidopsis , IDD 16 overexpression decreased abaxial stomatal density in a dose‐dependent manner. Time course analysis revealed that the initiation of stomatal precursor cells in the IDD 16 ‐ OE plants was severely inhibited. Consistent with these findings, the transcription of SPCH was greatly repressed in the IDD 16 ‐ OE plants. In contrast, IDD 16‐ RNA i transgenic line resulted in enhanced stomatal density, suggesting that IDD 16 is an intrinsic regulator of stomatal development. Ch IP analysis indicated that IDD 16 could directly bind to the SPCH promoter. Furthermore, Arabidopsis plants overexpressing IDD 16 exhibited significantly increased drought tolerance and higher integrated water use efficiency ( WUE ) due to reduction in leaf transpiration. Collectively, our results established that IDD 16 negatively regulates stomatal initiation via trans‐repression of SPCH , and thus provide a practical tool for increasing plant WUE through the manipulation of IDD 16 expression.

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“…For example, CYCD4 is involved in stomatal-lineage divisions in the hypocotyls (Kono et al, 2007). Dominant-negative form of CDKB1;1 and CDKA1;1, as well as higher-order mutants of CYCAs inhibit the SCD of GMCs (Boudolf et al, 2004; Yang et al, 2014). It was reported that FLP directly represses CDKB1;1 and CDKA1;1 (Xie et al, 2010; Yang et al, 2014), and FAMA binds to the promoter region of CDKB1;1 (Hachez et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

MUTE Directly Orchestrates Cell State Switch and the Single Symmetric Division to Create Stomata

Han

Sugihara

et al. 2018

Preprint

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Highlights 22 23 •Complete inventories of gene expression in stomatal differentiation state are elucidated 24 •MUTE switches stomatal patterning program initiated by its sister bHLH, SPEECHLESS 25 •MUTE directly induces cell-cycle genes and their direct transcriptional repressors 26 •Incoherent feed-forward loop by MUTE ensures the single division of a stomatal 27 precursor 28 29 30 SUMMARY 31 Precise cell division control is critical for developmental patterning. For the differentiation of a 32 functional stoma, a cellular valve for efficient gas exchange, the single symmetric division of an 33 immediate precursor is absolutely essential. Yet, the mechanism governing the single division 34 event remains unclear. Here we report the complete inventories of gene expression by the 35 Arabidopsis bHLH protein MUTE, a potent inducer of stomatal differentiation. MUTE switches 36 the gene expression program initiated by its sister bHLH, SPEECHLESS. MUTE directly 37 induces a suite of cell-cycle genes, including CYCD5;1, and their transcriptional repressors, 38 FAMA and FOUR LIPS. The architecture of the regulatory network initiated by MUTE represents 39 an Incoherent Type 1 Feed-Forward Loop. Our mathematical modeling and experimental 40 perturbations support a notion that MUTE orchestrates a transcriptional cascade leading to the 41 tightly-restricted, robust pulse of cell-cycle gene expression, thereby ensuring the single cell 42 division to create functional stomata.43 44 93 lineage cells and singular GCs, respectively (MacAlister et al., 2007; Ohashi-Ito and Bergmann, 94 2006). We thus hypothesized that MUTE governs the gene regulatory networks to create 95 stomata. To test this, we performed a genome-wide profiling of early MUTE-responsive genes.96 5 Comparison of SPCH and MUTE target genes revealed how MUTE disconnects stomatal-97 lineage cells from extrinsic inhibitory signals, thus 'locks in' the differentiation program. Contrary 98 to the known role of MUTE in terminating the proliferating meristemoids (Pillitteri et al., 2007), 99 our study identified cell cycle and cell division genes as overwhelming majorities of the MUTE 100 targets. MUTE directly binds to the promoters and upregulates novel and previously described 101 cell-cycle regulators of the GMC symmetric division process. At the same time, MUTE directly 102 binds to the promoters and upregulates FAMA and FLP, which in turn repress the cell-cycle 103 regulators. Our mathematical modeling predictions and experimental perturbations of network 104 motif demonstrate that an incoherent feed-forward loop mediated by MUTE, cell cycle regulators, 105and FAMA/FLP is sufficient to articulate the single symmetric division event with high fidelity. 106Our study establishes the role for MUTE in orchestrating a transcriptional cascade leading to 107 stomatal differentiation and defines a core regulatory circuit for the single symmetric division. 108 109 Results 110 111 MUTE induces and represses specific sets of transcriptomes

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Requirement for A-type cyclin-dependent kinase and cyclins for the terminal division in the stomatal lineage of Arabidopsis

Abstract: SummaryCDKA;1 is required for the termial divison of stomatal development. The results presented here use targeted expression to fine-tune the roles of CDKs and cyclins in regulating guard cell production.

Cited by 43 publications

References 43 publications

C-terminal domain (CTD) phosphatase links Rho GTPase signaling to Pol II CTD phosphorylation in Arabidopsis and yeast

C-terminal domain (CTD) phosphatase links Rho GTPase signaling to Pol II CTD phosphorylation in Arabidopsis and yeast

IDD16 negatively regulates stomatal initiation via trans‐repression of SPCH in Arabidopsis

MUTE Directly Orchestrates Cell State Switch and the Single Symmetric Division to Create Stomata

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