Calcium signals in guard cells enhance the efficiency by which abscisic acid triggers stomatal closure

Huang, Shouguang; Waadt, Rainer; Nuhkat, Maris; Kollist, Hannes; Hedrich, Rainer; Roelfsema, M. Rob G.

doi:10.1111/nph.15985

Cited by 80 publications

(59 citation statements)

References 76 publications

(126 reference statements)

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“…As a measure of the reliability of our method in identifying cell type–expressed genes and of our ability to correctly annotate biological processes to a cell type, we compared a list of genes enriched in GCs in our analysis with a previous study that profiled GC functions. In agreement with these published reports (Gray, 2005; Lawson, 2009; Song et al, 2014; Niu et al, 2018; Huang et al, 2019), we found genes that respond to oxidative stress, salt stress, bacteria, cadmium ions and are involved in stomatal movement and photosynthesis, are preferentially expressed in GCs (Figure 4A and Figure S6). Our analysis further increased the spectrum of biological processes associated with GC development to include protein transport, vesicle-mediated transport, and cell death (Figure 4A and Figure S6).…”

Section: Resultssupporting

confidence: 93%

Global Dynamic Molecular Profiles of Stomatal Lineage Cell Development by Single-Cell RNA Sequencing

Liu

Zhou

Guo

et al. 2020

Preprint

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30The regulation of stomatal lineage cell development has been extensively investigated. 31 However a comprehensive characterization of this biological process based on 32 single-cell transcriptome analysis has not yet been reported. Here, we performed 33 RNA-seq on over 12,844 individual cells from the cotyledons of five-day-old 34 Arabidopsis seedlings. We identified 11 cell clusters corresponding mostly to cells at 35 specific stomatal developmental stages with a series of new marker genes. 36 Comparative analysis of genes with the highest variable expression in these cell 37 clusters revealed three transcriptional networks that regulate the development of 38 mesophyll and guard cells, as well as the differentiation from protodermal to guard 39 mother cells. We investigated the developmental dynamics of marker genes via 40 pseudo-time analysis which revealed potential interactions between them. The 41 identification of several novel marker genes suggests new regulatory mechanisms 42 during development of stomatal cell lineage. 43 44 45 46 47 48 49 50 51 52 3 / 37 53 54 55 75 MacAlister et al., 2007; Pillitteri et al., 2007). To specify each cell state differentiation, 76 SPCH, MUTE, and FAMA form heterodimers with two paralogous bHLH-leucine 77 zipper (bHLH-LZ) transcription factors, SCREAM (SCRM) and SCRM2 (Kanaoka et 78 al., 2008). In addition, two partially redundant R2R3 MYB transcription factors, 79 FOUR LIPS (FLP) and MYB88, control stomatal terminal differentiation 80 independently of FAMA (GMC to GCs) (Lai et al., 2005; Ohashi-Ito and Bergmann, 81 2006). Two secreted cysteine-rich peptides, EPIDERMAL PATTERNING FACTOR1 82 4 / 37 (EPF1) and EPF2, are expressed at later and earlier stages of stomatal development, 83 respectively. These peptides are perceived by the cell-surface receptors, ERECTA 84 (ER)-family leucine-rich repeat receptor kinases (LRR-RKs), ER-LIKE1 (ERL1) and 85 ERL2, resulting in inhibition of stomatal development (Shpak et al., 2005; Hara et al., 86 2007; Hunt and Gray, 2009b; Lee et al., 2012). The receptor-like protein TOO 87 MANY MOUTHS (TMM) modulates the signaling strength of ER-family receptor 88kinases in a domain-specific manner (Nadeau and Sack, 2002; Lee et al., 2012). 89 Genetic evidence suggests that these signals are mediated via a mitogen-activated 90 protein kinase (MAPK) cascade, which eventually downregulates the transcription 91 factors responsible for initiating stomatal lineage via direct phosphorylation 92 (Bergmann et al., 2004; Lampard et al., 2008; Lampard et al., 2009; Kim et al., 2012). 93 Stomagen (also known as EPF-LIKE9) peptide promotes stomatal development by 94 competing with EPF2 for binding to ER (Sugano et al., 2010; Zhang et al., 2014; 95 Hronkova et al., 2015). One homeodomain-leucine zipper IV (HD-ZIP IV) protein, 96 HOMEODOMAIN GLABROUS2 (HDG2), acts as a key epidermal component 97 promoting stomatal differentiation (Peterson et al., 2013). It is highly expressed in 98 meristemoids, and a hdg2 mutant exhibits delayed meristemoid-to-GM...

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Section: Resultssupporting

confidence: 93%

Global Dynamic Molecular Profiles of Stomatal Lineage Cell Development by Single-Cell RNA Sequencing

Liu

Zhou

Guo

et al. 2020

Preprint

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“…The leaves were incubated in the bath solution (10 mM KCl, 1 mM CaCl 2 and 10 mM MES/BTP, pH 6) and illuminated with 100 µmol m −2 s −1 white light for at least 2 hr before the start of the experiment. Guard cells in the abaxial epidermis of intact leaves were applied with chitosan by using the current ejection technique (Huang et al, 2019), which the tip of a microelectrode was filled with 0.3 mg/mL of chitosan (or 10 mM of MES/BTP, pH6, as control), while the remaining part was filled with 300 mM KCl. The microelectrodes were connected to a custom-made amplifier (Ulliclamp01) via Ag/AgCl half-cells.…”

Section: Methodsmentioning

confidence: 99%

Anion channel SLAH3 is a regulatory target of chitin receptor-associated kinase PBL27 in microbial stomatal closure

Liu

Maierhofer

Rybak

et al. 2019

eLife

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In plants, antimicrobial immune responses involve the cellular release of anions and are responsible for the closure of stomatal pores. Detection of microbe-associated molecular patterns (MAMPs) by pattern recognition receptors (PRRs) induces currents mediated via slow-type (S-type) anion channels by a yet not understood mechanism. Here, we show that stomatal closure to fungal chitin is conferred by the major PRRs for chitin recognition, LYK5 and CERK1, the receptor-like cytoplasmic kinase PBL27, and the SLAH3 anion channel. PBL27 has the capacity to phosphorylate SLAH3, of which S127 and S189 are required to activate SLAH3. Full activation of the channel entails CERK1, depending on PBL27. Importantly, both S127 and S189 residues of SLAH3 are required for chitin-induced stomatal closure and anti-fungal immunity at the whole leaf level. Our results demonstrate a short signal transduction module from MAMP recognition to anion channel activation, and independent of ABA-induced SLAH3 activation.

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“…Recently, AGB1 , which encodes a heterotrimeric G‐protein β‐subunit, was shown to be required for Ca 2+ sensing and calcium‐induced stomatal closure in Arabidopsis (Jeon et al ., 2019). Ca 2+ was also described to increase the efficiency of ABA‐triggered stomatal closure (Huang et al ., 2019), with intracellular Ca 2+ being monitored in this study using a genetically encoded Ca 2+ reporter R‐GECO‐mTurquoise (Waadt et al ., 2017). Using intracellular double‐barreled microelectrodes in intact Arabidopsis leaves, the authors report that Ca 2+ accelerates stomatal closure (Huang et al ., 2019).…”

Section: Roles Of Basal Aba Concentrations In Guard Cells and Basal Amentioning

confidence: 99%

“…Ca 2+ was also described to increase the efficiency of ABA‐triggered stomatal closure (Huang et al ., 2019), with intracellular Ca 2+ being monitored in this study using a genetically encoded Ca 2+ reporter R‐GECO‐mTurquoise (Waadt et al ., 2017). Using intracellular double‐barreled microelectrodes in intact Arabidopsis leaves, the authors report that Ca 2+ accelerates stomatal closure (Huang et al ., 2019). These findings correlate with Boolean modeling predictions (Albert et al ., 2017).…”

Section: Roles Of Basal Aba Concentrations In Guard Cells and Basal Amentioning

confidence: 99%

Signaling mechanisms in abscisic acid‐mediated stomatal closure

et al. 2020

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Summary The plant hormone abscisic acid (ABA) plays a central role in the regulation of stomatal movements under water‐deficit conditions. The identification of ABA receptors and the ABA signaling core consisting of PYR/PYL/RCAR ABA receptors, PP2C protein phosphatases and SnRK2 protein kinases has led to studies that have greatly advanced our knowledge of the molecular mechanisms mediating ABA‐induced stomatal closure in the past decade. This review focuses on recent progress in illuminating the regulatory mechanisms of ABA signal transduction, and the physiological importance of basal ABA signaling in stomatal regulation by CO2 and, as hypothesized here, vapor‐pressure deficit. Furthermore, advances in understanding the interactions of ABA and other stomatal signaling pathways are reviewed here. We also review recent studies investigating the use of ABA signaling mechanisms for the manipulation of stomatal conductance and the enhancement of drought tolerance and water‐use efficiency of plants.

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Calcium signals in guard cells enhance the efficiency by which abscisic acid triggers stomatal closure

Cited by 80 publications

References 76 publications

Global Dynamic Molecular Profiles of Stomatal Lineage Cell Development by Single-Cell RNA Sequencing

Global Dynamic Molecular Profiles of Stomatal Lineage Cell Development by Single-Cell RNA Sequencing

Anion channel SLAH3 is a regulatory target of chitin receptor-associated kinase PBL27 in microbial stomatal closure

Signaling mechanisms in abscisic acid‐mediated stomatal closure

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