The tomato DELLA protein PROCERA promotes ABA responses in guard cells by upregulating ABA transporter

AbstractPlants reduce transpiration to avoid drought stress by stomatal closure. While abscisic acid (ABA) has a central role in the regulation of stomatal closure under water-deficit conditions, we demonstrated in tomato that the gibberellin (GA) response inhibitor, the DELLA protein PROCERA (PRO), promotes ABA-induced stomatal closure and gene transcription in guard cells. To study how PRO affects stomatal closure, we performed RNAseq analysis of isolated guard cells and identified the ABA transporters ABA-IMPORTING TRANSPORTER1.1 (AIT1.1) and AIT1.2, also called in Arabidopsis NPF4.6, as upregulated by PRO. Tomato has four AIT1 genes, but only AIT1.1 and AIT1.2 were upregulated by PRO, and only AIT1.1 exhibited high expression in guard cells. Functional analysis of AIT1.1 in yeast confirmed its activity as an ABA transporter, possibly importer. CRISPR-Cas9-defrived ait1.1 mutant exhibited increased transpiration, larger stomatal aperture and reduced response to ABA. Moreover, ait1.1 suppressed the promoting effects of PRO on ABA-induced stomatal closure and gene expression in guard cells. The negative interaction between GA and ABA has been studied for many years in numerous plant species. These studies suggest that the crosstalk is mediated by changes in hormone biosynthesis and signaling. Our results suggest that it is also mediated by changes in hormone transport.One-sentence SummaryThe tomato DELLA protein PROCERA promoted abscisic acid-induced stomatal closure and gene expression by upregulating the expression of the ABA transporter ABA-IMPORTING TRANSPORTER 1 in guard cells.

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Arabidopsis NPF4.6 and NPF5.1 Control Leaf Stomatal Aperture by Regulating Abscisic Acid Transport

Genes ◽

10.3390/genes12060885 ◽

2021 ◽

Vol 12 (6) ◽

pp. 885

Author(s):

Takafumi Shimizu ◽

Yuri Kanno ◽

Hiromi Suzuki ◽

Shunsuke Watanabe ◽

Mitsunori Seo

Keyword(s):

Abscisic Acid ◽

Plant Hormone ◽

Leaf Surface ◽

Stomatal Closure ◽

Guard Cells ◽

Cell Types ◽

Acid Transport ◽

Wild Type ◽

Vascular Tissues ◽

Abscisic Acid Transport

The plant hormone abscisic acid (ABA) is actively synthesized in vascular tissues and transported to guard cells to promote stomatal closure. Although several transmembrane ABA transporters have been identified, how the movement of ABA within plants is regulated is not fully understood. In this study, we determined that Arabidopsis NPF4.6, previously identified as an ABA transporter expressed in vascular tissues, is also present in guard cells and positively regulates stomatal closure in leaves. We also found that mutants defective in NPF5.1 had a higher leaf surface temperature compared to the wild type. Additionally, NPF5.1 mediated cellular ABA uptake when expressed in a heterologous yeast system. Promoter activities of NPF5.1 were detected in several leaf cell types. Taken together, these observations indicate that NPF5.1 negatively regulates stomatal closure by regulating the amount of ABA that can be transported from vascular tissues to guard cells.

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Ethylene inhibits abscisic acid-induced stomatal closure inVicia fabavia reducing nitric oxide levels in guard cells

New Zealand Journal of Botany ◽

10.1080/0028825x.2012.661064 ◽

2012 ◽

Vol 50 (2) ◽

pp. 203-216 ◽

Cited By ~ 6

Author(s):

XiaoPing She ◽

XiGui Song

Keyword(s):

Nitric Oxide ◽

Abscisic Acid ◽

Stomatal Closure ◽

Guard Cells

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The Tomato DELLA Protein PROCERA Acts in Guard Cells to Promote Stomatal Closure

The Plant Cell ◽

10.1105/tpc.17.00542 ◽

2017 ◽

Vol 29 (12) ◽

pp. 3186-3197 ◽

Cited By ~ 21

Author(s):

Ido Nir ◽

Hagai Shohat ◽

Irina Panizel ◽

Neil Olszewski ◽

Asaph Aharoni ◽

...

Keyword(s):

Stomatal Closure ◽

Guard Cells ◽

Della Protein

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Abscisic acid-independent stomatal CO2 signal transduction pathway and convergence of CO2 and ABA signaling downstream of OST1 kinase

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1809204115 ◽

2018 ◽

Vol 115 (42) ◽

pp. E9971-E9980 ◽

Cited By ~ 28

Author(s):

Po-Kai Hsu ◽

Yohei Takahashi ◽

Shintaro Munemasa ◽

Ebe Merilo ◽

Kristiina Laanemets ◽

...

Keyword(s):

Signal Transduction ◽

Abscisic Acid ◽

Protein Kinase ◽

Stomatal Closure ◽

Signal Transduction Pathway ◽

Guard Cells ◽

Aba Signaling ◽

Time Resolved ◽

Aba Receptor ◽

Biochemical Analyses

Stomatal pore apertures are narrowing globally due to the continuing rise in atmospheric [CO2]. CO2 elevation and the plant hormone abscisic acid (ABA) both induce rapid stomatal closure. However, the underlying signal transduction mechanisms for CO2/ABA interaction remain unclear. Two models have been considered: (i) CO2 elevation enhances ABA concentrations and/or early ABA signaling in guard cells to induce stomatal closure and (ii) CO2 signaling merges with ABA at OST1/SnRK2.6 protein kinase activation. Here we use genetics, ABA-reporter imaging, stomatal conductance, patch clamp, and biochemical analyses to investigate these models. The strong ABA biosynthesis mutants nced3/nced5 and aba2-1 remain responsive to CO2 elevation. Rapid CO2-triggered stomatal closure in PYR/RCAR ABA receptor quadruple and hextuple mutants is not disrupted but delayed. Time-resolved ABA concentration monitoring in guard cells using a FRET-based ABA-reporter, ABAleon2.15, and ABA reporter gene assays suggest that CO2 elevation does not trigger [ABA] increases in guard cells, in contrast to control ABA exposures. Moreover, CO2 activates guard cell S-type anion channels in nced3/nced5 and ABA receptor hextuple mutants. Unexpectedly, in-gel protein kinase assays show that unlike ABA, elevated CO2 does not activate OST1/SnRK2 kinases in guard cells. The present study points to a model in which rapid CO2 signal transduction leading to stomatal closure occurs via an ABA-independent pathway downstream of OST1/SnRK2.6. Basal ABA signaling and OST1/SnRK2 activity are required to facilitate the stomatal response to elevated CO2. These findings provide insights into the interaction between CO2/ABA signal transduction in light of the continuing rise in atmospheric [CO2].

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Transcriptional Regulation of Protein Phosphatase 2C Genes to Modulate Abscisic Acid Signaling

International Journal of Molecular Sciences ◽

10.3390/ijms21249517 ◽

2020 ◽

Vol 21 (24) ◽

pp. 9517

Author(s):

Choonkyun Jung ◽

Nguyen Hoai Nguyen ◽

Jong-Joo Cheong

Keyword(s):

Abscisic Acid ◽

Osmotic Stress ◽

Gene Transcription ◽

Stomatal Closure ◽

Guard Cells ◽

Stress Conditions ◽

Physical Interaction ◽

Aba Signaling ◽

Negative Feedback Regulation ◽

Pp2c Gene

The plant hormone abscisic acid (ABA) triggers cellular tolerance responses to osmotic stress caused by drought and salinity. ABA controls the turgor pressure of guard cells in the plant epidermis, leading to stomatal closure to minimize water loss. However, stomatal apertures open to uptake CO2 for photosynthesis even under stress conditions. ABA modulates its signaling pathway via negative feedback regulation to maintain plant homeostasis. In the nuclei of guard cells, the clade A type 2C protein phosphatases (PP2Cs) counteract SnRK2 kinases by physical interaction, and thereby inhibit activation of the transcription factors that mediate ABA-responsive gene expression. Under osmotic stress conditions, PP2Cs bind to soluble ABA receptors to capture ABA and release active SnRK2s. Thus, PP2Cs function as a switch at the center of the ABA signaling network. ABA induces the expression of genes encoding repressors or activators of PP2C gene transcription. These regulators mediate the conversion of PP2C chromatins from a repressive to an active state for gene transcription. The stress-induced chromatin remodeling states of ABA-responsive genes could be memorized and transmitted to plant progeny; i.e., transgenerational epigenetic inheritance. This review focuses on the mechanism by which PP2C gene transcription modulates ABA signaling.

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A chloroplast retrograde signal, 3’-phosphoadenosine 5’-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

eLife ◽

10.7554/elife.23361 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 60

Author(s):

Wannarat Pornsiriwong ◽

Gonzalo M Estavillo ◽

Kai Xun Chan ◽

Estee E Tee ◽

Diep Ganguly ◽

...

Keyword(s):

Gene Expression ◽

Abscisic Acid ◽

Seed Germination ◽

Alternative Pathway ◽

Stomatal Closure ◽

Anion Channel ◽

Aba Signaling ◽

Calcium Dependent ◽

Secondary Messenger ◽

Signaling Components

Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3′-phosphoadenosine 5′- phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost1-2. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to fine-tune physiological responses.

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