Loss of nitrate reductases NIA1 and NIA2 impairs stomatal closure by altering genes of core ABA signaling components in Arabidopsis

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.

Download Full-text

Functional characterization and reconstitution of ABA signaling components using transient gene expression in rice protoplasts

Frontiers in Plant Science ◽

10.3389/fpls.2015.00614 ◽

2015 ◽

Vol 6 ◽

Cited By ~ 20

Author(s):

Namhyo Kim ◽

Seok-Jun Moon ◽

Myung K. Min ◽

Eun-Hye Choi ◽

Jin-Ae Kim ◽

...

Keyword(s):

Gene Expression ◽

Functional Characterization ◽

Transient Gene Expression ◽

Aba Signaling ◽

Signaling Components

Download Full-text

Protease Inhibitor-Dependent Inhibition of Light-Induced Stomatal Opening

Frontiers in Plant Science ◽

10.3389/fpls.2021.735328 ◽

2021 ◽

Vol 12 ◽

Author(s):

Tenghua Wang ◽

Wenxiu Ye ◽

Yin Wang ◽

Maoxing Zhang ◽

Yusuke Aihara ◽

...

Keyword(s):

Matrix Metalloproteinase ◽

Protease Inhibitor ◽

Signaling Pathway ◽

Stomatal Closure ◽

Screening Method ◽

Stomatal Opening ◽

Matrix Metalloproteinase 2 ◽

Aba Signaling ◽

Bioinformatics Analyses ◽

Chemical Screening

Stomata in the epidermis of plants play essential roles in the regulation of photosynthesis and transpiration. Stomata open in response to blue light (BL) by phosphorylation-dependent activation of the plasma membrane (PM) H+-ATPase in guard cells. Under water stress, the plant hormone abscisic acid (ABA) promotes stomatal closure via the ABA-signaling pathway to reduce water loss. We established a chemical screening method to identify compounds that affect stomatal movements in Commelina benghalensis. We performed chemical screening using a protease inhibitor (PI) library of 130 inhibitors to identify inhibitors of stomatal movement. We discovered 17 PIs that inhibited light-induced stomatal opening by more than 50%. Further analysis of the top three inhibitors (PI1, PI2, and PI3; inhibitors of ubiquitin-specific protease 1, membrane type-1 matrix metalloproteinase, and matrix metalloproteinase-2, respectively) revealed that these inhibitors suppressed BL-induced phosphorylation of the PM H+-ATPase but had no effect on the activity of phototropins or ABA-dependent responses. The results suggest that these PIs suppress BL-induced stomatal opening at least in part by inhibiting PM H+-ATPase activity but not the ABA-signaling pathway. The targets of PI1, PI2, and PI3 were predicted by bioinformatics analyses, which provided insight into factors involved in BL-induced stomatal opening.

Download Full-text

The fungal sesquiterpenoid pyrenophoric acid B uses the plant ABA biosynthetic pathway to inhibit seed germination

Journal of Experimental Botany ◽

10.1093/jxb/erz306 ◽

2019 ◽

Vol 70 (19) ◽

pp. 5487-5494 ◽

Cited By ~ 1

Author(s):

Jorge Lozano-Juste ◽

Marco Masi ◽

Alessio Cimmino ◽

Suzette Clement ◽

Maria A Fernández ◽

...

Keyword(s):

Seed Germination ◽

Seedling Establishment ◽

Biosynthetic Pathway ◽

Aba Signaling ◽

Wild Type ◽

Invasive Weed ◽

Seed Mortality ◽

Signaling Components ◽

Aba Biosynthesis ◽

Aba Receptors

Abstract Pyrenophoric acid (P-Acid), P-Acid B, and P-Acid C are three phytotoxic sesquiterpenoids produced by the ascomycete seed pathogen Pyrenophora semeniperda, a fungus proposed as a mycoherbicide for biocontrol of cheatgrass, an extremely invasive weed. When tested in cheatgrass bioassays, these metabolites were able to delay seed germination, with P-Acid B being the most active compound. Here, we have investigated the cross-kingdom activity of P-Acid B and its mode of action, and found that it activates the abscisic acid (ABA) signaling pathway in order to inhibit seedling establishment. P-Acid B inhibits seedling establishment in wild-type Arabidopsis thaliana, while several mutants affected in the early perception as well as in downstream ABA signaling components were insensitive to the fungal compound. However, in spite of structural similarities between ABA and P-Acid B, the latter is not able to activate the PYR/PYL family of ABA receptors. Instead, we have found that P-Acid B uses the ABA biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to reduce seedling establishment. We propose that the fungus P. semeniperda manipulates plant ABA biosynthesis as a strategy to reduce seed germination, increasing its ability to cause seed mortality and thereby increase its fitness through higher reproductive success.

Download Full-text

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].

Download Full-text

ABA signaling components in Phelipanche aegyptiaca

Scientific Reports ◽

10.1038/s41598-019-42976-3 ◽

2019 ◽

Vol 9 (1) ◽

Author(s):

Gil Wiseglass ◽

Oded Pri-Tal ◽

Assaf Mosquna

Keyword(s):

Aba Signaling ◽

Signaling Components

Download Full-text

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.

Download Full-text

A repressor complex silencing ABA signaling in seeds?

Journal of Experimental Botany ◽

10.1093/jxb/eraa062 ◽

2020 ◽

Vol 71 (10) ◽

pp. 2847-2853 ◽

Cited By ~ 1

Author(s):

Hiroyuki Nonogaki

Keyword(s):

Seed Germination ◽

Seed Dormancy ◽

Transcriptional Repression ◽

Target Genes ◽

Aba Signaling ◽

Molecular Events ◽

Aba Sensitivity ◽

Repressor Complex ◽

Transcription Factor Target ◽

Signaling Components

Abstract Seed dormancy is induced primarily by abscisic acid (ABA) and maintained through elevated levels of ABA sensitivity in seeds. The core mechanisms of ABA-imposed seed dormancy are emerging, but it is still unclear how these blockages in seeds are eliminated during after-ripening, or what molecular events in imbibed seeds are responsible for the initial stages of germination induction. Some pieces of evidence suggest that a repressor complex, which potentially triggers seed germination through the suppression of ABA signaling components, might be present in seeds. The usual suspect, protein phosphatase 2C, which inactivates kinases and shuts down ABA signaling in the major dormancy pathway, is possibly associated with this complex. Other members, such as WD40 proteins and histone deacetylase subunits, homologs of which are found in the flowering repressor complex, perhaps constitute this complex in seeds. The repressor activity could counteract the dormancy mechanisms in an overwhelming manner, through well-coordinated inactivation and turnover of germination-suppressing transcription factors, which is probably accompanied by chromatin silencing and transcriptional repression of the transcription factor target genes. This review provides a perspective on a putative seed germination-inducing repressor complex, including its possible modes of action and upstream regulators.

Download Full-text

Evolutionary Conservation of ABA Signaling for Stomatal Closure

PLANT PHYSIOLOGY ◽

10.1104/pp.16.01848 ◽

2017 ◽

Vol 174 (2) ◽

pp. 732-747 ◽

Cited By ~ 55

Author(s):

Shengguan Cai ◽

Guang Chen ◽

Yuanyuan Wang ◽

Yuqing Huang ◽

D. Blaine Marchant ◽

...

Keyword(s):

Stomatal Closure ◽

Evolutionary Conservation ◽

Aba Signaling

Download Full-text

RPK1 and BAK1 sequentially form complexes with OST1 to regulate ABA-induced stomatal closure

Journal of Experimental Botany ◽

10.1093/jxb/erz489 ◽

2019 ◽

Author(s):

Yun Shang ◽

Dami Yang ◽

Yunmi Ha ◽

Hyun-young Shin ◽

Kyoung Hee Nam

Keyword(s):

Water Status ◽

Stomatal Closure ◽

Expression Patterns ◽

Cell Movement ◽

Guard Cells ◽

Aba Signaling ◽

Signaling Systems ◽

Underlying Mechanisms

Abstract Regulation of plant water status occurs via abscisic acid (ABA)-induced stomatal closure. Open Stomata 1 (OST1) is a critical ABA signaling component regulating this process in guard cells. We previously reported that BRI1-associated receptor kinase 1 (BAK1) positively regulates ABA-induced stomatal closure by interacting with, and phosphorylating OST1. Here, we show that the Receptor-like Protein Kinase 1 (RPK1), previously known to be induced by ABA, is a positive ABA-signaling component in guard cell movement, and interacts with OST1. ABA-inducible expression patterns were observed in RPK1 and OST1, but not in BAK1. We investigated the underlying mechanisms by which the RPK1/OST1 and BAK1/OST1 complexes interact in stomatal guard cells by monitoring the complex formation continuously using FRET analyses. We found that the BAK1/OST1 complex was formed earlier than the RPK1/OST1 complex in response to ABA. In vitro and semi-in vivo kinase assays revealed that a trans-phosphorylation event occurred in the RPK1/OST1 complex, which differs from that in the BAK1/OST1 complex, wherein only OST1 phosphorylation occurred via BAK1. ABA Insensitive 1 (ABI1) only dephosphorylated OST1 in the BAK1/OST1 complex, but dephosphorylated both RPK1 and OST1 proteins in the RPK1/OST1 complex. Our results suggest that there are multiple coordinated ABA signaling systems to regulate stomatal movement.

Download Full-text