Nitrated Cyclic GMP Modulates Guard Cell Signaling in<i>Arabidopsis</i>

Joudoi, Takahiro; Shichiri, Yudai; Kamizono, Nobuto; Akaike, Takaaki; Sawa, Tomohiro; Yoshitake, Jun; Yamada, Naotaka; Iwai, Sumio

doi:10.1105/tpc.112.105049

Cited by 133 publications

(118 citation statements)

References 65 publications

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“…However, MYB44 also negatively regulates ABA responses (Jaradat et al, 2013;Li et al, 2014) involved in stomatal closure, leaf senescence, and ROS scavenging (Persak and Pitzschke, 2014). In our study, MYB44 expression correlated positively with glycerol levels and negatively with the expression of NOGC1, a nitric oxide-dependent guanylyl cyclase involved in stomatal closure via Ca 2+ signaling (Mulaudzi et al, 2011;Joudoi et al, 2013). In addition, MYB44 correlated positively (r = 0.85, P = 0.001) with the chloroplastic lipid transfer protein LTPc1 (At2g10940), which together with LTPc2 (At2g45180) was up-regulated during O 3 stress but not herbivore stress (Supplemental Figs.…”

Section: Effects Of O 3 Stress On Photosynthesis and Stomatal Regulationmentioning

confidence: 53%

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

et al. 2016

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Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O 3 ), a global anthropogenic pollutant, directly affects living organisms and ecosystems, including plant-herbivore interactions. In this study, we investigate the stress responses of Brassica nigra (wild black mustard) exposed consecutively to O 3 and the specialist herbivore Pieris brassicae. Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O 3 and herbivory responses. O 3 stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O 3 to herbivory induced characteristic plant defense responses, including a decrease in central metabolism, induction of the jasmonic acid/ethylene pathways, and emission of volatiles. Omics network and pathway analyses predicted a link between glycerol and central energy metabolism that influences the osmotic stress response and stomatal closure. Further physiological measurements confirmed that while O 3 stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O 3 , resulting in a phenotype similar to that observed after herbivory alone. This study clarifies the consequences of multiple stress interactions on a plant metabolic system and also illustrates how omics data can be integrated to generate new hypotheses in ecology and plant physiology.

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Section: Effects Of O 3 Stress On Photosynthesis and Stomatal Regulationmentioning

confidence: 53%

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

et al. 2016

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“…3) (21). On the other hand, several studies have found a positive role of exogenous application of NO in ABA-induced stomatal closure (15,20,22,24). Exogenous NO might promote stomatal closure by regulating ion channels (20,23), or by generating nitrated cGMP (24).…”

Section: Discussionmentioning

confidence: 99%

“…Exogenous NO might promote stomatal closure by regulating ion channels (20,23), or by generating nitrated cGMP (24). Alternatively, the observed positive role of exogenous NO on ABA responses in guard cells might be caused by secondary effects, such as induction of ROS or other second messengers (24,47).…”

Section: Discussionmentioning

confidence: 99%

“…Exogenous application of NO can trigger stomatal closure, whereas application of the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (c-PTIO) inhibits stomatal closure (22), suggesting a positive role of exogenous NO in stomatal closure. Several studies have suggested that exogenous NO may affect stomatal responses to ABA by regulating an inward K + channel (20), an anion channel (23), and the generation of nitrated cGMP (24), although the direct target of NO in ABA signaling remains unclear.…”

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confidence: 99%

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Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1

Wang¹,

Hou³

et al. 2014

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

315

212

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The phytohormone abscisic acid (ABA) plays important roles in plant development and adaptation to environmental stress. ABA induces the production of nitric oxide (NO) in guard cells, but how NO regulates ABA signaling is not understood. Here, we show that NO negatively regulates ABA signaling in guard cells by inhibiting open stomata 1 (OST1)/sucrose nonfermenting 1 (SNF1)-related protein kinase 2.6 (SnRK2.6) through S-nitrosylation. We found that SnRK2.6 is S-nitrosylated at cysteine 137, a residue adjacent to the kinase catalytic site. Dysfunction in the S-nitrosoglutathione (GSNO) reductase (GSNOR) gene in the gsnor1-3 mutant causes NO overaccumulation in guard cells, constitutive S-nitrosylation of SnRK2.6, and impairment of ABA-induced stomatal closure. Introduction of the Cys137 to Ser mutated SnRK2.6 into the gsnor1-3/ ost1-3 double-mutant partially suppressed the effect of gsnor1-3 on ABA-induced stomatal closure. A cysteine residue corresponding to Cys137 of SnRK2.6 is present in several yeast and human protein kinases and can be S-nitrosylated, suggesting that the S-nitrosylation may be an evolutionarily conserved mechanism for protein kinase regulation.A bscisic acid (ABA) plays critical roles in seed dormancy and germination, plant growth, and adaptation to environmental challenges (1, 2). Stresses, such as drought and high salt conditions, increase ABA concentration in plants as a result of ABA biosynthesis or ABA release from its inactive, conjugated forms (3). In the presence of ABA, the ABA receptors in the PYR1 (Pyrabactin Resistance 1)/PYL (PYR1-Like)/RCAR (Regulatory Component of ABA receptor) protein family bind to and inhibit the activity of clade A protein phosphatase 2Cs (PP2Cs), which are considered as coreceptors and negative regulators of ABA signaling (4-6). This process then results in the release of sucrose nonfermenting 1 (SNF1)-related protein kinase 2s (SnRK2s) from suppression by the PP2Cs. As central components of the ABA signaling pathway, the activated SnRK2s phosphorylate dozens of downstream effectors to regulate various physiological processes, including stomatal closure, root growth and development, seed dormancy, seed germination, and flowering (7).As the gateway for photosynthetic CO 2 uptake and transpirational water loss, stomata are critical for plant growth and physiology (8). ABA regulates stomatal movement and mutations in ABA biosynthesis genes (9), or in the PYL or SnRK2.6 (also known as OST1) genes cause open-stomata phenotypes (10). On the other hand, dysfunction of the PP2Cs or overexpression of RCAR1/PYL9 causes stomatal closure (5). Among the three SnRK2s, SnRK2.2, -2.3, and -2.6, which are most important for ABA signaling, SnRK2.6 is preferentially expressed in guard cells and plays a critical role in stomatal regulation, whereas SnRK2.2 and -2.3 are mainly expressed in seeds and young seedlings and are thus more important for seed germination and seedling growth (4, 11). SnRK2.6 phosphorylates the slow (S-type) anion channel associated 1 and inward potass...

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“…4,5) We discovered endogenous formation of the nitrated cGMP derivative 8-nitroguanosine 3′,5′-cyclic monophosphate (8-nitro-cGMP) under conditions associated with excess production of both nitric oxide (NO) and reactive oxygen species in mammalian cells [7][8][9][10][11][12][13][14][15][16][17] as well as in plants. 18,19) Biochemical analyses revealed that 8-nitro-cGMP can activate PKG1α to a similar extent as native cGMP can. 9,12) Although native cGMP is degraded by phosphodiesterase to form guanosine 5′-mono-phosphate, 8-nitro-cGMP was resistant to phosphodiesterasemediated degradation.…”

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confidence: 99%

Synthesis and Characterization of 8-Nitroguanosine 3′,5′-Cyclic Monophosphorothioate Rp-Isomer as a Potent Inhibitor of Protein Kinase G1α

Ahmed

Zhang

Ono

et al. 2017

Biological & Pharmaceutical Bulletin

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Guanosine 3′,5′-cyclic monophosphate (cGMP)-dependent protein kinases (PKG) are kinases regulating diverse physiological functions including vascular smooth muscle relaxation, neuronal synaptic plasticity, and platelet activities. Certain PKG inhibitors, such as Rp-diastereomers of derivatives of guanosine 3′,5′-cyclic monophosphorothioate (Rp-cGMPS), have been designed and used to study PKG-regulated cell signaling. 8-Nitroguanosine 3′,5′-cyclic monophosphate (8-nitro-cGMP) is an endogenous cGMP derivative formed as a result of excess production of reactive oxygen species and nitric oxide. 8-Nitro-cGMP causes persistent activation of PKG1α through covalent attachment of cGMP moieties to cysteine residues of the enzyme (i.e., the process called protein S-guanylation). In this study, we synthesized a nitrated analogue of Rp-cGMPS, 8-nitroguanosine 3′,5′-cyclic monophosphorothioate Rp-isomer (Rp-8-nitro-cGMPS), and investigated its effects on PKG1α activity. We synthesized Rp-8-nitro-cGMPS by reacting Rp-8-bromoguanosine 3′,5′-cyclic monophosphorothioate (Rp-8-bromo-cGMPS) with sodium nitrite. Rp-8-Nitro-cGMPS reacted with the thiol compounds cysteine and glutathione to form Rp-8-thioalkoxy-cGMPS adducts to a similar extent as did 8-nitro-cGMP. As an important finding, a protein S-guanylation-like modification was clearly observed, by using Western blotting, in the reaction between recombinant PKG1α and Rp-8-nitro-cGMPS. Rp-8-Nitro-cGMPS inhibited PKG1α activity with an inhibitory constant of 22 µM in a competitive manner. An organ bath assay with mouse aorta demonstrated that Rp-8-nitro-cGMPS inhibited vascular relaxation induced by acetylcholine or 8-bromo-cGMP more than Rp-8-bromo-cGMPS did. These findings suggest that Rp-8-nitro-cGMPS inhibits PKG through induction of an S-guanylation-like modification by attaching the Rp-cGMPS moiety to the enzyme. Additional study is warranted to explore the potential application of Rp-8-nitro-cGMPS to biochemical and therapeutic research involving PKG1α activation.

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Nitrated Cyclic GMP Modulates Guard Cell Signaling inArabidopsis

Cited by 133 publications

References 65 publications

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1

Synthesis and Characterization of 8-Nitroguanosine 3′,5′-Cyclic Monophosphorothioate Rp-Isomer as a Potent Inhibitor of Protein Kinase G1α

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