Powering the plasma membrane Ca2+-ROS self-amplifying loop

Pottosin, Igor; Zepeda‐Jazo, Isaac

doi:10.1093/jxb/ery179

Cited by 14 publications

(7 citation statements)

References 24 publications

(33 reference statements)

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“…These results reveal that Ca 2+ signaling is essential for melatonin-mediated CBF-responsive pathway and subsequent cold tolerance. [62,67]. Consistent with the previous findings, we found that H 2 O 2 and Ca 2+ interact, forming a reciprocal positive-regulatory loop that mediates melatonin-induced CBF pathway and cold tolerance (Figure 9).…”

Section: Ca 2+ Mediates Melatonin-induced Cbf-responsive Pathway and Cold Tolerancesupporting

confidence: 91%

“…As two crucial signal molecules, the interactions between H 2 O 2 and Ca 2+ signal have been well documented in various physiological actions, especially in defense against abiotic stressors [ 53 , 67 ]. For instance, stress-triggered Ca 2+ signal can phosphorylate and activate RBOHD via Ca 2+ -dependent protein kinase to generate H 2 O 2 , which in turn elicits a Ca 2+ signal through receptor-like kinases, such as GUARD CELL HYDROGEN PEROXIDE RESISTANT1, forming a self-propagating mutual activation loop between Ca 2+ and H 2 O 2 signals [ 62 , 67 ]. Consistent with the previous findings, we found that H 2 O 2 and Ca 2+ interact, forming a reciprocal positive-regulatory loop that mediates melatonin-induced CBF pathway and cold tolerance ( Figure 9 ).…”

Section: Discussionmentioning

confidence: 99%

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Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)

Chang

Guo

et al. 2021

Antioxidants

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Cold stress is a major environmental factor that detrimentally affects plant growth and development. Melatonin has been shown to confer plant tolerance to cold stress through activating the C-REPEAT BINDING FACTOR (CBF) pathway; however, the underlying modes that enable this function remain obscure. In this study, we investigated the role of H2O2 and Ca2+ signaling in the melatonin-induced CBF pathway and cold tolerance in watermelon (Citrullus lanatus L.) through pharmacological, physiological, and genetic approaches. According to the results, melatonin induced H2O2 accumulation, which was associated with the upregulation of respiratory burst oxidase homolog D (ClRBOHD) during the early response to cold stress in watermelon. Besides, melatonin and H2O2 induced the accumulation of cytoplasmic free Ca2+ ([Ca2+]cyt) in response to cold. This was associated with the upregulation of cyclic nucleotide-gated ion channel 2 (ClCNGC2) in watermelon. However, blocking of Ca2+ influx channels abolished melatonin- or H2O2-induced CBF pathway and cold tolerance. Ca2+ also induced ClRBOHD expression and H2O2 accumulation in early response to cold stress in watermelon. Inhibition of H2O2 production in watermelon by RBOH inhibitor or in Arabidopsis by AtRBOHD knockout compromised melatonin-induced [Ca2+]cyt accumulation and melatonin- or Ca2+-induced CBF pathway and cold tolerance. Overall, these findings indicate that melatonin induces RBOHD-dependent H2O2 generation in early response to cold stress. Increased H2O2 promotes [Ca2+]cyt accumulation, which in turn induces H2O2 accumulation via RBOHD, forming a reciprocal positive-regulatory loop that mediates melatonin-induced CBF pathway and subsequent cold tolerance.

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Section: Ca 2+ Mediates Melatonin-induced Cbf-responsive Pathway and Cold Tolerancesupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)

Chang

Guo

et al. 2021

Antioxidants

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“…Recently, the ROS‐Ca 2+ self‐amplifying loop is gaining shape and has been shown to be involved in diverse plant responses (Pottosin & Zepeda‐Jazo, ). The knockout of AtGLRs like GLR3.1/3.5 or GLR3.3 leads to fewer transcripts of Ca 2+ sensing proteins and abolishes the stimuli‐induced changes in intracellular Ca 2+ concentration (Kong et al, ; Wudick et al, ).…”

Section: Discussionmentioning

confidence: 99%

Tomato GLR3.3 and GLR3.5 mediate cold acclimation‐induced chilling tolerance by regulating apoplastic H₂O₂ production and redox homeostasis

Jiang

et al. 2019

Plant Cell & Environment

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Plant glutamate receptor-like (GLR) genes play important roles in plant development and immune response. However, the functions of GLRs in abiotic stress response remain unclear. Here we show that cold acclimation at 12°C induced the transcripts of GLR3.3 and GLR3.5 with increased tolerance against a subsequent chilling at 4°C. Silencing of GLR3.3 or/and GLR3.5 or application of the antagonist of ionotropic glutamate receptor 6,7-dinitroquinoxaline-2,3-dione (DNQX), all compromised the acclimation-induced increases in the transcripts of respiratory burst oxidase homolog1 (RBOH1), activity of NADPH oxidase, the accumulation of apoplastic H 2 O 2 and the ratio of reduced glutathione (GSH) to oxidized glutathione (GSSG), resulting in an attenuated chilling tolerance; the effect, however, was rescued by foliar application of H 2 O 2 or GSH. Both RBOH1-silenced and glutathione biosynthesis genes, γglutamylcysteine synthetase (GSH1)-and glutathione synthetase (GSH2)-cosilenced plants had decreased chilling tolerance with reduced GSH/GSSG ratio. Moreover, application of DNQX had little effects on the GSH/GSSG ratio and the tolerance in RBOH1-silenced plants and GSH1-and GSH2-cosilenced plants. These findings unmasked the functional hierarchy of GLR-H 2 O 2 -glutathione cascade and shed new light on cold response pathway in tomato plants.

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“…The source depends on the relative expression of amine oxidases: mainly DAO in dicots and mainly PAO in monocots ( Moschou et al, 2008 ). Transmission of the external ROS signal to internal signaling is mediated by ROS-activated Ca 2+ influx, positively fed back to ROS production due to a Ca 2+ activation of the PM-bound NADPH-dehydrogenase ( Takeda et al, 2008 ; Demidchik et al, 2018 ; Pottosin and Zepeda-Jazo, 2018 ). In pea roots, OH • at lower and higher levels, respectively, induced a transient Ca 2+ pumping by Ca 2+ -ATPase and a sustained Ca 2+ influx via ROSIC ( Zepeda-Jazo et al, 2011 ).…”

Section: Effects Of Polyamine Catabolites: Ros and Gabamentioning

confidence: 99%

Modulation of Ion Transport Across Plant Membranes by Polyamines: Understanding Specific Modes of Action Under Stress

et al. 2021

Self Cite

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This work critically discusses the direct and indirect effects of natural polyamines and their catabolites such as reactive oxygen species and γ-aminobutyric acid on the activity of key plant ion-transporting proteins such as plasma membrane H+ and Ca2+ ATPases and K+-selective and cation channels in the plasma membrane and tonoplast, in the context of their involvement in stress responses. Docking analysis predicts a distinct binding for putrescine and longer polyamines within the pore of the vacuolar TPC1/SV channel, one of the key determinants of the cell ionic homeostasis and signaling under stress conditions, and an additional site for spermine, which overlaps with the cytosolic regulatory Ca2+-binding site. Several unresolved problems are summarized, including the correct estimates of the subcellular levels of polyamines and their catabolites, their unexplored effects on nucleotide-gated and glutamate receptor channels of cell membranes and Ca2+-permeable and K+-selective channels in the membranes of plant mitochondria and chloroplasts, and pleiotropic mechanisms of polyamines’ action on H+ and Ca2+ pumps.

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Powering the plasma membrane Ca2+-ROS self-amplifying loop

Abstract: This article comments on:Makavitskaya M, Svistunenko D, Navaselsky I, et al. 2018. .

Cited by 14 publications

References 24 publications

Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)

Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)

Tomato GLR3.3 and GLR3.5 mediate cold acclimation‐induced chilling tolerance by regulating apoplastic H₂O₂ production and redox homeostasis

Modulation of Ion Transport Across Plant Membranes by Polyamines: Understanding Specific Modes of Action Under Stress

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Powering the plasma membrane Ca2+-ROS self-amplifying loop

Abstract: This article comments on:Makavitskaya M, Svistunenko D, Navaselsky I, et al. 2018. .

Cited by 14 publications

References 24 publications

Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)

Positive Interaction between H2O2 and Ca2+ Mediates Melatonin-Induced CBF Pathway and Cold Tolerance in Watermelon (Citrullus lanatus L.)

Tomato GLR3.3 and GLR3.5 mediate cold acclimation‐induced chilling tolerance by regulating apoplastic H2O2 production and redox homeostasis

Modulation of Ion Transport Across Plant Membranes by Polyamines: Understanding Specific Modes of Action Under Stress

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Product

Resources

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Tomato GLR3.3 and GLR3.5 mediate cold acclimation‐induced chilling tolerance by regulating apoplastic H₂O₂ production and redox homeostasis