Effects of anion channel blockers NPPB and DIDS on tobacco pollen tube growth and its mitochondria state

Breygina, Maria; Smirnova, A. V.; Maslennikov, M. V.; Матвеева, Н. П.; Yermakov, I. P.

doi:10.1134/s1990519x10030119

Cited by 7 publications

(4 citation statements)

References 26 publications

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“…On the one hand, uptake of anions into the PTs serves the fast osmotically driven growth process; on the other hand, tip efflux of anions strongly correlates with PT growth rate (Zonia et al, 2001(Zonia et al, , 2002Gutermuth et al, 2013). Leakage of anions from pollen grains is essential to initiate pollen germination, while tube growth is inhibited when anion fluxes are disrupted pharmacologically (Zonia et al, 2002;Breygina et al, 2009Breygina et al, , 2010Breygina et al, , 2012Gutermuth et al, 2013). Apical anion fluxes are two to three orders of magnitude greater than the ones for Ca 2+ and H + , suggesting that they likely play an important physiological role in PT growth control as well (Holdaway-Clarke et al, 1997;Certal et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Tip‐localized Ca²⁺‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Gutermuth¹,

Herbell²,

Lassig

et al. 2018

New Phytologist

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Pollen tubes (PTs) are characterized by having tip-focused cytosolic calcium ion (Ca ) concentration ([Ca ] ) gradients, which are believed to control PT growth. However, the mechanisms by which the apical [Ca ] orchestrates PT growth are not well understood. Here, we aimed to identify these mechanisms by combining reverse genetics, cell biology, electrophysiology, and live-cell Ca and anion imaging. We triggered Ca -channel activation by applying hyperpolarizing voltage pulses and observed that the evoked [Ca ] increases were paralleled by high anion channel activity and a decrease in the cytosolic anion concentration at the PT tip. We confirmed a functional correlation between these patterns by showing that inhibition of Ca -permeable channels eliminated the [Ca ] increase, resulting in the abrogation of anion channel activity via Ca -dependent protein kinases (CPKs). Functional characterization of CPK and anion-channel mutants revealed a CPK2/20/6-dependent activation of SLAH3 and ALMT12/13/14 anion channels. The impaired growth phenotypes of anion channel and CPK mutants support the physiological significance of a kinase- and Ca -dependent pathway to control PT growth via anion channel activation. Other than unveiling this functional link, our membrane hyperpolarization method allows for unprecedented manipulation of the [Ca ] gradient or oscillations in the PT tips and opens an array of opportunities for channel screenings.

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Section: Introductionmentioning

confidence: 99%

Tip‐localized Ca²⁺‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Gutermuth¹,

Herbell²,

Lassig

et al. 2018

New Phytologist

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“…Inhibition of anion fluxes in pollen tubes or grains via inhibitors results in growth arrest or retains pollen germination, respectively; furthermore, pharmacological and osmotic manipulations suggest that anion effluxes have a crucial role in water homeostasis (Zonia et al, 2002;Breygina et al, 2010). Patch-clamp studies revealed three different anion channel conductances in pollen grains and tube protoplasts (Tavares et al, 2011a).…”

Section: Introductionmentioning

confidence: 99%

Pollen Tube Growth Regulation by Free Anions Depends on the Interaction between the Anion Channel SLAH3 and Calcium-Dependent Protein Kinases CPK2 and CPK20

Gutermuth¹,

et al. 2013

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(J.A.F.).Apical growth in pollen tubes (PTs) is associated with the presence of tip-focused ion gradients and fluxes, implying polar localization or regulation of the underlying transporters. The molecular identity and regulation of anion transporters in PTs is unknown. Here we report a negative gradient of cytosolic anion concentration focused on the tip, in negative correlation with the cytosolic Ca 2+ concentration. We hypothesized that a possible link between these two ions is based on the presence of Ca 2+ -dependent protein kinases (CPKs). We characterized anion channels and CPK transcripts in PTs and analyzed their localization. Yellow fluorescent protein (YFP) tagging of a homolog of SLOW ANION CHANNEL-ASSOCIATED1 (SLAH3:YFP) was widespread along PTs, but, in accordance with the anion efflux, CPK2/CPK20/CPK17/CPK34:YFP fluorescence was strictly localized at the tip plasma membrane. Expression of SLAH3 with either CPK2 or CPK20 (but not CPK17/CPK34) in Xenopus laevis oocytes elicited S-type anion channel currents. Interaction of SLAH3 with CPK2/CPK20 (but not CPK17/CPK34) was confirmed by Förster-resonance energy transfer fluorescence lifetime microscopy in Arabidopsis thaliana mesophyll protoplasts and bimolecular fluorescence complementation in living PTs. Compared with wild-type PTs, slah3-1 and slah3-2 as well as cpk2-1 cpk20-2 PTs had reduced anion currents. Double mutant cpk2-1 cpk20-2 and slah3-1 PTs had reduced extracellular anion fluxes at the tip. Our studies provide evidence for a Ca 2+ -dependent CPK2/CPK20 regulation of the anion channel SLAH3 to regulate PT growth.

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“…Plant roots discharge hydrogen ions and organic ligands through ion channels, which are then adsorbed on the root epidermis (Breygina et al, 2010;Dai and Chen, 2005). Organic acids in root exudates can dissolve and transform certain insoluble minerals via acidification, ligand exchange, and reduction, thus allowing nutrient release and thereby improving the bioavailability of nutrients (Guo et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Organic Acids Exuded From Roots Increase the Available Potassium Content in the Rhizosphere Soil: A Rhizobag Experiment in Nicotiana tabacum

Yang¹,

Yang²,

Yu³

et al. 2019

horts

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Additional index words. root, soil potassium, organic acid, root vigor, stress-resistant enzyme activity Abstract. Organic acid secretion from higher plant roots into the rhizosphere soil plays an important role in nutrient acquisition and metal detoxification; however, their precise functions and the related mechanisms in abiotic stress tolerance remain poorly understood. Tobacco is an important crop plant, so thoroughly elucidating these factors in tobacco is of high priority. In the present study, the activation effect on soil potassium (K), contents of exuded organic acids, and physiological changes in the roots of various tobacco varieties under both normal K supply and K-deficiency stress were investigated. Our results showed that one high-K variety (ND202) exhibited a significantly higher total content of organic acids in the root exudates and the highest available K content in the rhizosphere soil, compared with two common ones (K326 and NC89). Moreover, the high-K tobacco variety was less affected in terms of root vigor under K-deficiency stress, and displayed greater increases in the activities of the stress-resistant enzymes consisting of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT). Taken together, these results provide evidence that tobacco roots exude large amounts of organic acids to increase the available K content in the rhizosphere soil and improve the utilization rate of soil K.

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Effects of anion channel blockers NPPB and DIDS on tobacco pollen tube growth and its mitochondria state

Cited by 7 publications

References 26 publications

Tip‐localized Ca²⁺‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Tip‐localized Ca²⁺‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Pollen Tube Growth Regulation by Free Anions Depends on the Interaction between the Anion Channel SLAH3 and Calcium-Dependent Protein Kinases CPK2 and CPK20

Organic Acids Exuded From Roots Increase the Available Potassium Content in the Rhizosphere Soil: A Rhizobag Experiment in Nicotiana tabacum

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Effects of anion channel blockers NPPB and DIDS on tobacco pollen tube growth and its mitochondria state

Cited by 7 publications

References 26 publications

Tip‐localized Ca2+‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Tip‐localized Ca2+‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Pollen Tube Growth Regulation by Free Anions Depends on the Interaction between the Anion Channel SLAH3 and Calcium-Dependent Protein Kinases CPK2 and CPK20

Organic Acids Exuded From Roots Increase the Available Potassium Content in the Rhizosphere Soil: A Rhizobag Experiment in Nicotiana tabacum

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Tip‐localized Ca²⁺‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation

Tip‐localized Ca²⁺‐permeable channels control pollen tube growth via kinase‐dependent R‐ and S‐type anion channel regulation