Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps

Scherzer, Sönke; Böhm, Jennifer; Król, Elżbieta; Shabala, Lana; Kreuzer, Ines; Larisch, Christina; Bemm, Felix; Al‐Rasheid, Khaled A. S.; Shabala, Sergey; Rennenberg, Heinz; Neher, Erwin; Hedrich, Rainer

doi:10.1073/pnas.1507810112

Cited by 99 publications

(89 citation statements)

References 41 publications

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“…Likewise, plasma membrane transporters for sulfate, as well as nitrogen-containing solutes, were induced by insects, suggesting that metabolites and macromolecules, such as amino acids, peptides, and nucleotides/ DNA, all represent part of Dionaea's diet. Furthermore, we found that the Dionaea ammonium transporter DmAMT1 is induced in active traps, as well as a Dionaea AKT1-like potassium channel and a HAK5-like high-affinity potassium transporter (Scherzer et al 2015). When we analyzed the kinetics of transporter expression, it became apparent that upon trap stimulation, the expression of DmAMT1, DmHAK5, and DmHKT1 was induced 2-4 h after the onset of the stimulus, reaching peak expression after 12 h (Fig.…”

Section: −13mentioning

confidence: 89%

“…Dionaea requires potassium for turgor formation and trap reopening, as well as for growth and the development of new traps. For the uptake of prey-derived potassium ions, Dionaea glands operate two K + selective uptake systems in concert: a low-affinity, high-capacity K + channel DmAKT1 and a high-affinity, low-capacity proton-coupled K + transporter DmHAK5 (Scherzer et al 2015).…”

Section: Venus Flytrap Transcriptomementioning

confidence: 99%

“…Osmolarity was adjusted to 240 mOsm/kg using D-sorbitol. Membrane potential recordings were performed as described elsewhere (Scherzer et al 2015) using a standard solution supplemented with varying concentrations of either NaCl, KCl, or NH 4 Cl as indicated in the figure legend.…”

Section: Electrophysiologymentioning

confidence: 99%

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Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

et al. 2016

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Although the concept of botanical carnivory has been known since Darwin's time, the molecular mechanisms that allow animal feeding remain unknown, primarily due to a complete lack of genomic information. Here, we show that the transcriptomic landscape of the Dionaea trap is dramatically shifted toward signal transduction and nutrient transport upon insect feeding, with touch hormone signaling and protein secretion prevailing. At the same time, a massive induction of general defense responses is accompanied by the repression of cell death–related genes/processes. We hypothesize that the carnivory syndrome of Dionaea evolved by exaptation of ancient defense pathways, replacing cell death with nutrient acquisition.

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Section: −13mentioning

confidence: 89%

Section: Venus Flytrap Transcriptomementioning

confidence: 99%

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Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

et al. 2016

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“…The transcription of HAK5 is induced by K + deficiency (Gierth et al, 2005), which is an important mechanism in plant responses to LK stress . Recent reports showed that HAK5 and its ortholog in Dionaea muscipula (DmHAK5) are also regulated by the protein kinase CIPK23 (Ragel et al, 2015;Scherzer et al, 2015).…”

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confidence: 99%

AtKC1 and CIPK23 Synergistically Modulate AKT1-Mediated Low-Potassium Stress Responses in Arabidopsis

et al. 2016

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In Arabidopsis (Arabidopsis thaliana), the Shaker K + channel AKT1 conducts K + uptake in root cells, and its activity is regulated by CBL1/9-CIPK23 complexes as well as by the AtKC1 channel subunit. CIPK23 and AtKC1 are both involved in the AKT1-mediated low-K + (LK) response; however, the relationship between them remains unclear. In this study, we screened suppressors of low-K + sensitive [lks1 (cipk23)] and isolated the suppressor of lks1 (sls1) mutant, which suppressed the leaf chlorosis phenotype of lks1 under LK conditions. Map-based cloning revealed a point mutation in AtKC1 of sls1 that led to an amino acid substitution (G322D) in the S6 region of AtKC1. The G322D substitution generated a gain-of-function mutation, AtKC1 D , that enhanced K + uptake capacity and LK tolerance in Arabidopsis. Structural prediction suggested that glycine-322 is highly conserved in K + channels and may function as the gating hinge of plant Shaker K + channels. Electrophysiological analyses revealed that, compared with wild-type AtKC1, AtKC1 D showed enhanced inhibition of AKT1 activity and strongly reduced K + leakage through AKT1 under LK conditions. In addition, phenotype analysis revealed distinct phenotypes of lks1 and atkc1 mutants in different LK assays, but the lks1 atkc1 double mutant always showed a LK-sensitive phenotype similar to that of akt1. This study revealed a link between CIPK-mediated activation and AtKC1-mediated modification in AKT1 regulation. CIPK23 and AtKC1 exhibit distinct effects; however, they act synergistically and balance K + uptake/leakage to modulate AKT1-mediated LK responses in Arabidopsis.

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“…Growing on mineral-deficient soils, the carnivorous Venus flytrap (Dionaea muscipula) lures, captures, and digests small arthropods (3)(4)(5)(6)(7)(8) to feed on the nutrients extracted from their flesh (9)(10)(11)(12). Closure of the bilobed snap trap is initiated by mechanical stimulation of trigger hairs located at the inner trap surface.…”

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confidence: 99%

Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells

Scherzer

Shabala

Hedrich

et al. 2017

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

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The Venus flytrap Dionaea muscipula captures insects and consumes their flesh. Prey contacting touch-sensitive hairs trigger traveling electrical waves. These action potentials (APs) cause rapid closure of the trap and activate secretory functions of glands, which cover its inner surface. Such prey-induced haptoelectric stimulation activates the touch hormone jasmonate (JA) signaling pathway, which initiates secretion of an acidic hydrolase mixture to decompose the victim and acquire the animal nutrients. Although postulated since Darwin's pioneering studies, these secretory events have not been recorded so far. Using advanced analytical and imaging techniques, such as vibrating ion-selective electrodes, carbon fiber amperometry, and magnetic resonance imaging, we monitored stimuluscoupled glandular secretion into the flytrap. Trigger-hair bending or direct application of JA caused a quantal release of oxidizable material from gland cells monitored as distinct amperometric spikes. Spikes reminiscent of exocytotic events in secretory animal cells progressively increased in frequency, reaching steady state 1 d after stimulation. Our data indicate that trigger-hair mechanical stimulation evokes APs. Gland cells translate APs into touch-inducible JA signaling that promotes the formation of secretory vesicles. Early vesicles loaded with H + and Cl − fuse with the plasma membrane, hyperacidifying the "green stomach"-like digestive organ, whereas subsequent ones carry hydrolases and nutrient transporters, together with a glutathione redox moiety, which is likely to act as the major detected compound in amperometry. Hence, when glands perceive the haptoelectrical stimulation, secretory vesicles are tailored to be released in a sequence that optimizes digestion of the captured animal.amperometry | exocytosis | Dionaea muscipula | secretion | plant digestion

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Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps

Cited by 99 publications

References 41 publications

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

Venus flytrap carnivorous lifestyle builds on herbivore defense strategies

AtKC1 and CIPK23 Synergistically Modulate AKT1-Mediated Low-Potassium Stress Responses in Arabidopsis

Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells

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