Exogenous γ-aminobutyric acid (GABA) affects pollen tube growth via modulating putative Ca2+-permeable membrane channels and is coupled to negative regulation on glutamate decarboxylase

Yu, Guang Hui; Zou, Jie; Feng, Jing; Peng, Xiong Bo; Wu, Jizhong; Wu, Ying; Palanivelu, Ravishankar; Sun, Menghan

doi:10.1093/jxb/eru171

Cited by 88 publications

(60 citation statements)

References 45 publications

(75 reference statements)

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“…Thus, the Ca 2+ channels are the key components for regulating the Ca 2+ gradients and are consequently essential for pollen tube guidance. Using electrophysiological techniques, inward Ca 2+ currents were observed in both pollen grain and pollen tube protoplasts (31)(32)(33)(34)(35)(36), supporting the presence of plasma membrane Ca 2+ channels in pollen tube tips. Recently, a number of candidate Ca 2+ channels were identified in pollen tubes, including six cyclic nucleotide-gated channels (CNGCs) and two glutamate receptor-like channels (GLRs) in Arabidopsis (37)(38)(39)(40).…”

mentioning

confidence: 68%

Cyclic nucleotide-gated channel 18 is an essential Ca ²⁺ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Gao

Wang

et al. 2016

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

138

108

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In flowering plants, pollen tubes are guided into ovules by multiple attractants from female gametophytes to release paired sperm cells for double fertilization. It has been well-established that Ca2+ gradients in the pollen tube tips are essential for pollen tube guidance and that plasma membrane Ca2+ channels in pollen tube tips are core components that regulate Ca2+ gradients by mediating and regulating external Ca2+ influx. Therefore, Ca2+ channels are the core components for pollen tube guidance. However, there is still no genetic evidence for the identification of the putative Ca2+ channels essential for pollen tube guidance. Here, we report that the point mutations R491Q or R578K in cyclic nucleotide-gated channel 18 (CNGC18) resulted in abnormal Ca2+ gradients and strong pollen tube guidance defects by impairing the activation of CNGC18 in Arabidopsis. The pollen tube guidance defects of cngc18-17 (R491Q) and of the transfer DNA (T-DNA) insertion mutant cngc18-1 (+/−) were completely rescued by CNGC18. Furthermore, domain-swapping experiments showed that CNGC18’s transmembrane domains are indispensable for pollen tube guidance. Additionally, we found that, among eight Ca2+ channels (including six CNGCs and two glutamate receptor-like channels), CNGC18 was the only one essential for pollen tube guidance. Thus, CNGC18 is the long-sought essential Ca2+ channel for pollen tube guidance in Arabidopsis.

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confidence: 68%

Cyclic nucleotide-gated channel 18 is an essential Ca ²⁺ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Gao

Wang

et al. 2016

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

138

108

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“…In plants, GABA is not just a metabolite but rather a signal molecule, which was shown to be involved in various physiological processes such as pollen tube growth (Yu et al, 2014), regulation of intracellular Ca 2+ levels (Fait et al, 2008) and ethylene production (Shi et al, 2010;Takayama et al, 2017); however, its functional mechanisms remain largely elusive (Bown and Shelp, 2016;Ramesh et al, 2015). In our study, the vegetative growth and flower/fruit setting were severely affected in GABA-increased mutants ( Figure 6 and Figures S6, S7 and S8), and a large number of GABA mutants exhibited dwarfism compared to WT plants ( Figure S6).…”

Section: Gaba Affects Plant Vegetative and Reproductive Growthmentioning

confidence: 99%

Multiplexed CRISPR/Cas9‐mediated metabolic engineering of γ‐aminobutyric acid levels in Solanum lycopersicum

Lin

et al. 2017

Plant Biotechnology Journal

231

103

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SummaryIn recent years, the type II CRISPR system has become a widely used and robust technique to implement site‐directed mutagenesis in a variety of species including model and crop plants. However, few studies manipulated metabolic pathways in plants using the CRISPR system. Here, we introduced the pYLCRISPR/Cas9 system with one or two single‐site guide RNAs to target the tomato phytoene desaturase gene. An obvious albino phenotype was observed in T0 regenerated plants, and more than 61% of the desired target sites were edited. Furthermore, we manipulated the γ‐aminobutyric acid (GABA) shunt in tomatoes using a multiplex pYLCRISPR/Cas9 system that targeted five key genes. Fifty‐three genome‐edited plants were obtained following single plant transformation, and these samples represented single to quadruple mutants. The GABA accumulation in both the leaves and fruits of genomically edited lines was significantly enhanced, and the GABA content in the leaves of quadruple mutants was 19‐fold higher than that in wild‐type plants. Our data demonstrate that the multiplex CRISPR/Cas9 system can be exploited to precisely edit tomato genomic sequences and effectively create multisite knockout mutations, which could shed new light on plant metabolic engineering regulations.

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“…In plants, the application of 50 µM 3-MPA was shown to affect GABA synthesis, causing an abnormal formation of pollen tubes due to the disruption of actin organization in these organs. With higher amounts (2 mM), 3-MPA completely inhibited pollen germination (Yu et al 2014). Using 50 µM 3-MPA, our results show that the GABA-induced tendril coiling score was significantly reduced by the inhibitor after 20 and 30 h (Fig.…”

Section: Impact Of Ja and Gaba On Tendril Coiling In Grapevinementioning

confidence: 58%

“…However, in plants, GABA was reported to be involved in diverse processes, such as influencing cell respiration by regulating the Krebs cycle and acting as a compound for signaling development and growth (Bouché and Fromm 2004;Bown and Shelp 2016). In Arabidopsis and tobacco, optimal pollen, pistil, and root growth were described to be dependent on GABA levels (Mirabella et al 2008;Renault et al 2011;Yu et al 2014). GABA can accumulate in plants upon abiotic stress such as salt and cold (Wallace et al 1984;Ramputh and Bown 1996).…”

Section: Tendrils Show Higher Gaba Levelsmentioning

confidence: 99%

Tendril Coiling in Grapevine: Jasmonates and a New Role for GABA?

Malabarba

Reichelt

Pasquali

et al. 2018

J Plant Growth Regul

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Grapevine (Vitis vinifera L., Vitaceae) belongs to the genus Vitis, and is characterized as a vine due to the presence of tendrils, which are located opposite to leaves. Tendrils are thigmo-responsive organs, able to carry out delicate mechanosensory responses upon touch and related stimuli. These organs are an adaptation of the plant to climb with the help of support to higher places and finally remain at a position with favorable light quality. In previous studies on Bryonia dioica (Cucurbitaceae), phytohormones of the jasmonate class were identified as the endogenous hormone signals to initiate coiling of the tendrils. Strikingly, this is still the only example for jasmonate-induced tendril coiling. In grapevine, three compounds (12-oxo-phytodienoic acid, jasmonic acid (JA), and JA isoleucine conjugate) of the jasmonate class were found at higher concentrations in non-coiled tendrils when compared with coiled ones. Upon treatment with phytohormones, we could confirm the activity of jasmonates on tendril coiling in grapevine. However, not jasmonates but a non-proteinogenic amino acid, γ-aminobutyric acid (GABA), was detected to accumulate in grapevine tendrils at significantly higher levels than in all other tissues, independent of their coiling status. For GABA we detected a significant, transient positive effect on tendril coiling. Use of a GABA synthesis blocker, 3-mercaptopropionic acid, caused reduced GABA-but not JA-induced coiling scores. No additive effect of JA plus GABA was detectable on the tendrils' coiling score. Thus, for grapevine, our data demonstrate a strong activity of jasmonates in tendril coiling induction even without mechanical stimuli and, furthermore, the data also suggest that GABA can independently promote tendril coiling.

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Exogenous γ-aminobutyric acid (GABA) affects pollen tube growth via modulating putative Ca2+-permeable membrane channels and is coupled to negative regulation on glutamate decarboxylase

Abstract: SummaryThis work reveals how tobacco pistil and style may communicate with pollen tubes and regulate their growth during fertilization via the γ-aminobutyric acid–Ca2+-permeable channel–glutamate decarboxylase–calmodulin signalling pathway.

Cited by 88 publications

References 45 publications

Cyclic nucleotide-gated channel 18 is an essential Ca ²⁺ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Cyclic nucleotide-gated channel 18 is an essential Ca ²⁺ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Multiplexed CRISPR/Cas9‐mediated metabolic engineering of γ‐aminobutyric acid levels in Solanum lycopersicum

Tendril Coiling in Grapevine: Jasmonates and a New Role for GABA?

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Exogenous γ-aminobutyric acid (GABA) affects pollen tube growth via modulating putative Ca2+-permeable membrane channels and is coupled to negative regulation on glutamate decarboxylase

Abstract: SummaryThis work reveals how tobacco pistil and style may communicate with pollen tubes and regulate their growth during fertilization via the γ-aminobutyric acid–Ca2+-permeable channel–glutamate decarboxylase–calmodulin signalling pathway.

Cited by 88 publications

References 45 publications

Cyclic nucleotide-gated channel 18 is an essential Ca 2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Cyclic nucleotide-gated channel 18 is an essential Ca 2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Multiplexed CRISPR/Cas9‐mediated metabolic engineering of γ‐aminobutyric acid levels in Solanum lycopersicum

Tendril Coiling in Grapevine: Jasmonates and a New Role for GABA?

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Cyclic nucleotide-gated channel 18 is an essential Ca ²⁺ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis

Cyclic nucleotide-gated channel 18 is an essential Ca ²⁺ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis