The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in <i>Arabidopsis</i>

Li, Lijuan; Ren, Fei; Gao, Xin-Qi; Wei, Pengcheng; Wang, Xuechen

doi:10.1111/j.1365-3040.2012.02592.x

Cited by 45 publications

(45 citation statements)

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“…Monitoring the dynamic changes in guard cell vacuolar structures revealed an intense remodeling during stomatal movements (11,12). Pharmacological and genetic approaches indicated that dynamic changes of the vacuole are crucial for achieving the full amplitude of stomatal movement (12)(13)(14). However, so far, no specific tonoplast transport proteins or processes have been functionally linked to vacuolar dynamics during guard cell movements.…”

mentioning

confidence: 99%

Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake

Andrés

Perez‐Hormaeche

Leidi

et al. 2014

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

197

155

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Stomatal movements rely on alterations in guard cell turgor. This requires massive K + bidirectional fluxes across the plasma and tonoplast membranes. Surprisingly, given their physiological importance, the transporters mediating the energetically uphill transport of K + into the vacuole remain to be identified. Here, we report that, in Arabidopsis guard cells, the tonoplast-localized K + / H + exchangers NHX1 and NHX2 are pivotal in the vacuolar accumulation of K + and that nhx1 nhx2 mutant lines are dysfunctional in stomatal regulation. Hypomorphic and complete-loss-of-function double mutants exhibited significantly impaired stomatal opening and closure responses. Disruption of K + accumulation in guard cells correlated with more acidic vacuoles and the disappearance of the highly dynamic remodelling of vacuolar structure associated with stomatal movements. Our results show that guard cell vacuolar accumulation of K + is a requirement for stomatal opening and a critical component in the overall K + homeostasis essential for stomatal closure, and suggest that vacuolar K + fluxes are also of decisive importance in the regulation of vacuolar dynamics and luminal pH that underlie stomatal movements.stomata | luminal pH control T he rapid accumulation and release of K + and of organic and inorganic anions by guard cells controls the opening and closing of stomata and thereby gas exchange and transpiration of plants. The intracellular events that underlie stomatal opening start with plasma membrane hyperpolarization caused by the activation of H + -ATPases, which induces K + uptake through voltage-gated inwardly rectifying K + in channels (1). Potassium uptake is accompanied by the electrophoretic entry of the counterions chloride, nitrate, and sulfate, and by the synthesis of malate. These osmolytes, together with sucrose accumulation, increase the turgor in guard cells and thereby drive stomatal opening. Stomatal closure is initiated by activation of the plasma membrane localized chloride and nitrate efflux channels SLAC1 and SLAH3 that are regulated by the SnRK2 protein kinase OST1 and the Ca 2+ -dependent protein kinases CPK21 and 23 (2, 3). CPK6 also activates SLAC1 and coordinately inhibits rectifying K + in channels to hinder stomatal opening (4, 5). Sulfate and organic acids exit the guard cell through R-type anion channels. The accompanying reduction in guard cell turgor results in stomatal closure (1).Despite the established role of plasma membrane transport in guard cell function and stomatal movement, ion influx into the cytosol represents only a transit step to the vacuole, as more than 90% of the solutes released from guard cells originate from vacuoles (6). In contrast to the plasma membrane, knowledge of the transport processes occurring in intracellular compartments of guard cells during stomatal movements is less advanced (7). Only recently, AtALMT9 has been shown to act as a malateinduced chloride channel at the tonoplast that is required for stomatal opening (8). Vacuoles govern turgor-driven cha...

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mentioning

confidence: 99%

Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake

Andrés

Perez‐Hormaeche

Leidi

et al. 2014

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

197

155

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“…3), seemed to function separately, with the internal layer being linked to the tannin content and the external layer being attached to the cytoplasmic cytoskeleton (Fleurat-Lessard 1988). Indeed, the actin network is involved in the regulation of vacuole morphology, as shown by its disruption in Arabidopsis guard cells, which results in the inhibition of vacuole fusion during stomatal opening (Li et al 2012). However, the detailed mechanism of the manner by which actin affects transvacuolar strand formation, and vacuole fusion has not yet been elucidated (Zhang et al 2014).…”

Section: Distributions Of Double Vacuolar Apparatus In Various Sensitmentioning

confidence: 96%

Co-occurrence of tannin and tannin-less vacuoles in sensitive plants

Fleurat‐Lessard

Béré²,

Lallemand³

et al. 2015

Protoplasma

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Vacuoles of different types frequently coexist in the same plant cell, but the duality of the tannin/tannin-less vacuoles observed in Mimosa pudica L. is rare. In this plant, which is characterized by highly motile leaves, the development and original features of the double vacuolar compartment were detailed in primary pulvini from the young to the mature leaf stage. In young pulvini, the differentiation of tannin vacuoles first occurred in the epidermis and progressively spread toward the inner cortex. In motor cells of nonmotile pulvini, tannin deposits first lined the membranes of small vacuole profiles and then formed opaque clusters that joined together to form a large tannin vacuole (TV), the proportion of which in the cell was approximately 45%. At this stage, transparent vacuole profiles were rare and small, but as the parenchyma cells enlarged, these profiles coalesced to form a transparent vacuole with a convexity toward the larger-sized tannin vacuole. When leaf motility began to occur, the two vacuole types reached the same relative proportion (approximately 30%). Finally, in mature cells displaying maximum motility, the large transparent colloidal vacuole (CV) showed a relative proportion increasing to approximately 50%. At this stage, the proportion of the tannin vacuole, occurring in the vicinity of the nucleus, decreased to approximately 10%. The presence of the condensed type of tannins (proanthocyanidins) was proven by detecting their fluorescence under UV light and by specific chemical staining. This dual vacuolar profile was also observed in nonmotile parts of M. pudica (e.g., the petiole and the stem). Additional observations of leaflet pulvini showing more or less rapid movements showed that this double vacuolar structure was present in certain plants (Mimosa spegazzinii and Desmodium gyrans), but absent in others (Albizzia julibrissin, Biophytum sensitivum, and Cassia fasciculata). Taken together, these observations strongly suggest that a direct correlation cannot be found between the presence of a tannin vacuole and the osmoregulated motility of pulvini.

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“…Even in Arabidopsis, different cell types have an order-of-magnitude variation in filament elongation rates. For example, studies have found that guard cells and pollen have elongation rates of 0.3-0.7 μm/s (57,82,83,134), which, when balanced with disassembly at nearly equal rates, could be indicative of filament treadmilling. Similarly, in moss protonemal cells and Arabidopsis cotyledon or root epidermal cells, assembly and disassembly appear to be nearly equivalent (3,96).…”

Section: Variations On a Theme In Different Organisms And Cell Typesmentioning

confidence: 98%

“…In very few cases, however, have single-filament dynamics been evaluated quantitatively in these mutant plants. Guard cells from Arabidopsis arp2 and arp3 mutants have modest but significant increases in actin filament dynamics ( Table 2): Filament elongation and depolymerization rates are enhanced by as much as 40%, and the severing frequency is doubled (57). The reason for this is not clear, because the ARP2/3 complex is not known to sever filaments or bind G-actin, unless perhaps there is a shift in the ratio of F-to G-actin in arp2/3 mutant plants.…”

Section: Filament Initiation Needs To Be Interrogated Genetically Andmentioning

confidence: 99%

“…Thus, guard cells have the potential to become a powerful model system for characterizing the interaction between early signaling events and actin dynamics within a single cell (38,39,57,100,109,121). A large number of signaling components that potentially mediate actin remodeling in guard cells have been identified.…”

Section: Stomatal Opening Is Modulated By Actin Remodeling and Dynamimentioning

confidence: 99%

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Signaling to Actin Stochastic Dynamics

Li¹,

Blanchoin

Staiger

2015

Annu. Rev. Plant Biol.

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Advances in microscopy techniques applied to living cells have dramatically transformed our view of the actin cytoskeleton as a framework for cellular processes. Conventional fluorescence imaging and static analyses are useful for quantifying cellular architecture and the network of filaments that support vesicle trafficking, organelle movement, and response to biotic stress. However, new imaging techniques have revealed remarkably dynamic features of individual actin filaments and the mechanisms that underpin their construction and turnover. In this review, we briefly summarize knowledge about actin and actin-binding proteins in plant systems. We focus on the quantitative properties of the turnover of individual actin filaments, highlight actin-binding proteins that participate in actin dynamics, and summarize the current genetic evidence that has been used to dissect specific aspects of the stochastic dynamics model. Finally, we describe some signaling pathways in which recent data implicate changes in actin filament dynamics and the associated cytoplasmic responses.

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The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in Arabidopsis

Abstract: ABSTRACT

Cited by 45 publications

References 50 publications

Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake

Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake

Co-occurrence of tannin and tannin-less vacuoles in sensitive plants

Signaling to Actin Stochastic Dynamics

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