Actin Filaments of Guard Cells Are Reorganized in Response to Light and Abscisic Acid

Eun, Soon-Ok; Lee, Youngsook

doi:10.1104/pp.115.4.1491

Cited by 119 publications

(107 citation statements)

References 29 publications

(24 reference statements)

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“…There is a growing body of evidence suggesting that fast reconfiguration of guard‐cell cortical actin bundles occurs during stomatal closure triggered by darkness, abscisic acid (ABA) and pathogen‐associated molecular patterns (Eun & Lee, 1997; Gao et al ., 2008; Shimono et al ., 2016). Moreover, stabilisation of filamentous actin using phalloidin prevents ABA‐induced stomatal closure, indicating an important function of actin reorganisation in stomatal regulation (Kim et al ., 1995).…”

Section: Introductionmentioning

confidence: 99%

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Isner

Costa

et al. 2017

New Phytologist

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Summary Stomata respond to darkness by closing to prevent excessive water loss during the night. Although the reorganisation of actin filaments during stomatal closure is documented, the underlying mechanisms responsible for dark‐induced cytoskeletal arrangement remain largely unknown.We used genetic, physiological and cell biological approaches to show that reorganisation of the actin cytoskeleton is required for dark‐induced stomatal closure.The opal5 mutant does not close in response to darkness but exhibits wild‐type (WT) behaviour when exposed to abscisic acid (ABA) or CaCl2. The mutation was mapped to At5g18410, encoding the PIR/SRA1/KLK subunit of the Arabidopsis SCAR/WAVE complex. Stomata of an independent allele of the PIR gene (Atpir‐1) showed reduced sensitivity to darkness and F1 progenies of the cross between opal5 and Atpir‐1 displayed distorted leaf trichomes, suggesting that the two mutants are allelic. Darkness induced changes in the extent of actin filament bundling in WT. These were abolished in opal5. Disruption of filamentous actin using latrunculin B or cytochalasin D restored wild‐type stomatal sensitivity to darkness in opal5.Our findings suggest that the stomatal response to darkness is mediated by reorganisation of guard cell actin filaments, a process that is finely tuned by the conserved SCAR/WAVE–Arp2/3 actin regulatory module.

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Section: Introductionmentioning

confidence: 99%

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Isner

Costa

et al. 2017

New Phytologist

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“…those lining the whole post-cytokinetic VW, the stomatal pore AF bundle, the AFs lining the polar VW ends and the radial AFs lining the periclinal walls (the first three AF ' systems ' are described for the first time herein ; radial AFs have already been described in GCs of Selaginella (Cleary et al, 1993), Commelina (Kim et al, 1995 ;Eun & Lee, 1997), and Tradescantia (Cleary & Mathesius, 1996)) ; (b) the consistent positional relationship of most cortical AF and MT systems observed in GCs ; (c) the reorganization of AFs lining the periclinal walls at an advanced stage of GC differentiation, a phenomenon not followed by MTs, which retain their radial pattern ; at this stage the cortical AFs form a reticulum lining the margins of the growing wall thickenings of the stomatal pore.…”

Section: Actin Filament Organization In Differentiating Guard Cellsmentioning

confidence: 99%

“…The presence of cortical actin filaments (AFs) in the kidney-shaped GCs has been described only in Commelina (Kim et al, 1995 ;Eun & Lee, 1997), Tradescantia (Cleary & Mathesius, 1996) and Selaginella (Cleary et al, 1993). On the periclinal GC faces they appear to radiate out from the rims of the stomatal pore.…”

Section: mentioning

confidence: 99%

Microtubule and actin filament organization during stomatal morphogenesis in the fern Asplenium nidus. II. Guard cells

Apostolakos

Galatis

1999

New Phytologist

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The post-cytokinetic guard cells of Asplenium nidus display a prominent perinuclear microtubule system and a few microtubules under the periclinal walls. Afterwards, microtubules appear on the whole surface of the ventral wall, whereas those below the periclinal walls proliferate and tend to become parallel with the ventral wall. The perinuclear microtubules gradually diminish but persist in later stages of guard cell differentiation. In postcytokinetic guard cells, actin is found in the perinuclear cytoplasm and in the cortical cytoplasm lining all the walls. In differentiating guard cells, the following cortical microtubules and actin filament ' systems ' appear in succession : (a) radial microtubule and actin filament arrays beneath the periclinal walls converging on the stomatal pore region, (b) anticlinal microtubule bundles, which are co-localized with actin filaments, along the ventral wall outlining the region of the stomatal pore, (c) periclinal microtubules and actin filaments on the polar ventral wall ends. These cytoskeletal systems, except for the radial actin filaments, persist in advanced stages of guard cell differentiation. Instead of the radial actin filaments, a prominent actin filament reticulum is organized under the margins of the developing wall thickenings of the stomatal pore. In addition, an extensive endoplasmic actin filament reticulum develops around the plastids. It seems likely that the successive microtubule systems in guard cells are formed by putative microtubule organizing centres operating in a definite spatial and temporal succession. Guard cell morphogenesis is the outcome of a definite process, in which the cortical microtubule cytoskeleton plays the primary role, implicated in the deposition of cellulose microfibrils and probably of the local wall thickenings. Callose or a callose-like glucan is deposited on the whole surface of the nascent ventral wall and in the wall regions where thickenings are deposited. Finally, the guard cells of Asplenium assume a kidney shape and display polar hypostomatic swellings. Particular structural features established in guard cell mother cells affect guard cell morphogenesis.

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“…Closure of stomata has been ascribed to a release of the guard cell turgor pressure primarily caused by Cl − and K + efflux (Blatt 2000). Additionally, a reorganization of the actin cytoskeleton of guard cells has been observed after ABA treatment (Eun and Lee 1997). Despite this observation, the precise role of the actin cytoskeleton in regulating stomatal relaxation has remained elusive because of the lack of characterized regulators of the plant actin cytoskeleton (Blatt 2000).…”

mentioning

confidence: 98%

Inactivation of AtRac1 by abscisic acid is essential for stomatal closure

Lemichez¹,

Wu²,

Sánchez³

et al. 2001

Genes Dev.

232

229

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Plant water homeostasis is maintained by the phytohormone abscisic acid (ABA), which triggers stomatal pore closure in response to drought stress. We identified the Arabidopsis small guanosine triphosphatase (GTPase) protein AtRac1 as a central component in the ABA-mediated stomatal closure process. ABA treatment induced inactivation of AtRac GTPases and disruption of the guard cell actin cytoskeleton. In contrast, in the ABA-insensitive mutant abi1-1, which is impaired in stomatal closure, neither AtRac inactivation nor actin cytoskeleton disruption was observed on ABA treatment. These observations indicate that AtRac1 inactivation is a limiting step in the ABA-signaling cascade leading to stomatal closure. Consistent with these findings, expression of a dominant-positive mutant of AtRac1 blocked the ABA-mediated effects on actin cytoskeleton and stomatal closure in wild-type plants, whereas expression of a dominant-negative AtRac1 mutant recapitulated the ABA effects in the absence of the hormone. Moreover, the dominant-negative form of AtRac1 could also restore stomatal closure in abi1-1. These results define AtRac1 as a central element for plant adaptation to drought.

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Actin Filaments of Guard Cells Are Reorganized in Response to Light and Abscisic Acid

Cited by 119 publications

References 29 publications

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Microtubule and actin filament organization during stomatal morphogenesis in the fern Asplenium nidus. II. Guard cells

Inactivation of AtRac1 by abscisic acid is essential for stomatal closure

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