Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C

Staxén, Irina; Pical, Christophe; Montgomery, L. T.; Gray, Julie E.; Hetherington, Alistair M.; McAinsh, Martin Robert

doi:10.1073/pnas.96.4.1779

Cited by 340 publications

(324 citation statements)

References 49 publications

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“…1), showing that the PP1/PP2A protein phosphatase inhibitors, okadaic acid and calyculin A, enhanced I Ca channel activity (Köhler and Blatt, 2002). In addition, phospholipids have been implicated in ABA-triggered cytosolic Ca 21 increases and stomatal closure (Staxen et al, 1999;Lemtiri-Chlieh et al, 2000). Treatment of epidermal strips with the phosphatidylinositol (PI)-3-kinase and PI-4-kinase inhibitors wortmannin and LY294002 inhibited PI kinase enzyme activities, enhanced stomatal opening, and impaired ABA-induced cytosolic Ca 21 increases, indicating that PI-3-P and PI-4-P modulate ABA signaling in guard cells (Jung et al, 2002).…”

Section: Ros and Aba Signalingmentioning

confidence: 99%

The Role of Reactive Oxygen Species in Hormonal Responses

Kwak

Nguyen²,

Schroeder³

2006

Plant Physiology

306

193

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Reactive oxygen species (ROS) are versatile molecules mediating a variety of cellular responses in plant cells, including programmed cell death (PCD), development, gravitropism, and hormone signaling. A picture showing how ROS function in signal transduction networks has started to emerge as the result of recent studies providing genetic, cell biological, and physiological evidence describing roles for ROS in signaling (Apel and Hirt, 2004;Laloi et al., 2004;Mittler et al., 2004;Mori and Schroeder, 2004). However, further efforts are necessary to characterize the targets and molecular functions of ROS, as well as the complex interplay of ROS-generating and ROSscavenging mechanisms. Moreover, the interactions of nitric oxide with other ROS species in hormone signaling is a subject of interest (Desikan et al., 2004;Wendehenne et al., 2004;Guo and Crawford, 2005;Bright et al., 2006). Due to limited space, in this Update article we focus on recent progress made in understanding the roles of ROS in hormone signaling. AUXIN, ETHYLENE, AND ROSROS have been implicated as second messengers in several plant hormone responses. Joo et al. (2001) showed that ROS are asymmetrically generated in roots by gravistimulation to regions of reduced growth. A function for ROS in root curvature was reported by inhibiting cell growth, thus contributing to tropisms. Auxin also induced ROS production in roots and the auxin transport inhibitor N-1-naphthylphthlamic acid did not inhibit hydrogen peroxide (H 2 O 2 )-induced root curvature, leading to the suggestion that ROS play a role downstream of transport in auxin signaling and gravitropism (Joo et al., 2001).A pharmacological study suggested that ethylene and ROS are required for root nodule initiation and function as positive transducers downstream of the Nod factor response in a semiaquatic legume (D'Haeze et al., 2003). Additional studies have suggested roles of ethylene in either stomatal opening or closing, depending on the plant species (Giulivo, 1986). Recently, it was reported that H 2 O 2 -mediated stomatal closure is completely disrupted in the loss-of-function mutant of the ethylene receptor etr1-7, suggesting a role for ETR1 in guard cell ROS signaling and stomatal closure (Desikan et al., 2005). Interestingly, in another recent study, ethylene was proposed to counteract stomatal closure (Tanaka et al., 2005). Abscisic acid (ABA)-induced stomatal closure was inhibited by ethylene or the hormone precursor 1-aminocyclopropane-1-carboxylic acid and by the ethylene-overproducing mutation eto1-1 (Tanaka et al., 2005). Moreover, this ethylene-induced inhibition of stomatal closure was suppressed in two ethylene-insensitive mutants, the dominant etr1-1 allele, and ein3-1 (Tanaka et al., 2005). Reverse transcription-PCR analysis with guard cellenriched epidermal strips showed that ETR1 is expressed in guard cells (Desikan et al., 2005). ATH1 and AG oligonucleotide-based (Affymetrix) microarray analyses of guard cell-expressed genes suggest that at least the ETR1, ERS1, and EIN4 eth...

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Section: Ros and Aba Signalingmentioning

confidence: 99%

The Role of Reactive Oxygen Species in Hormonal Responses

Kwak

Nguyen²,

Schroeder³

2006

Plant Physiology

306

193

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“…It should be noted that in other ABA-dependent responses that involve Ca 2ϩ , PI-PLC is not always implicated. For example, in broad bean, a total inhibition of ABA-induced stomatal closure requires both U73122 and nicotinamide, an inhibitor of cADPR synthesis (Jacob et al, 1999) whereas, in Commelina communis, treatment with U73122 is sufficient to inhibit ABA-induced cytosolic [Ca 2ϩ ] oscillations and stomatal closure (Staxen et al, 1999). Thus, it appears that different Ca 2ϩ channels may act in parallel or cooperate in ABA-signaling pathways according to the cell or the organ considered.…”

Section: Rab18 Expression In Arabidopsis Suspension Cellsmentioning

confidence: 99%

“…In the same species, it was demonstrated that an increase in PLC1 activity was necessary for the induction of the RD29a, KIN2, and RD22 ABAresponsive genes . In Commelina communis guard cells, Staxen et al (1999) have shown that U73122, an inhibitor of phosphatidylinositol-PLC (PI-PLC) activity, abolished ABAinduced cytosolic [Ca 2ϩ ] oscillations and stomatal closure.The involvement of phospholipase D (PLD) in ABA responses is better understood (Wang, 1999;Munnik, 2001 Article, publication date, and citation information can be found at www.plantphysiol.org/cgi …”

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confidence: 99%

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Plasmalemma Abscisic Acid Perception Leads to RAB18Expression via Phospholipase D Activation in Arabidopsis Suspension Cells

et al. 2002

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Abscisic acid (ABA) plays a key role in the control of stomatal aperture by regulating ion channel activities and water exchanges across the plasma membrane of guard cells. Changes in cytoplasmic calcium content and activation of anion and outward-rectifying K ϩ channels are among the earliest cellular responses to ABA in guard cells. In Arabidopsis suspension cells, we have demonstrated that outer plasmalemma perception of ABA triggered similar early events. Furthermore, a Ca 2ϩ influx and the activation of anion channels are part of the ABA-signaling pathway leading to the specific expression of RAB18. Here, we determine whether phospholipases are involved in ABA-induced RAB18 expression. Phospholipase C is not implicated in this ABA pathway. Using a transphosphatidylation reaction, we show that ABA plasmalemma perception results in a transient stimulation of phospholipase D (PLD) activity, which is necessary for RAB18 expression. Further experiments showed that PLD activation was unlikely to be regulated by heterotrimeric G proteins. We also observed that ABA-dependent stimulation of PLD was necessary for the activation of plasma anion current. However, when ABA activation of plasma anion channels was inhibited, the ABA-dependent activation of PLD was unchanged. Thus, we conclude that in Arabidopsis suspension cells, ABA stimulation of PLD acts upstream from anion channels in the transduction pathway leading to RAB18 expression.Abscisic acid (ABA) regulates seed maturation and germination, adaptation of plants to water shortage, cold, and high salinity (Leung and Giraudat, 1998). Several ABA transduction mutants have been isolated in Arabidopsis in which diverse loci affecting ABA response have been identified (for review, see Merlot and Giraudat, 1997;Leung and Giraudat, 1998). Among the best characterized are the ABAinsensitive abi-1 and abi-2 mutations, which affect protein phosphatases (Leung et al., 1997); the abi-3 (Giraudat et al., 1992;Parcy et al., 1994), abi-4 (Finkelstein et al., 1998), and abi-5 (Finkelstein and Lynch, 2000), which are mutated in transcription processes; and the ABA-hypersensitive era1 mutant, deleted for the ␤-subunit of a farnesyl transferase which acts as a negative regulator (Cutler et al., 1996). In guard cells, ABA transduction pathways have been extensively analyzed. Stomatal aperture is controlled by ABA through the activation of anion currents, which depolarizes the plasma membrane and promotes the activation of outward-rectifying K ϩ currents (Schroeder et al., 2001). In aleurone cells, ABA causes a decrease in cytoplasmic Ca 2ϩ content, which is necessary for the inhibition of GA promotion of ␣-amylase activity (Ritchie and Gilroy, 1998). In Arabidopsis suspension cells, similar ion channel activation has been observed (Jeannette et al., 1999; Ghelis et al., 2000a Ghelis et al., , 2000bTakahashi et al., 2001). However, the precise sequence of events triggered by ABA in these models remains unknown.Recent research has provided new data about the role of phospholipases...

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“…17,18 Conversely, microinjection of the Ins(1,4,5)P 3 antagonist heparin 20 or reduction of Ins(1,4,5)P 3 production by inhibiting the activity or expression of PI-PLCs inhibits ABA-mediated signal transduction in guard cells. 21,22 Among the nine putative PI-PLC isoforms found in the Arabidopsis genome, 23,24 only PLC1 has been studied in depth, but not in guard cells. PLC1 is highly induced under dehydration and high salinity conditions 25 and is required for secondary responses to ABA signals.…”

Section: In Stomatal Openingmentioning

confidence: 99%

Roles of phosphoinositides in regulation of stomatal movements

Lee

2008

Plant Signaling & Behavior

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Guard cells sense various environmental and internal stimuli and, in response, modulate the stomatal aperture to a size optimal for growth and adaptation. Among the many factors involved in the fine regulation of stomata, we have focused our studies on the role of phosphoinositides. Our recent study published in the Plant Journal (52:803-16) provides evidence for an important role for phosphatidylinositol 4,5-bis-phosphate (PtdIns(4,5)P 2 ) in inducing stomatal opening. Light induces translocation of a PtdIns(4,5)P 2 -binding protein from the cytosol to the plasma membrane and treatments that increase the intracellular PtdIns(4,5)P 2 level induce stomatal opening in the absence of light irradiation. Inhibition of anion channel activity, a negative regulator for stomatal opening, was suggested as a mechanism of PtdIns(4,5)P 2 -induced stomatal opening. We also reported that phosphatidylinositol 3-phosphate (PtdIns(3)P) and phosphatidylinositol 4-phosphate (PtdIns(4)P) regulate actin dynamics in guard cells. The effects of the phosphoinositides were specific, and were not induced by other lipids with similar structures. The roles of different interacting partners are likely to be important for these lipids to produce specific changes in guard cell activity.

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Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C

Cited by 340 publications

References 49 publications

The Role of Reactive Oxygen Species in Hormonal Responses

The Role of Reactive Oxygen Species in Hormonal Responses

Plasmalemma Abscisic Acid Perception Leads to RAB18Expression via Phospholipase D Activation in Arabidopsis Suspension Cells

Roles of phosphoinositides in regulation of stomatal movements

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