Abscisic Acid-Induced Phosphoinositide Turnover in Guard Cell Protoplasts of Vicia faba

Lee, Youngsook; Choi, Young Bong; Suh, Sujeoung; Lee, Joon Sang; Assmann, Sarah M.; Joe, Cheol O.; Kelleher, Joseph F.; Crain, Richard C.

doi:10.1104/pp.110.3.987

Cited by 170 publications

(129 citation statements)

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“…This rapid increase in Ca 2ϩ is preceded by an increase in IP 3 (Lee et al, 1996) and is dependent on increased PLC activity (Staxen et al, 1999). Accordingly, microinjection of caged IP 3 into guard cells has been shown to be sufficient for stomatal closure (Gilroy et al, 1990).…”

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confidence: 99%

An Arabidopsis Inositol 5-Phosphatase Gain-of-Function Alters Abscisic Acid Signaling

2003

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Signals can be perceived and amplified at the cell membrane by receptors coupled to the production of a variety of second messengers, including inositol 1,4,5-trisphosphate (IP 3 ). We previously have identified 15 putative inositol 5-phosphatases (5PTases) from Arabidopsis and shown that At5PTase1 can hydrolyze IP 3 . To determine whether At5PTase1 can terminate IP 3 -mediated signaling, we analyzed transgenic plants ectopically expressing At5PTase1. Stomata from leaves of At5PTase1 transgenic plants were abscisic acid (ABA) and light insensitive, and ABA induction of genes was delayed. Quantification of IP 3 in plants exposed to ABA indicated that ABA induced two IP 3 increases in wild-type plants. Both of these IP 3 increases were reduced in At5PTase1 transgenic plants, indicating that IP 3 may be necessary for stomatal closure and temporal control of ABA-induced gene expression. To determine if ABA could induce expression of At5PTase1, we examined RNA and protein levels of At5PTase1 in wild-type plants exposed to ABA. Our results indicate that At5PTase1 is up-regulated in response to ABA. This is consistent with At5PTase1 acting as a signal terminator of ABA signaling.The ability to respond to a variety of biotic and abiotic signals is crucial to plants. Signals outside the cell can be perceived and amplified at the cell membrane by receptors linked to a variety of signaling pathways, including the inositol 1,4,5-trisphosphate (IP 3 ) pathway (Stevenson et al., 2000; Taylor and Thorn, 2001). In this pathway, signals activate phospholipase C (PLC), which catalyzes the hydrolysis of phosphatidylinositol-4,5-bisphosphate to form diacylglycerol and IP 3 . IP 3 then binds to intracellular receptors, triggering the release of Ca 2ϩ from intracellular stores into the cytosol (Berridge, 1993).In plants, there is evidence that signals such as light (Shacklock et al., 1992), gravity (Perera et al., 1999(Perera et al., , 2001, and abscisic acid (ABA; Wu et al., 1997; Sanchez and Chua, 2001) are relayed via IP 3 signaling. Most of the information on IP 3 signaling has arisen from studies utilizing ABA. The most notable affect of ABA on plants is its ability to induce stomatal closure (Allen et al., 2001). When open, stomatal pores allow the influx of CO 2 and water vapor to move outward, driving the transpirational process. ABA is thought to trigger stomatal closure by inducing cytosolic Ca 2ϩ increases, which, in turn inhibit plasma membrane H ϩ -ATPases and inwardrectifying K ϩ channels. Subsequent activation of outward-rectifying K ϩ channels allows for ion efflux from the guard cell and a decrease in guard cell turgor, resulting in stomatal closure (Blatt et al., 1990;Lemtiri-Chlieh and MacRobbie, 1994; Schroeder et al., 2001a).One key component in the mechanism of stomatal closure is an initial increase in cytosolic Ca 2ϩ concentration that occurs within minutes of ABA exposure (McAinsh et al., 2000;Allen et al., 2001; Webb et al., 2001). This rapid increase in Ca 2ϩ is preceded by an increase in IP 3 (Lee et a...

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confidence: 99%

An Arabidopsis Inositol 5-Phosphatase Gain-of-Function Alters Abscisic Acid Signaling

2003

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“…Their roles in regulation of stomatal movements have been reported previously. [1][2][3][4][5] The level of phosphoinositides changes rapidly in response to ABA treatment, while that of other membrane lipids remains similar, 1 suggesting that phosphoinositides are likely to be involved in ABA signaling. Various phosphoinositides use distinct mechanisms to induce distinct effects in regulating the stomatal aperture.…”

Section: Introductionmentioning

confidence: 99%

“…We predict that further analysis of the 5PTases may provide additional information on the role of this group of enzymes in guard cell signaling, based on our previous observation that when lithium, an inhibitor of inositol mono-and bis-phosphate phosphatases, was present in the guard cell protoplast medium, the level of Ins(1,4,5)P 3 increased approximately two fold after ABA treatment of guard cells. 1 The 5PTases may also inhibit stomatal opening by reducing the level of PtdIns(4,5)P 2 in the guard cells. Defective stomatal opening in plants that overexpress 5PTase 1 29 may be due to a decreased level of PtdIns(4,5)P 2 , but this possibility was not investigated.…”

Section: In Stomatal Openingmentioning

confidence: 99%

“…[17][18][19] The level of Ins(1,4,5)P 3 increases rapidly and transiently after ABA treatment of guard cells. 1 Photolysis of microinjected caged Ins(1,4,5)P 3 leads to Ca 2+ release, inactivates guard cell K + channels, and induces stomatal closing. 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.…”

Section: In Stomatal Openingmentioning

confidence: 99%

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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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“…In mammalian cells, Ins(1,4,5) P 3 is known to trigger calcium influx by activating calcium channels, 2 whereas DAG causes activation of protein kinase C (PKC). 3 Plant PI-PLC is associated with a spectrum of processes concerning signal transduction in events such as guard cell signaling, 4 salt stress, osmotic stress, acquired resistance, 5,6 Nod factor signaling, 7 drought, 8 systemic acquired resistance, 9 carbon fixation in C4 plants 10 and response to the pathogen. 11 In this review, we have attempted to introduce current understanding of plant PI-PLC with respect to its localization, regulation, and activity.…”

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confidence: 99%