Cooperative Function of PLDδ and PLDα1 in Abscisic Acid-Induced Stomatal Closure in Arabidopsis
Misugi UrajiTakeshi KatagiriEiji OkumaWenxiu YeMohammad Anowar HossainChoji MasudaAya MiuraYoshimasa NakamuraIzumi C. MoriKazuo ShinozakiYoshiyuki Murata
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Abstract Phospholipase D (PLD) is involved in responses to abiotic stress and abscisic acid (ABA) signaling. To investigate the roles of two Arabidopsis (Arabidopsis thaliana) PLDs, PLDα1 and PLDδ, in ABA signaling in guard cells, we analyzed ABA responses in guard cells using Arabidopsis wild type, pldα1 and pldδ single mutants, and a pldα1 pldδ double mutant. ABA-induced stomatal closure was suppressed in the pldα1 pldδ double mutant but not in the pld single mutants. The pldα1 and pldδ mutations reduced ABA-induced phosphatidic acid production in epidermal tissues. Expression of either PLDα1 or PLDδ complemented the double mutant stomatal phenotype. ABA-induced stomatal closure in both pldα1 and pldδ single mutants was inhibited by a PLD inhibitor (1-butanol ), suggesting that both PLDα1 and PLDδ function in ABA-induced stomatal closure. During ABA-induced stomatal closure, wild-type guard cells accumulate reactive oxygen species and nitric oxide and undergo cytosolic alkalization, but these changes are reduced in guard cells of the pldα1 pldδ double mutant. Inward-rectifying K+ channel currents of guard cells were inhibited by ABA in the wild type but not in the pldα1 pldδ double mutant. ABA inhibited stomatal opening in the wild type and the pldδ mutant but not in the pldα1 mutant. In wild-type rosette leaves, ABA significantly increased PLDδ transcript levels but did not change PLDα1 transcript levels. Furthermore, the pldα1 and pldδ mutations mitigated ABA inhibition of seed germination. These results suggest that PLDα1 and PLDδ cooperate in ABA signaling in guard cells but that their functions do not completely overlap.Keywords:
Phospholipase D
Wild type
Vicia
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Abstract. Abscisic acid (ABA) is taken up by guard cells of isolated epidermata of Valerianella locusta only at low external pH values. At pH 8.0, when nearly all ABA molecules are present as the union of ABA (ABA − ), no uptake can be observed. ABA‐dependent movement of stomata was tested at external pH values between 5.0 and 8.0. Independent of the external pH, ABA induced stomatal closure at all tested ABA concentrations. It is concluded that ABA need not be taken up into the cytosol of the guard cells in order to induce slomatal closure. The primary site of ABA action at the guard cell plasmalemma must be located either at the outer surface of the plasmalemma or at least be easily accessible from outside. ABA− is as effective as undissociated ABA (ABAH).
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The function and location of guard cells uniquely subject them to stress. First, stomatal movements require large fluctuations in the concentration of potassium salts. Second, guard cell inner walls are the first surfaces exposed to evaporation and apoplastic solutes may accumulate there as a result. We have therefore investigated whether guard cells exhibit atypical expression of dehydrin genes because dehydrins accumulate in vegetative tissues in response to water stress. We have also assayed for osmotin mRNA, which is up‐regulated in leaves in response to various stresses. mRNA probes for several representative genes were used with RNA extracts from control and water‐stressed Vicia faba leaflets. Correlatively, these probes were used with RNA extracts from “isolated’ guard cells that had been incubated with combinations of abscisic acid, mannitol and Ca 2+ . (Isolated guard cells are epidermal strips sonicated to destroy cells other than guard cells.) Hybridization with the probe prepared for a dehydrin from Pisum sativum (Psdhn 1) was detected in leaf extracts only if the leaf had been stressed. Similarly, after 1‐ and 6‐h incubations with abscisic acid, isolated guard cells contained an mRNA that hybridized with the probe for Psdhn 1. Appearance of this abscisic acid‐dependent mRNA required neither mannitol nor exogenous Ca 2+ . Regardless of the conditions or tissue, no hybridization was detected with the probe against osmotin, but our interpretation of this result is qualified. The simplest conclusion is that atypical expression of dehydrin is not the mechanism by which guard cells cope with their peculiar function and location.
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Guard (computer science)
Leakage (economics)
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The plant hormone abscisic acid (ABA) is actively synthesized in vascular tissues and transported to guard cells to promote stomatal closure. Although several transmembrane ABA transporters have been identified, how the movement of ABA within plants is regulated is not fully understood. In this study, we determined that Arabidopsis NPF4.6, previously identified as an ABA transporter expressed in vascular tissues, is also present in guard cells and positively regulates stomatal closure in leaves. We also found that mutants defective in NPF5.1 had a higher leaf surface temperature compared to the wild type. Additionally, NPF5.1 mediated cellular ABA uptake when expressed in a heterologous yeast system. Promoter activities of NPF5.1 were detected in several leaf cell types. Taken together, these observations indicate that NPF5.1 negatively regulates stomatal closure by regulating the amount of ABA that can be transported from vascular tissues to guard cells.
Vascular tissue
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Of the many physiological processes that abscisic acid affects in plants, movement of guard cells is a particularly important one. By opening and closing stomata, the guard cells regulate water loss or retention through transpiration. Li et al. have now identified a component of the abscisic acid signaling cascade that is specific to guard cell action. The protein AAPK (abscisic acid-activated serine-threonine protein kinase), the gene for which has now been cloned from Vicia faba, responds through auto- and transphosphorylation to abscisic acid and is required for guard cell response to abscisic acid signals. Li, J., Wang, X.Q., Watson, M.B., and Assmann, S.M. (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287 : 300-303. [Abstract] [Full Text]
Strigolactone
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Twenty analogues of abscisic acid have been tested for their activity as inhibitors of stomatal opening in isolated epidermis of Commelina communis. A number of derivatives showed slight activity but only two treatments resulted in significant stomatal closure and this was accompanied by destruction of the guard cell membranes. Such damage is characteristic of the stomatal response to farnesol, another sesquiterpenoid also thought to be involved in control of water loss. The implication of these results in the study of antitranspirants is considered.
Epidermis (zoology)
Commelinaceae
Water Stress
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Of the many physiological processes that abscisic acid affects in plants, movement of guard cells is a particularly important one. By opening and closing stomata, the guard cells regulate water loss or retention through transpiration. Li et al. have now identified a component of the abscisic acid signaling cascade that is specific to guard cell action. The protein AAPK (abscisic acid-activated serine-threonine protein kinase), the gene for which has now been cloned from Vicia faba, responds through auto- and transphosphorylation to abscisic acid and is required for guard cell response to abscisic acid signals.Li, J., Wang, X.Q., Watson, M.B., and Assmann, S.M. (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287: 300-303. [Abstract] [Full Text]
Strigolactone
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