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Putative primary involvement of Arabidopsis phosphoinositide-specific phospholipase C1 within abscisic acid-induced stomatal closing

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Biologia Plantarum

Abstract

Stomatal closing to abscisic acid (ABA) was studied in leaf epidermal peels of a dexamethasone (Dex)-inducible transgenic line expressing the phospholipase C AtPLC1 antisense in the Columbia genetic background. In the absence of Dex, the Ca2+ buffer, ethylene glycol-bis(b-aminoethyl ether)-N,N,N′,N′-tetraacetic acid (EGTA) and the phopholipase C inhibitor, 1-[6-{[17β-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl]-1H-pyrrole-2,5-dione (U73122) specifically inhibited the response to 20 µM ABA, whereas the Ca2+ buffer, 1,2-bis(o-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid (BAPTA) inhibited the response to 20 or 30 µM ABA. Neither EGTA nor BAPTA increased the U73122 effect. Applying 30 µM Dex specifically affected 20 µM ABA-induced stomatal closing through reducing its magnitude as well as suppressing the EGTA, BAPTA and U73122 inhibitory effects. Neither Dex nor U73122 changed the specific inhibitory effects of both the antagonist of cyclic ADP-ribose synthesis, nicotinamide and the GTP-binding protein (G protein) modulators, pGlu-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH2 (GP Ant-2) and mas17 on 30 µM ABA-induced stomatal closing. When tested in combination, substituting nicotinamide for mas17, but not for GP Ant-2, enhanced their inhibitory effect to an extent that BAPTA did not increase. These results supported that AtPLC1 primarily mediates the Ca2+-dependent stomatal closing response to 20 µM ABA as much as 30 µM Dex did not affect 20 µM ABA-induced stomatal closing when tested on the wild type Columbia-4 ecotype. Furthermore, the present study suggested that Ca2+ mobilization did not involve any dependency between AtPLC1 and a putative G protein-coupled ADP-ribosyl cyclase at the tested ABA concentrations.

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Abbreviations

ABA:

abscisic acid

ARC:

ADP-ribosyl cyclase

BAPTA:

1,2-bis(o-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid

cADPR:

cyclic ADP-ribose

Dex:

dexamethasone

EGTA:

ethylene glycol-bis(b-aminoethyl ether)-N,N,N′,N′-tetraacetic acid

GP Ant-2:

pGlu-Gln-D-Trp-Phe-D-Trp-D-Trp-Met-NH2

G protein:

GTP-binding protein

Gα:

G protein α subunit

IP3 :

inositol 1,4,5-triphosphate

PI-PLC:

phosphoinositide-specific phospholipase C

U73122:

1-[6-{[17β-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl]-1H-pyrrole-2,5-dione

U73343:

1-[6-{[17β-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl]-2,5-pyrrolidine-dione

7TMS:

seven-transmembrane-span

References

  • Aoyama, T., Chua, N.-H.: A glucocorticoid-mediated transcriptional induction system in transgenic plants.-Plant J. 11: 605–612, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Apone, F., Alyeshmerni, N., Wiens, K., Chalmers, D., Chrispeels, M.J., Colucci, G.: The G-protein-coupled receptor GCR1 regulates DNA synthesis through activation of phosphatidylinositol-specific phospholipase C.-Plant Physiol. 133: 571–579, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Armstrong, F., Blatt, M.R.: Evidence for K+ channel control in Vicia guard cells coupled by G-proteins to a 7TMS receptor mimetic. Plant J. 8: 187–198, 1995.

    Article  CAS  Google Scholar 

  • Assmann, S.M.: Heterotrimeric and unconventional GTP binding proteins in plant cell signaling.-Plant Cell 14(Suppl.): S355–S373, 2002.

    PubMed  CAS  Google Scholar 

  • Bähner, M., Sander, P., Paulsen, R., Huber, A.: The visual G protein of fly photoreceptors interacts with the PDZ domain assembled INAD signaling complex via direct binding of activated Gαq to phospholipase C\( \tilde \beta \). -J. biol. Chem. 275: 2901–2904, 2000.

    Article  PubMed  Google Scholar 

  • Burnette, R.N., Gunesekera, B.M., Gillaspy, G.E.: An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling.-Plant Physiol. 132: 1011–1019, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Colucci, G., Apone, F., Alyeshmerni, N., Chalmers, D., Chrispeels, M.J.: GCR1, the putative Arabidopsis G protein-coupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering.-Proc. nat. Acad. Sci. USA 99: 4736–4741, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Cousson, A.: Pharmacological study of two potential Ca2+ signalling pathways within stomatal closing in response to abscisic acid in Commelina communis L.-Plant Sci. 145: 67–74, 1999.

    Article  CAS  Google Scholar 

  • Cousson, A.: Two potential Ca2+-mobilising processes depend on the abscisic acid concentration and growth temperature in the Arabidopsis stomatal guard cell.-J. Plant Physiol. 160: 493–501, 2003a.

    Article  PubMed  CAS  Google Scholar 

  • Cousson, A.: Pharmacological evidence for a positive influence of the cyclic GMP-independent transduction on the cyclic GMP-mediated Ca2+-dependent pathway within Arabidopsis stomatal opening in response to auxin.-Plant Sci. 164: 759–767, 2003b.

    Article  CAS  Google Scholar 

  • Cousson, A.: Two calcium mobilizing pathways implicated within abscisic acid-induced stomatal closing in Arabidopsis thaliana.-Biol. Plant. 51: 285–291, 2007.

    Article  CAS  Google Scholar 

  • Cousson, A., Vavasseur, A.: Two potential Ca2+-dependent transduction pathways in stomatal closing in response to abscisic acid.-Plant Physiol. Biochem. 36: 257–262, 1998.

    Article  CAS  Google Scholar 

  • Essen, L-O., Perisic, O., Cheung, R., Katan, M., Williams, R.L.: Crystal structure of a mammalian phosphoinositide-specific phospholipase Cδ.-Nature 380: 595–602, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Galione, A.: Cyclic ADP-ribose, the ADP-ribosyl cyclase and calcium signalling.-Mol. cell. Endocrinol. 98: 125–131, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Gilroy, S., Read, N.D., Trewavas, A.J.: Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure.-Nature 346: 769–771, 1990.

    Article  PubMed  CAS  Google Scholar 

  • Hajdukiewicz, P., Svab, Z., Maliga, P.: The small, versatile pPZP family of Agrobacterium vectors for plant transformation.-Plant. mol. Biol. 25: 989–994, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Higashida, H., Egorova, A., Higashida, C., Zhong, Z.-G., Yokoyama, S., Noda, M., Zhang, J.-S.: Sympathetic potentiation of cyclic ADP-ribose formation in rat cardiac myocytes.-J. biol. Chem. 274: 33348–33354, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Higashijima, T., Burnier, J., Ross, E.M.: Regulation of Gi and Go by mastoparan, related amphiphilic peptides, and hydrophobic amines. Mechanism and structural determinants of activity.-J. biol. Chem. 265: 14176–14186, 1990.

    PubMed  CAS  Google Scholar 

  • Hirayama, T., Ohto, C., Mizoguchi, T., Shinozaki, K.: A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana.-Proc. nat. Acad. Sci. USA 92: 3903–3907, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, L., Mills, L.N., Pical, C., Leckie, C.P., Aitken, F.L., Kopka, J., Mueller-Roeber, B., McAinsh, M.R., Hetherington, A.M., Gray, J.E.: Phospholipase C is required for the control of stomatal aperture by ABA.-Plant J. 34: 47–55, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Ishige, F., Takaishi, M., Foster, R., Chua, N.-H., Oeda, K.: A G-box motif (GCCACGTGCC) tetramer confers high levels of constitutive expression in dicot and monocot.-Plant J. 18: 443–448, 1999.

    Article  CAS  Google Scholar 

  • Kelly, W.B., Esser, J.E., Schroeder, J.I.: Effects of cytosolic calcium and limited, possible dual, effects of G protein modulators on guard cell inward potassium channels.-Plant J. 8: 479–489, 1995.

    Article  CAS  Google Scholar 

  • Larsen, P.B., Tai, C.Y., Kochian, L.V., Howell, S.H.: Arabidopsis mutants with increased sensitivity to aluminum.-Plant Physiol. 110: 743–751, 1996.

    Article  PubMed  CAS  Google Scholar 

  • Leckie, C.P., McAinsh, M.R., Allen, G.J., Sanders, D., Hetherington, A.M.: Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose.-Proc. nat. Acad. Sci. USA 95: 15837–15842, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Lee, Y., Assmann, S.M.: Diacylglycerols induce both ion pumping in patch-clamped guard cell protoplasts and opening of intact stomata.-Proc. nat. Acad. Sci. USA 88: 2127–2131, 1991.

    Article  PubMed  CAS  Google Scholar 

  • Leymarie, J., Lascève, G., Vavasseur, A.: Interaction of stomatal responses to ABA and CO2 in Arabidopsis thaliana.-Aust. J. Plant Physiol. 25: 785–791, 1998.

    Article  CAS  Google Scholar 

  • Lin, Y.F., Tseng, M.J., Hsu, H.L., Wu, Y.W., Lee, Y.H., Tsai, Y.H.: A novel follicle-stimulating hormone-induced G alpha h/phospholipase C delta 1 signaling pathway mediating rat sertoli cell Ca2+-influx.-Mol. Endocrinol. 20: 2514–2527, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Macrez-Leprêtre, N., Morel, J.-L., Mironneau, J.: Effects of phospholipase C inhibitors on Ca2+ channel stimulation and Ca2+ release from intracellular stores evoked by α1A-and α2A-adrenoceptors in rat portal vein myocytes.-Biochem. biophys. Res. Commun. 218: 30–34, 1996.

    Article  PubMed  Google Scholar 

  • Mueller-Roeber, B., Pical, C.: Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C.-Plant Physiol. 130: 22–46, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Mukai, H., Munekata, E., Higashijima, T.: G protein antagonists: a novel hydrophobic peptide competes with receptor for G protein binding.-J. biol. Chem. 267: 16237–16243, 1992.

    PubMed  CAS  Google Scholar 

  • Otterhag, L., Sommarin, M., Pical, C.: N-terminal EF-hand-like domain is required for phosphoinositide-specific phospholipase C activity in Arabidopsis thaliana.-FEBS lett. 497: 165–170, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Pandey, S., Assmann, S.M.: The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein α subunit GPA1 and regulates abscisic acid signaling.-Plant Cell 16: 1616–1632, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez, J.-P., Chua, N.-H.: Arabidopsis PLC1 is required for secondary responses to abscisic acid signals.-Plant Cell 13: 1143–1154, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez, J.-P., Duque, P., Chua, N.-H.: ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis.-Plant J. 38: 381–395, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Sanders, D., Pelloux, J., Brownlee, C., Harper, J.F.: Calcium at the crossroads of signaling.-Plant Cell 14(Suppl.): S401–S417, 2002.

    PubMed  CAS  Google Scholar 

  • Sethi, J.K., Empson, R.M., Galione, A.: Nicotinamide inhibits cyclic ADP-ribose-mediated calcium signalling in sea urchin eggs.-Biochem. J. 319: 613–617, 1996.

    PubMed  CAS  Google Scholar 

  • Staxen, I., Pical, C., Montgomery, L.T., Gray, J.E., Hetherington, A.M., McAinsh, M.R.: Abscisic acid induces oscillations in guard cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C.-Proc. nat. Acad. Sci. USA 96: 1779–1784, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Takenouchi, T., Ogihara, K., Sato, M., Kitani, H.: Inhibitory effects of U73122 and U73343 on Ca2+ influx and pore formation induced by the activation of P2X7 nucleotide receptors in mouse microglial cell line.-Biochim. biophys. Acta. 1726: 177–186, 2005.

    PubMed  CAS  Google Scholar 

  • Thompson, A.K., Mostafapour, S.P., Denlinger, L.C., Bleasdale, J.E., Fisher, S.K.: The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. A role for Gp in receptor compartmentation.-J. biol. Chem. 266: 23856–23862, 1991.

    PubMed  CAS  Google Scholar 

  • Wang, X.-Q., Ullah, H., Jones, A.M., Assmann, S.M.: G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells.-Science 292: 2070–2072, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki, K., Shinozaki, K.: A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress.-Plant Cell 6: 251–264, 1994.

    Article  PubMed  CAS  Google Scholar 

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Cousson, A. Putative primary involvement of Arabidopsis phosphoinositide-specific phospholipase C1 within abscisic acid-induced stomatal closing. Biol Plant 52, 493–501 (2008). https://doi.org/10.1007/s10535-008-0096-2

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