Biologia plantarum 53:53-62, 2009 | DOI: 10.1007/s10535-009-0008-0
Involvement of phospholipase C-independent calcium-mediated abscisic acid signalling during Arabidopsis response to drought
- 1 CEA, DSV, IBEB, Lab. Echanges Membran et Signalisation, Saint-Paul-lez-Durance, France
- 2 CNRS, UMR, Biol. Veget. et Microbiol. Environ., Saint-Paul-lez-Durance, France
- 3 Aix-Marseille Université, Saint-Paul-lez-Durance, France
The present study investigated whether Ca2+ mobilization independent of phosphoinositide-specific phospholipase C (PI-PLC) would delay wilting in Arabidopsis thaliana (L.) Heynh. cv. Columbia through mediating stomatal closure at abscisic acid (ABA) concentrations rising beyond a drought-specific threshold value. In wild type (WT) epidermis, the PI-PLC inhibitor (U73122) affected the stomatal response to 20 µM ABA but not to 30 µM ABA. Disruption in GTP-binding protein ά subunit 1 (GPA1) affected the stomatal response to 30 µM ABA, but not to 20 µM ABA. In the gpa1-4 mutant, the inhibitory effects of the Ca2+ buffer, 1,2-bis(0-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA), the inactive mastoparan analogue, mas17 and the antagonist of cyclic ADP-ribose synthesis, nicotinamide, were differentially attenuated on 30 µM ABA-induced stomatal closure. By contrast, the NADPH oxidase atrbohD/F double mutation fully suppressed inhibition of 20 µM ABA-induced stomatal closure by BAPTA or U73122 as well as inhibition of 30 µM ABA-induced stomatal closure by BAPTA, mas17 or nicotinamide. On the contrary, The Al resistant alr-104 mutation modulated ABA-induced stomatal closure by a stimulatory effect of U73122 and an increased sensitivity to mas17, nicotinamide and BAPTA. Compared to WT, the atrbohD/F double mutant was more hypersensitive than the gpa1-4 mutant to wilting under the tested water stress conditions, whereas wilting was delayed in the alr-104 mutant. Since the atrbohD/F mutation breaks down ABA-induced Ca2+ signalling through fully preventing apoplastic Ca2+ to enter into the guard cells, these results showed that a putative guard cell GPA1-dependent ADP-ribosyl cyclase activity should contribute to drought tolerance within PI-PLC-independent-Ca2+-mediated ABA signalling.
Keywords: ADP-ribosyl cyclase; alr-104 mutation; atrbohD, F double mutation; gpa1-4 mutation; stomatal closure
Subjects: abscisic acid (ABA); Arabidopsis thaliana; calcium; cyclic ADP-ribose; GTP-binding protein; mutagenesis, mutants; NADPH oxidase; nicotinamide; phospholipase; signalling; stomata closure; stomata guard cells; water stress
Received: March 21, 2008; Accepted: December 17, 2008; Published: March 1, 2009 Show citation
References
- 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.
Go to original source... - Blatt, M.R., Armstrong, F.: K+ channels of stomatal guard cells: abscisic-acid-evoked control of the outward rectifier mediated by cytoplasmic pH.-Planta 191: 330-341, 1993.
Go to original source... - Ceni, C., Muller-Steffner, H., Lund, F., Pochon, N., Schweitzer, A., De Waard, M., Schuber, F., Villaz, M., Moutin, M.-J.: Evidence for an intracellular ADP-ribosyl cyclase/NAD+-glycohydrolase in brain from CD38-deficient mice.-J. biol. Chem. 278: 40670-40678, 2003.
Go to original source... - Chen, J.-G., Gao, Y., Jones, A.M.: Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots.-Plant Physiol. 141: 887-897, 2006.
Go to original source... - Cousson, A.: Carbon dioxide and ferricyanide parallel each other to inhibit Commelina stomatal opening in a putative Ca2+-independent fashion.-J. Plant Physiol. 159: 281-291, 2002.
Go to original source... - 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.
Go to original source... - 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.
Go to original source... - Cousson, A.: Two calcium mobilizing pathways implicated within abscisic acid-induced stomatal closing in Arabidopsis thaliana.-Biol. Plant. 51: 285-291, 2007.
Go to original source... - Cousson, A.: Putative primary involvement of Arabidopsis phosphoinositide-specific phospholipase C1 within abscisic acid-induced stomatal closing.-Biol. Plant. 52: 493-501, 2008.
Go to original source... - 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.
Go to original source... - Degenhardt, J., Larsen, P.B., Howell, S.H., Kochian, L.V.: Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH.-Plant Physiol. 117: 19-27, 1998.
Go to original source... - 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.
Go to original source... - Grabov, A., Blatt, M.R.: Parallel control of the inward-rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells.-Planta 201: 84-95, 1997.
Go to original source... - Graeff, R.M., Franco, L., De Flora, A., Lee, H.C.: Cyclic GMP-dependent and-independent effects on the synthesis of the calcium messengers cyclic ADP-ribose and nicotinic acid adenine dinucleotide phosphate.-J. biol. Chem. 273: 118-125, 1998.
Go to original source... - 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.
Go to original source... - 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.
Go to original source... - Kinoshita, T., Nishimura, M., Shimazaki, K-I.: Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of faba bean.-Plant Cell 7: 1333-1342, 1995.
Go to original source... - Kwak, J.M., Mori, I.C., Pei, Z-M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D.G., Schroeder, J.I.: NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.-EMBO J. 22: 2623-2633, 2003.
Go to original source... - Larsen, P.B., Degenhardt, J., Tai, C.Y., Stenzler, L.M., Howell, S.H., Kochian, L.V.: Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots.-Plant Physiol. 117: 9-18, 1998.
Go to original source... - 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.
Go to original source... - 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.
Go to original source... - 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.
Go to original source... - Miles, G.P., Samuel, M.A., Jones, A.M., Ellis, B.E.: Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins.-Plant Physiol 134: 1332-1336, 2004.
Go to original source... - Sanchez, J.-P., Chua, N.-H.: Arabidopsis PLC1 is required for secondary responses to abscisic acid signals.-Plant Cell 13: 1143-1154, 2001.
Go to original source... - Sanchez, J.-P., Duque, P., Chua, N.-H.: ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis.-Plant Cell 38: 381-395, 2004.
Go to original source... - Sanders, D., Pelloux, J., Brownlee, C., Harper, J.F.: Calcium at the crossroads of signaling.-Plant Cell 14(Suppl.): S401-S417, 2002.
Go to original source... - Schulz-Lessdorf, B., Lohse, G., Hedrich, R.: GCAC1 recognizes the pH gradient across the plasma membrane: a pH-sensitive and ATP-dependent anion channel links guard cell membrane potential to acid and energy metabolism.-Plant J. 10: 993-1004, 1996.
Go to original source... - 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.
Go to original source... - Shinozaki, K., Yamaguchi-Shinozaki, K.: Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.-Curr. Opin. Plant Biol. 3: 217-223, 2000.
Go to original source... - Takahashi, S., Katagiri, T., Hirayama, T., Yamaguchi-Shinozaki, K., Shinozaki, K.: Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-triphosphate independent of abscisic acid in Arabidopsis cell culture.-Plant Cell Physiol 42: 214-222, 2001.
Go to original source... - 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.
Go to original source... - 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.
Go to original source... - Wu, Y., Kuzma, J., Maréchal, E., Graeff, R., Lee, H.C., Foster, R., Chua, N.-H.: Abscisic acid signaling through cyclic ADP-ribose in plants.-Science 278: 2126-2130, 1997.
Go to original source...



