Skip to main content
NCBI home page
Plant Physiology logoLink to Plant Physiology
. 1992 Aug;99(4):1416–1421. doi: 10.1104/pp.99.4.1416

Involvement of Calmodulin and Calmodulin-Dependent Myosin Light Chain Kinase in Blue Light-Dependent H+ Pumping by Guard Cell Protoplasts from Vicia faba L. 1

Ken-ichiro Shimazaki 1,2, Toshinori Kinoshita 1,2, Mitsuo Nishimura 1,2
PMCID: PMC1080641  PMID: 16669053

Abstract

Signal transduction processes involved in blue light-dependent proton pumping were investigated using guard cell protoplasts from Vicia faba. N-[2-(Methylamino)ethyl]-5-isoquinolinesulfonamide, an inhibitor of cyclic AMP- and cyclic GMP-dependent protein kinases, had no effect. 1-(5-Isoquinolinesulfonyl)-2-methylpiperazine (H-7) and calphostin C, inhibitors of protein kinase C, produced slight inhibition of the blue light-dependent proton pumping. 1-[N, O-Bis(5-isoquinolinesulfonyl)-N-methyl-l-tyrosyl] -4-phenylpiperazine, a specific inhibitor of Ca2+/calmodulin (CaM)-dependent protein kinase II, did not inhibit the proton pumping, but 1-(5-iodonaphthalene-1-sulfonyl)-1H-hexahydro-1,4-diazepine and 1-(5-chloro-naphthalene-1-sulfonyl)-1H-hexahydro-1,4-diazepine (ML-9), inhibitors of Ca2+/CaM-dependent myosin light chain kinase, strongly suppressed the proton pumping. A CaM antagonist, N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide (W-7), inhibited blue light-dependent proton pumping, whereas its less active structural analog, N-(6-aminohexyl)-1-naphthalenesulfonamide (W-5), had little effect on the response. Other CaM antagonists, trifluoperazine, compound 48/80, prenylamine, and 3-(2-benzothiazolyl)-4,5-dimethoxy-N-[3-(4-phenyl-piperidinyl)- propylbenzenesulfonamide inhibited the proton pumping. In accord with these results, light-induced stomatal opening in the epidermis of Commelina benghalensis ssp. was inhibited by ML-9 and W-7, but not by H-7 and W-5. Thus, it is concluded that CaM and Ca2+/CaM-dependent myosin light chain kinase are the components of the signal transduction process in blue light-dependent proton pumping in guard cells.

Full text

PDF
1416

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adelstein R. S., Eisenberg E. Regulation and kinetics of the actin-myosin-ATP interaction. Annu Rev Biochem. 1980;49:921–956. doi: 10.1146/annurev.bi.49.070180.004421. [DOI] [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  3. Blatt M. R., Thiel G., Trentham D. R. Reversible inactivation of K+ channels of Vicia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate. Nature. 1990 Aug 23;346(6286):766–769. doi: 10.1038/346766a0. [DOI] [PubMed] [Google Scholar]
  4. Braam J., Davis R. W. Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell. 1990 Feb 9;60(3):357–364. doi: 10.1016/0092-8674(90)90587-5. [DOI] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  6. Gilroy S., Fricker M. D., Read N. D., Trewavas A. J. Role of Calcium in Signal Transduction of Commelina Guard Cells. Plant Cell. 1991 Apr;3(4):333–344. doi: 10.1105/tpc.3.4.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gilroy S., Read N. D., Trewavas A. J. Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature. 1990 Aug 23;346(6286):769–771. doi: 10.1038/346769a0. [DOI] [PubMed] [Google Scholar]
  8. Harper J. F., Sussman M. R., Schaller G. E., Putnam-Evans C., Charbonneau H., Harmon A. C. A calcium-dependent protein kinase with a regulatory domain similar to calmodulin. Science. 1991 May 17;252(5008):951–954. doi: 10.1126/science.1852075. [DOI] [PubMed] [Google Scholar]
  9. Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry. 1984 Oct 9;23(21):5036–5041. doi: 10.1021/bi00316a032. [DOI] [PubMed] [Google Scholar]
  10. Hidaka H., Yamaki T., Naka M., Tanaka T., Hayashi H., Kobayashi R. Calcium-regulated modulator protein interacting agents inhibit smooth muscle calcium-stimulated protein kinase and ATPase. Mol Pharmacol. 1980 Jan;17(1):66–72. [PubMed] [Google Scholar]
  11. Iino M., Ogawa T., Zeiger E. Kinetic properties of the blue-light response of stomata. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8019–8023. doi: 10.1073/pnas.82.23.8019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kanamori M., Naka M., Asano M., Hidaka H. Effects of N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide and other calmodulin antagonists (calmodulin interacting agents) on calcium-induced contraction of rabbit aortic strips. J Pharmacol Exp Ther. 1981 May;217(2):494–499. [PubMed] [Google Scholar]
  13. Kawamoto S., Hidaka H. 1-(5-Isoquinolinesulfonyl)-2-methylpiperazine (H-7) is a selective inhibitor of protein kinase C in rabbit platelets. Biochem Biophys Res Commun. 1984 Nov 30;125(1):258–264. doi: 10.1016/s0006-291x(84)80362-9. [DOI] [PubMed] [Google Scholar]
  14. Kobayashi E., Nakano H., Morimoto M., Tamaoki T. Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun. 1989 Mar 15;159(2):548–553. doi: 10.1016/0006-291x(89)90028-4. [DOI] [PubMed] [Google Scholar]
  15. Lee Y., Assmann S. M. Diacylglycerols induce both ion pumping in patch-clamped guard-cell protoplasts and opening of intact stomata. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2127–2131. doi: 10.1073/pnas.88.6.2127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  17. Saitoh M., Ishikawa T., Matsushima S., Naka M., Hidaka H. Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem. 1987 Jun 5;262(16):7796–7801. [PubMed] [Google Scholar]
  18. Schroeder J. I., Hagiwara S. Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9305–9309. doi: 10.1073/pnas.87.23.9305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schroeder J. I., Raschke K., Neher E. Voltage dependence of K channels in guard-cell protoplasts. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4108–4112. doi: 10.1073/pnas.84.12.4108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sharkey T. D., Raschke K. Effect of Light Quality on Stomatal Opening in Leaves of Xanthium strumarium L. Plant Physiol. 1981 Nov;68(5):1170–1174. doi: 10.1104/pp.68.5.1170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tanaka T., Umekawa H., Saitoh M., Ishikawa T., Shin T., Ito M., Itoh H., Kawamatsu Y., Sugihara H., Hidaka H. Modulation of calmodulin function and of Ca2+-induced smooth muscle contraction by the calmodulin antagonist, HT-74. Mol Pharmacol. 1986 Mar;29(3):264–269. [PubMed] [Google Scholar]
  22. Tokumitsu H., Chijiwa T., Hagiwara M., Mizutani A., Terasawa M., Hidaka H. KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazi ne, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem. 1990 Mar 15;265(8):4315–4320. [PubMed] [Google Scholar]

Articles from Plant Physiology are provided here courtesy of Oxford University Press

RESOURCES