Abstract
It was revealed that cGMP is involved in the control of photoperiodic flower induction. Further insight into the signalling function of cGMP is likely to be obtained by analysis of its effectors. Therefore, in the present study, we used various agents that cause changes in cGMP-dependent kinase (PKG) activity and examined their effects on the activity of kinase isolated from Pharbitis nil and flower induction. It was found that exogenous applications of PKG activators (cGMP, 8-pCPT-cGMP, 8-Br-cGMP, 8-pCPT-PET-cGMP) to cotyledons which were exposed to a 12-h-long subinductive night significantly increased flowering response. From among the many antagonists of cGMP-dependent protein kinase Rp-8-Br-PET-cGMPS, Rp-8-pCPT-cGMP and the synthetic heptapeptide inhibitor of PKG were used for our analysis. When Rp-8-Br-PET-cGMPS and Rp-8-pCPT-cGMP were applied during a 16-h-long inductive night, significant reduction in the number of flower buds was observed, whereas synthetic heptapeptide did not change the intensity of flowering. The influence of the analysed chemicals on protein kinase activity was also examined in vitro. With the exception of synthetic heptapeptide, which seems ineffective, the enzyme activity was stimulated by all agonists and significantly reduced by all antagonists. The activity of protein kinase was assayed in P. nil soluble protein fractions from plants grown under flower-inducing and non-inducing conditions. In vitro phosphorylation was slightly greater in the soluble fraction obtained from plants grown under the flower-inducing condition, reaching 1.05 nmol/min/mg protein, when compared to the control 0.81 nmol/min/mg protein. In relation to the results described above, we can conclude that cGMP as a mediator participating in photoperiodic flower induction may govern this process by the phosphorylation mechanism via its influence on cGMP-dependent protein kinase activity.
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References
Balagué C, Lin B, Alcon C, Flottes G, Malmström S, Köhler C et al (2003) HLMI, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15:365–379. doi:10.1105/tpc.006999
Bowler C, Chua NH (1994) Emerging themes of plant signal transduction. Plant Cell 6:1529–1541
Bowler C, Neuhaus G, Yamagata H, Chua NH (1994) Cyclic GMP and calcium mediate phytochrome transduction. Cell 77:73–81. doi:10.1016/0092-8674(94)90236-4
Butt E, Pöhler D, Genieser H-G, Huggins JP, Bucher B (1994) Inhibition of cyclic GMP-dependent protein kinase-mediated effects by (Rp)-8-bromo-PET-cyclic GMPS. Br J Pharmacol 116:3110–3116
Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK, Bent AF (2000) The Arabidopsis dnd1 defense, no death gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97:9323–9328. doi:10.1073/pnas.150005697
Cousson A, Vavasseur A (1998) Putative involvement of Ca2+ and GTP-binding proteins in cyclic-GMP-mediated induction of stomatal opening by auxin in Commelina communis L. Planta 206:308–314. doi:10.1007/s004250050405
Dubovskaya LV, Volotovsky ID (2004) Affinity chromatography isolation and characterization of soluble cGMP-binding proteins from Avena sativa seedlings. Bulg J Plant Physiol 30:14–24
Dubovskaya LV, Molchan OV, Volotovsky ID (2002) Cyclic GMP-binding activity in Avena sativa seedlings. Russ J Plant Physiol 2:216–220. doi:10.1023/A:1014801623322
Friebe A, Koesling D (2003) Regulation of nitric oxide-sensitive guanylyl cyclase. Circ Res 93:96–105. doi:10.1161/01.RES.0000082524.34487.31
Friedrich P, Curvetto N, Giusto N (1999) Cyclic AMP-dependent protein phosphorylation in guard cell protoplasts of Vicia faba L. Biocell 23:203–210
Garcia-Mata C, Gay R, Sokolovsky S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 19:11116–11121. doi:10.1073/pnas.1434381100
Hammond RW, Zhao Y (2000) Characterisation of a tomato protein kinase gene induced by infection by potato spindle tuber viroid. Mol Plant Microbe Interact 13:903–910. doi:10.1094/MPMI.2000.13.9.903
Hasunuma K, Funadera K, Furukawa K, Miyamoto-Shinoyama (1988) Rhythmic oscillation of cyclic 3′, 5′-guanosine monophosphate concentration and stimulation of flowering by cyclic GMP in Lemna paucicostata. Photochem Photobiol 48:89–92
Hasunuma K, Ogura Y, Yabe N (1998) Early events occurring during light signal transduction in plant and fungi. J Photosci 5:73–81
Hofmann F (2005) The biology of cyclic nucleotide-dependent protein kinases. J Biol Chem 280:1–4
Hood J, Granger HJ (1998) Protein kinase G mediates vascular endothelia growth factor-induced Raf-1 activation and proliferation in human endothelial cells. J Biol Chem 273:23504–23508. doi:10.1074/jbc.273.36.23504
Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670. doi:10.1104/pp.104.054494
Jaworski K, Szmidt-Jaworska A, Tretyn A, Kopcewicz J (2003) Biochemical evidence for calcium-dependent protein kinase from Pharbitis nil and its involvement in photoperiodic flower induction. Phytochemistry 62:1047–1055. doi:10.1016/S0031-9422(02)00677-5
Jaworski K, Szmidt-Jaworska A, Tretyn A, Kopcewicz J (2004) Calmodulin from Pharbitis nil: purification and characterization. Biol Plant 48:55–60. doi:10.1023/B:BIOP.0000024275.66196.d9
Kato R, Uno I, Ishikawa T, Fujii T (1993) Effect of cAMP on the activity of soluble protein kinases in Lemna paucicostata. Plant Cell Physiol 24:841–848
Knight H, Knight MR (2001) Abiotic stress signaling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267. doi:10.1016/S1360-1385(01)01946-X
Komatsu S, Hirano H (1993) Protein kinase activity and protein phosphorylation in rice (Oryza sativa L.) leaf. Plant Sci 94:127–137. doi:10.1016/0168-9452(93)90014-Q
Liu J-Q, Leggewie G, Varotto S (1999) Characterisation of an anther-expressed protein kinase gene in the potato Solanum berthaultii and its antisense inhibition in transgenic plants. Sex Plant Reprod 11:336–346. doi:10.1007/s004970050161
Liu P, Meng L-J, Zhang H-X, Chen J, Wang X-C (2002) Involvement of cAMP in ABA signal transduction in tobacco suspension cells. Acta Bot Sin 44:1432–1437
Maathuis FJ (2006) cGMP modulates gene transcription and cation transport in Arabidopsis roots. Plant J 45:700–711. doi:10.1111/j.1365-313X.2005.02616.x
Maathuis FJ, Sanders D (2001) Sodium uptake in Arabidopsis root is regulated by cyclic nucleotides. Plant Physiol 127:1617–1625. doi:10.1104/pp.127.4.1617
Murad F (1994) Cyclic GMP: synthesis, metabolism and function. In: Murad F (ed) Advances in pharmacology, vol 26. Academic Press Inc, San Diego, California
Navazio L, Mariani P, Sanders D (2001) Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 125:2129–2138. doi:10.1104/pp.125.4.2129
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35. doi:10.1046/j.1469-8137.2003.00804.x
Newton RP, Smith CJ (2004) Cyclic nucleotides. Phytochemistry 65:2423–2437. doi:10.1016/j.phytochem.2004.07.026
Penson SP, Schuurink RC, Fath A, Gubler F, Jacobsen JV, Jones RL (1996) cGMP is required for gibberellic acid-induced gene expression in barley aleurone. Plant Cell 8:2325–2333
Prado AM, Porterfield DM, Feijo JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714. doi:10.1242/dev.01153
Rabkin SW, Klassen SS, Tsang MY (2007) Sodium nitroprusside activates p38 mitogen activated protein kinase through a cGMP/PKG independent mechanism. Life Sci 81:640–646. doi:10.1016/j.lfs.2007.06.022
Schaap P (2005) Guanylyl cyclases across the tree of life. Front Biosci 10:1485–1498. doi:10.2741/1633
Schuurink RC, Shartzer SF, Fath A, Jones RL (1998) Characterization of calmodulin-binding transporter from the plasma membrane of barley aleurone. Proc Natl Acad Sci USA 95:1944–1949. doi:10.1073/pnas.95.4.1944
Schwede F, Maronde E, Genieser H-G, Jastorff B (2000) Cyclic nucleotide analogs as biochemical tools and prospective drugs. Pharmacol Ther 87:199–226. doi:10.1016/S0163-7258(00)00051-6
Sharma VK, Jain PK, Maheshwari SC, Khurana JP (1999) Changes in phosphorylation status of wheat plastid polypeptide are influenced by light, calcium and cAMP. J Plant Biochem Biotechnol 8:87–92
Stern JH, Kaupp UB, MacLeish PR (1986) Control of the light-regulated current in rod photoreceptors by cyclic GMP, calcium and l-cis-diltiazem. Proc Natl Acad Sci USA 83:1163–1167. doi:10.1073/pnas.83.4.1163
Szmidt-Jaworska A, Jaworski K, Tretyn A, Kopcewicz J (2003) Biochemical evidence for a cGMP-regulated protein kinase in Pharbitis nil. Photochemistry 63:635–642. doi:10.1016/S0031-9422(03)00247-4
Szmidt-Jaworska A, Jaworski K, Tretyn A, Kopcewicz J (2004) The involvement of cyclic GMP in photoperiodic flower induction of Pharbitis nil. J Plant Physiol 161:277–284. doi:10.1078/0176-1617-01122
Szmidt-Jaworska A, Jaworski K, Kopcewicz J (2006) The involvement of cyclic ADPR in photoperiodic flower induction of Pharbitis nil. J Plant Growth Regul 25:233–244. doi:10.1007/s00344-006-0015-8
Szmidt-Jaworska A, Jaworski K, Kopcewicz J (2008) The involvement of cyclic GMP in phytochrome-controlled flowering of Pharbitis nil. J Plant Physiol 165:858–867. doi:10.1016/j.jplph.2007.02.010
Talke IN, Blaudez D, Maathuis FJ, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293. doi:10.1016/S1360-1385(03)00099-2
Thomas B (2006) Light signals and flowering. J Exp Bot 13:3387–3393. doi:10.1093/jxb/erl071
Thomas B, Vince-Prue D (1996) Photoperiodism in plants. Academic Press, London
Tretyn A, Czaplewska J, Cymerski M, Kopcewicz J, Kendrick RE (1994) The mechanism of calcium action on flower induction in Pharbitis nil. J Plant Physiol 144:562–568
Tretyn A, Łukaszewska H, Kopcewicz J, Oleńczuk A, Nowakowska A (1997) The role of cotyledons in photoperiodic flower induction of Pharbitis nil. In: Greppin H, Penel C, Simon P (eds) Traveling Shot on Plant Development. Uni Geneva Press, Geneva, pp 51–62
Vallad G, Rivkin M, Vallejos C, McClean P (2001) Cloning and homology modelling of a Pto-like protein kinase family of common bean (Phaseolus vulgaris L). Theor Appl Genet 103:1046–1058. doi:10.1007/s001220100705
Vince-Prue D (1994) The duration of light and photoperiodic responses. In: Kendrick RE, Kronenberg GHM (eds) Photomorphogenesis in plants. Kluwer Acad. Publ, Dordrecht
Vince-Prue D, Gressel J (1985) Pharbitis nil. In: Halevy AH (ed) Handbook of flowering, vol IV. CRS Press Inc, Boca Raton, Florida, pp 47–81
Yuan Q, Ouyang S, Liu J, Suh B, Cheung F, Sultana R et al (2003) The TIGR rice genome annotation resource: annotating the rice genome and creating resource for plant biologists. Nucleic Acids Res 31:229–233. doi:10.1093/nar/gkg059
Zhao J, Guo YQ, Fujita K, Sakai K (2004) Involvement of cAMP signalling in elicitor-induced phytoalexin accumulation in Cupressus lusitanica cell cultures. New Phytol 161:723–733. doi:10.1111/j.1469-8137.2004.00976.x
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Szmidt-Jaworska, A., Jaworski, K. & Kopcewicz, J. Cyclic GMP stimulates flower induction of Pharbitis nil via its influence on cGMP regulated protein kinase. Plant Growth Regul 57, 115–126 (2009). https://doi.org/10.1007/s10725-008-9326-z
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DOI: https://doi.org/10.1007/s10725-008-9326-z