Biopolym. Cell. 2008; 24(6):441-452.
http://dx.doi.org/10.7124/bc.0007BC
Огляди
Молекулярні основи реалізації сигнального шляху фосфатидилінозитол-специфічної фосфоліпази С у клітинах рослин
1Яковенко О. М., 1Кретинін С. В., 1Кравець В. С.
  1. Інститут біоорганічної хімії та нафтохімії НАН України
    вул. Мурманська, 1, Київ, Україна, 02094

Abstract

Сигнали довкілля можуть сприйматися та посилюватися в клітинах завдяки сигнальним каскадам. У рослин фосфатидилінозитол-специфічна фосфоліпаза С (ФЛС) виконує важливу роль у клітинній відповіді на зовнішні стимули. Субстрат та продукти цього ферменту регулюють численні процеси в клітинах рослин. В огляді зосереджено увагу на молекулярних основах реалізації сигнального шляху фосфатидилінозитол- специфічної ФЛС. Аналіз даних може доповнити уявлення про механізми, що лежать в основі здатності рослин реагувати на різноманітні абіотичні та біотичні стреси.
Keywords: фосфатидилінозитол-специфічна фосфоліпаза С, трансдукція сигналу
Повний текст: (PDF, російською) (PDF, англійською)

References

[1] Meijer H. J. G., Munnik T. Phospholipid-based signaling in plants Annu. Rev. Plant Biol 2003 54:265–306.
[2] 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 1995 92, N 9:3903–3907.
[3] DeWald D. B., Torabinejad J., Jones C. A., Shope J. C., Cangelosi A. R., Thompson J. E., Prestwich G. D., Hama H. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis Plant Physiol 2001 126, N 2 P. 759–769.
[4] Smolenska-Sym G., Kacperska A. Inositol 1,4,5-trisphosphate formation in leaves of winter oilseed rape plants in response to freezing, tissue water potential and abscisic acid Physiol. Plant 1996 96, N 4:692–698.
[5] Vergnolle C., Vaultier M.-N., Taconnat L., Renou J.-P., Kader J.-C., Zachowski A., Ruelland E. The cold-induced early activation of phospholipases C and D pathways determines the response of two distinct clusters of genes in Arabidopsis suspension cell Plant Physiol 2005 139, N 3:1217–1233.
[6] Takahashi S., Katagiri T., Hirayama T., Yamaguchi-Shinozaki K., Shinozaki K. Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture Plant Cell Physiol 2001 42, N 2:214–222.
[7] Kim Y. J., Kim J. E., Lee J.-H., Lee M. H., Jung H. W., Bahk Y. Y., Hwang B. K., Hwang I., Kim W. T. The Vr-PLC3 gene encodes a putative plasma membrane-localized phosphoinositide-speciWc phospholipase C whose expression is induced by abiotic stress in mung bean (Vigna radiata L.) FEBS Lett 2004 556, N 1–3:127–136.
[8] Zonia L., Munnik T. Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes Plant Physiol 2004 134, N 2 P. 813–823.
[9] Das S., Hussain A., Bock C., Keller W. A., Georges F. Cloning of Brassica napus phospholipase C2 (BnPLC2), phosphatidylinositol 3-kinase (BnVPS34) and phosphatidylinositol synthase1 (BnPtdIns S1) – comparative analysis of the effect of abiotic stresses on the expression of phosphatidylinositol signal transduction-related genes in B. napus Planta 2005 220, N 5:777–784.
[10] Assmann S. M., Shimazaki K. The multisensory guard cell. Stomatal response to blue light and abscisic acid Plant Physiol 1999 119, N 3:809–815.
[11] Staxen I., Pical C., Montgomery L. T., Gray J. E., Hetherington A. M., McAinsh M. R. Abscisic acid induces phosphoinositide-specific phospholipase C-dependent oscillations in guard cell cytosolic free calcium Proc. Nat. Acad. Sci. USA 1999 96, N 4:1779–1784.
[12] Repp A., Mikami K., Mittmann F., Hartmann E. Phosphoinositide specific phospholipase C is involved in cytokinin and gravity responses in the moss Physcomitrella patens Plant J 2004 40, N 2 P. 250–259.
[13] Leeuwen W., Vermeer J. E. M., Theodorus W. J., Gadella Jr., Munnik T. Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings Plant J 2007 52, N 6:1014–1026.
[14] Alexander J., Lassalles J. P., Kado R. T. Opening of Ca2+ channels in isolated red beet root vacuole membrane by inositol 1,4,5-trisphosphate Nature 1990 343:567–570.
[15] Lemtir-Chlieh F., MacRobbie E. A. C., Webb A. A. R., Manison N. F., Brownlee C., Skepper J. N., Chen J., Prestwich G., Brearley C. A. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells Proc. Nat. Acad. Sci. USA 2003 100, N 17:10091–10095.
[16] Munnik T., Meijer H. J. G. Osmotic stress activates distinct lipid and MAPK signalling pathways in plants FEBS Lett 2001 498, N 2–3:172–178.
[17] Testerink C, Munnik T. Phosphatidic acid: a multifunctional stress signaling lipid in plants Trends Plant Sci 2005 10, N 8:368–375.
[18] Brearley C. A., Hanke D. E. Inositol phosphates in barley (Hordeum vulgare L.) aleurone tissue are stereochemically similar to the products of breakdown of InsP6 in vitro by wheatbran phytase Biochem. J 1996 318, N 1:279–286.
[19] Perera I. Y., Hung C. Y., Brady S., Muday G. K., Boss W. F. A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism Plant Physiol 2006 140, N 2:746–760.
[20] Yamaguchi-Shinozaki K., Shinozaki K. Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants Mol. Genet. and Genom 1993 236, N 2–3:331–340.
[21] Horowitz L. F., Hirdes W., Suh B. C., Hilgemann D. W., Mackie K., Hille B. Phospholipase C in living cells: activation, inhibition, Ca requirement and regulation of M current J. Gen. Physiol 2005 126, N 3:243–262.
[22] Hunt L., Otterhag L., Lee J. C., Lasheen T., Hunt J., Seki M., Shinozaki K., Sommarin M., Gilmour D. J., Pical C., Gray J. E. Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms New Phytologist 2004 162, N 3:643–654.
[23] Mills L. N., Hunt L., Leckie C. P., Aitken F. L., Wentworth M., McAinsh M. R., Gray J. E., Hetherington A. M. The effects of manipulating phospholipase C on guard cell ABA-signalling J. Exp. Biol 2004 55, N 395:199–204.
[24] 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 2003 34, N 1:47– 55.
[25] Rebecchi M. J., Pentyala S. N. Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev. 2000;80(4):1291-335.
[26] Cao Z., Zhang J., Li Y., Xu X., Liu G., Madan K.B., Yang H., Ren D. Preparation of polyclonal antibody specific for AtPLC4, an Arabidopsis phosphatidylinositol-specific phospholipase C in rabbits Protein Exp. and Purification 2007 52, N 2:306–312.
[27] Swann L., Larman M. G., Saunders C. M., Lai F. A. The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLC. Reproduction. 2004;127(4):431-9.
[28] 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 2001 497, N 2–3:165–170.
[29] 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 2002 130, N 1:22–46.
[30] Dowd P. E., Coursol S., Skirpan A. L., Kao T. H., Gilroyb S. Petunia phospholipase C1 is involved in pollen tube growth The Plant Cell 2006 18, N 12 P. 1438–1453.
[31] Suh P. G., Ryu S. H., Moon K. H., Suh H. W., Rhee S. G. Cloning and sequence of multiple forms of phospholipase C Cell 1988 54, N 9:161–169.
[32] Shi J., Gonzales R. A., Bhattacharyya M. K. Characterization of a plasma membrane-associated phosphoinositide-specific phospholipase C from soybean Plant J 1995 8, N 3 P. 381–390.
[33] Kopka J., Pical C., Gray J. E., Muller-Rober B. Molecular and enzymatic characterization of three phosphoinosidespecific phospholipase C isoforms from potato Plant Physiol 1998 116, N 1:239–250.
[34] Xu X., Cao Z., Liu G., Bhattacharyya M. K., Ren D. Cloning and expression of AtPLC6, a gene encoding a phosphatidylinositol-specific phospholipase C in Arabidopsis thaliana Chin. Sci. Bull 2004 49:567–573.
[35] Tasma M., Volker B., Steven A. W., Madan K. B. Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana Plant Physiol. and Biochem 2008 46, N 7:627–637.
[36] Hirayama T., Mitsukawa N., Shibata D., Shinozaki K. AtPLC2, a gene encoding phosphoinositide-specific phospholipase C, is constitutively expressed in vegetative and floral tissues in Arabidopsis thaliana Plant Mol. Biol 1997 34, N 1:175–180.
[37] Sanchez J. P., Chua N. H. Arabidopsis PLC1 is required for secondary responses to abscisic acid signals Plant Cell 2001 13:1143–1154.
[38] Wang C. R., Yang A. F., Yue G. D., Gao Q., Yin H.Y., Zhang J.-R. Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize Planta 2008 227, N 5:1127–1140.
[39] Hernarndez-Sotomayor S. M. T., Santos-Briones C. De Los, Munoz-Sanchez J. A., Loyola-Vargas V. M. Kinetic analysis of phospholipase C from Catharanthus roseus transformed roots using different assays Plant Physiol 1999 120, N 4:1075–1081.
[40] Rebecchi M., Boguslavsky V., Boguslavsky L., McLaughlin S. Phosphoinositide-specific phospholipase C-delta1: effect of monolayer surface pressure and electrostatic surface potentials on activity Biochemistry 1992 31, N 51:12748– 12753.
[41] James S. R., Paterson A., Harden T. K., Demel R. A., Downes C. P. Dependence of the activity of phospholipase C on surface pressure and surface composition in phospholipid monolayers and its implications for their regulation Biochemistry 1997 36, N 4:848–855.
[42] James S. R., Paterson A., Harden T. K., Downes C. P. Kinetic analysis of phospholipase C isoforms using phospholipid-detergent mixed micelles J. Biol. Chem 1995 270, N 20:11872–11881.
[43] Hartog M., Verhoef N., Munnik T. Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells Plant Physiol 2003 132, N 1:311–317.
[44] Melin P. M., Pical C., Jergil B., Sommarin M. Polyphosphoinositide phospholipase C in wheat root plasma membranes. Partial purification and characterization Biochim. et Biophys. Acta 1992 1123, N 2:163–169.
[45] Huang C.-H., Tate B. F., Crain R. C., Cote G. G. Mulitple phosphoinositide-specific phospholipases C in oat roots: characterization and partial purification Plant J 1995 8, N 2:257–267.
[46] Munnik T., Arisz S. A., de Vrije T., Musgrave A. G protein activation stimulates phospholipase D signaling in plants Plant Cell 1995 7, N 12:2197–2210.
[47] Colucci G., Apone F., Alyeshmerni N., Chalmers D., Chrispeels M. J. GCR1, the putative Arabidopsis G proteincoupled receptor gene is cell cycle-regulated, and its overexpression abolishes seed dormancy and shortens time to flowering Proc Natl Acad Sci U S A. 2002;99(7):4736-41.
[48] Pandey S., Chen J. G., Jones A. M., Assmann S. M. G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development Plant Physiol 2006 141, N 2:243–256.
[49] 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 2001 292, N 5524:2070–2072.
[50] Ullah H., Chen J. G., Young J. C., Im K. H., Sussman M. R., Jones A. M. Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis Science. 2001;292(5524):2066-9.
[51] Misra S., Wu Y., Venkataraman G., Sopory S. K., Tuteja N. Heterotrimeric G-protein complex and G-protein-coupled receptor from a legume (Pisum sativum): role in salinity and heat stress and cross-talk with phospholipase C Plant J 2007 51, N 4:656–669.
[52] Ortega X., Perez L. M. Participation of the phosphoinositide metabolism in the hypersensitive response of Citrus limon against Alternaria alternate Biol. Res 2001 34, N 1 P. 43–50.
[53] Novotna Z., Valentova O., Martinec J., Feltl T., Nokhrina K. Study of phospholipase D and C in maturing and germinating seeds of Brassica napus Biochem. Soc. Trans 2000 28, N 6:817–818.
[54] Lee Y. C., Suh S. L., Assmann S., Kelleher J., Crain C. Abscisic acid-induced phosphoinositide turnover in guard cells protoplasm of Vicia faba. Plant Physiol. 1996;110(3):987-996.
[55] Martinec J., Feltl T., Scanlon C. H., Lumsden P. J., Machackova I. Subcellular localization of a high affinity binding site for D-myo-inositol-1,4,5-trisphosphate from Chenopodium rubrum Plant Physiol 2000 124, N 1:475–483.
[56] Wu Y., Kuzma J., Marechal E., Graeff R., Lee H. C., Foster R., Chua N. H. Abscisic acid signalling through cyclic ADP-ribose in plants Science 1997 278:2126–2129.
[57] 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 1998 95, N 26:15837–15842.
[58] Navazio L., Bewell M. A., Siddiqua A., Dickinson G. D., Galione A., Sanders D. Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate Proc. Nat. Acad. Sci. USA 2000 97, N 15:8693–8698.
[59] Ng C. K., Carr K., McAinsh M. R., Powell B., Hetherington A. M. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate Nature 2001 410, N 6828:596–599.
[60] McAinsh M. R., Clayton H., Mansfield T. A., Hetherington A. M. Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress Plant Physiol 1996 111, N 4:1031–1042.
[61] Lemtiri-Chlieh F., MacRobbie E. A. C., Brearley C. A. Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells Proc. Nat. Acad. Sci. USA 2000 97, N 15:8687– 8692.
[62] Munnik T., Irvine R. F., Musgrave A. Phospholipid signalling in plants Biochim. et Biophys. Acta 1998 1389, N 3:222–272.
[63] Dasgupta S., Dasgupta D., Chatterjee A., Biswas S., Biswas B. B. Conformational changes in plant Ins(1,4,5)P3 receptor on interaction with different myo-inositol trisphosphates and its effect on Ca2+ release from microsomal fraction and liposomes. Biochem J. 1997;321 ( Pt 2):355-60.
[64] Stevenson J. M., Perera I. Y., Heilmann I., Persson S., Boss W. F. Inositol signaling and plant growth Trends Plant Sci 2000 5, N 8:252–258.
[65] Samanta S., Dalal B., Biswas S., Biswas B. B. Myoinositol tris-phosphate-phytase complex as an elicitor in calcium mobilization in plants Biochem. and Biophys. Res. Communs 1993 191, N 2:427–434.
[66] York J. D., Guo S., Odom A. R., Spiegelberg B. D., Stolz L. E. An expanded view of inositol signaling Adv. Enzyme Regul 2001 41: 57–71.
[67] Drrbak B. K., Watkins P. A. C., Chattaway J. A., Roberts K, Dawson A. P. Metabolism of inositol(1,4,5)trisphosphate by a soluble enzyme fraction from pea (Pisum sativum) roots Plant Physiol 1991 95, N 2:412–419.
[68] Drrbak B. K., Watkins P. A. C. Inositol(1,4,5)trisphosphate production in plant cells-stimulation by the venom peptides, mellitin and mastoparan Biochem. and Biophys. Res. Communs 1994 205, N 1:739–745.
[69] Van der Luit A. H., Piatti T., van Doorn A., Musgrave A., Felix G., Boller T., Munnik T. Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate Plant Physiol 2000 123, N 4:1507–1516.
[70] Munnik T. Phosphatidic acid: an emerging plant lipid second messenger Trends Plant Sci 2001 6, N 5:227–233.
[71] Lee S., Park J., Lee Y. Phosphatidic acid induces actin polymerization by activating protein kinases in soybean cells. Mol Cells. 2003;15(3):313-9.
[72] Sang Y., Cui D., Wang X. Phospholipase D and phosphatidic acid-mediated generation of superoxide in Arabidopsis Plant Physiol 2001 126, N 4:1449–1458.
[73] Farmer P. K., Choi J. H. Calcium and phospholipid activation of a recombinant calcium-dependent protein kinase (DcCPK1) from carrot (Daucus carota L.) Biochim. et Biophys. Acta 1999 1434, N 1:6–17.
[74] Lee Y., Lee Y. Roles of phosphoinositides in regulation of stomatal movements Plant Signaling and Behavior 2008 3, N 4:211–213.
[75] Suh P. G., Ryu S. H., Moon K. H., Suh H. W., Rhee S. G. Cloning and sequence of multiple forms of phospholipase C Cell 1988 54, N 2:161–169.
[76] Brill J. A., Hime G. R., Scharer-Schuksz M., Fuller M. T. A phospholipid kinase regulates actin organization and intercellular bridge formation during germline cytokinesis. Development. 2000;127(17):3855-64.
[77] Emoto K., Inadome H., Kanaho Y., Narumiya S., Umeda M. Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis J. Biol. Chem 2005 280, N 45:37901–37907.
[78] Carlton J. G., Cullen P. J. Coincidence detection in phosphoinositide signaling Trends Cell Biol 2005 15, N 10:540–547.
[79] Hilpela P., Vartiainen M. K., Lappalainen P. Regulation of the actin cytoskeleton by PI(4,5)P2 and PI(3,4,5)P3 Curr. Top. Microbiol. Immunol 2004 282:117–163.
[80] Balla T. Imaging and manipulating phosphoinositides in living cells J. Physiol 2007 582, N 3:927–937.
[81] De Matteis M. A., Di Campli A., Godi A. The role of the phosphoinositides at the Golgi complex Biochim. et Biophys. Acta 2005 1744, N 74:396–405.
[82] Haucke V. Phosphoinositide regulation of clathrin-mediated endocytosis Biochem. Soc. Trans 2005 33, N 6:1285–1289.
[83] Vermeer J. E., van Leeuwen W., Tobena-Santamaria R., Laxalt A. M., Jones D. R., Divecha N., Gadella T. W., Jr., Munnik T. Visualization of PtdIns3P dynamics in living plant cells Plant J 2006 47, N 5:687–700.
[84] Vincent P., Chua M., Nogue F., Fairbrother A., Mekeel H., Xu Y., Allen N., Bibikova T. N., Gilroy S., Bankaitis V. A. A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs J. Cell Biol 2005 168, N 5:801–812.
[85] Song M. F., Han Y. Z. Molecular cloning and characterization of a phosphoinositide-specific phospholipase C from Torenia fournieri Russ. J. Plant Physiol 2008 55, N 3:385– 389.
[86] Zhai S., Sui Z., Yang A., Zhang J. Characterization of a novel phosphoinositide-specific phospholipase C fro Zea mays and its expression in Escherichia coli Biotechnol. Lett 2005 27, N 11:799–804.