Abstract
Phosphoinositide-specific phospholipase C (PI-PLC) plays a central role in the phosphatidylinositol specific signal transduction pathway. Plant PI-PLCs have been demonstrated to be involved in various stimuli and physiological processes. Five Arabidopsis thaliana PI-PLC genes were overexpressed transiently in tobacco leaves, and one of them, AtPLC5, was stably expressed in transgenic Arabidopsis; a dexamethasone-inducible promoter was used. Expression of AtPLC5 in transiently transformed tobacco resulted in leaf senescence at 72 h after induction, while other AtPLC did not cause any visible changes. Stable overexpression of AtPLC5 in transgenic Arabidopsis resulted in clearly induced visible yellowing at 8 days after induction, meanwhile chlorophyll content was decreased, PI-PLC activity and electric conductivity were increased. qPCR results demonstrated that increased transcription of senescence-associated genes (SAG12, SAG13, SAG15, SAG18 and SAG29) were up regulated after AtPLC5 induction. When AtPLC5 fused with green fluorescent protein was transiently expressed in protoplasts prepared from Arabidopsis mesophyll cells, green fluorescence was clearly observed in the plasma membrane (PM). Moreover, western blot analysis indicated that AtPLC5 was found to be enriched in the PM fraction of transgenic Arabidopsis stably expressing AtPLC5. These results suggest that AtPLC5 is predominantly localized in the PM and may be a regulator of leaf senescence.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- AS:
-
Acetosyringone
- CaMV:
-
Cauliflower mosaic virus
- DAG:
-
1,2-Diacylglycerol
- DEX:
-
Dexamethasone
- IP3 :
-
Inositol 1,4,5-trisphosphate
- PI-PLC:
-
Phosphoinositide-specific phospholipase C
- PIP2 :
-
Phosphatidylinositol 4,5-bisphosphate
- PKC:
-
Protein kinase C
- PM:
-
Plasma membrane
- SAG:
-
Senescence-associated gene
References
Aoyama T, Chua NH (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11(3):605–612. doi:10.1046/j.1365-313X.1997.11030605.x
Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Köhler B, Mueller-Roeber B (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J 62(2):250–264. doi:10.1111/j.1365-313X.2010.04151.x
Berridge MJ (1993) Inositol trisphosphate and calcium signaling. Nature 361(6410):315–325
Briskin DP, Leonard RT, Hodges TK (1987) Isolation of plasma membrane: membrane markers and general principles. Methods Enzymol 148:542–558
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. doi:10.1046/j.1365-313x.1998.00343.x
Devaiah SP, Pan X, Hong Y, Roth M, Welti R, Wang X (2007) Enhancing seed quality and viability by suppressing phospholipase D in Arabidopsis. Plant J 50(6):950–957. doi:10.1111/j.1365-313X.2007.03103.x
Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657. doi:10.1038/nature05185
Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase Dα retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9(12):2183–2196. doi:10.1105/tpc.9.12.2183
Georges F, Das S, Ray H, Bock C, Nokhrina K, Kolla V, Keller W (2009) Over-expression of Brassica napus phosphatidylinositol-phospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. Plant Cell Environ 32:1664–1681. doi:10.1111/j.1365-3040.2009.02027.x
Gepstein S, Sabehi G, Carp MJ, Hajouj T, Nesher MFO, Yariv I, Dor C, Bassani M (2003) Large-scale identification of leaf senescence-associated genes. Plant J 36(5):629–642. doi:10.1046/j.1365-313X.2003.01908.x
Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27(5):521–549. doi:10.1111/j.1365-3040.2003.01158.x
He Y, Gan S (2002) A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 14(4):805–815. doi:10.1105/tpc.010422
Hirayama T, Ohto C, Mizoguchi T, Shinozaki K (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 92:3903–3907. doi:10.1073/pnas.92.9.3903
Hunt L, Otterhag L, Lee JC, Lasheen T, Hunt J, Seki M, Shinozaki K, Sommarin M, Gilmour DJ, Pical C (2004) Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms. New Phytol 162:643–654. doi:10.1111/j.1469-8137.2004.01069.x
Kapila J, De Rycke R, Van Montagu M, Angenon G (1997) An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122(1):101–108. doi:10.1016/S0168-9452(96)04541-4
Kim CY, Bove J, Assmann SM (2008) Overexpression of wound-responsive RNA-binding proteins induces leaf senescence and hypersensitive-like cell death. New Phytol 180(1):57–70. doi:10.1111/j.1469-8137.2008.02557.x
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685. doi:10.1038/227680a0
Li J, Wang X, Qin T, Zhang Y, Liu X, Sun J, Zhou Y, Zhu L, Zhang Z, Yuan M, Mao T (2011) MDP25, a novel calcium regulatory protein, mediates hypocotyl cell elongation by destabilizing cortical microtubules in Arabidopsis. Plant Cell 23(12):4411–4427. doi:10.1105/tpc.111.092684
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. doi:10.1146/annurev.arplant.57.032905.105316
Lutts S, Kinet J, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot Lond 78(3):389–398. doi:10.1006/anbo.1996.0134
Melin PM, Pical C, Jergil B, Sommarin M (1992) Polyphosphoinositide phospholipase C in wheat root plasma membranes. Partial purification and characterization. Biochim Biophys Acta 1123(2):163–169. doi:10.1016/0005-2760(92)90107-7
Miller JD, Arteca RN, Pell EJ (1999) Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 120(4):1015–1024. doi:10.1104/pp.120.4.1015
Munnik T, Testerink C (2009) Plant phospholipid signaling:”in a nutshell”. J Lipid Res 50:S260–S265. doi:10.1194/jlr.R800098-JLR200
Otterhag L, Sommarin M, Pical C (2001) N-terminal EF-hand-like domain is required for phosphoinositide-specific phospholipase C activity in Arabidopsis thaliana. FEBS Lett 497:165–170. doi:10.1016/S0014-5793(01)02453-X
Pružinská A, Tanner G, Aubry S, Anders I, Moser S, Muller T, Ongania K, Krautler B, Youn J, Liljegren S, Hörtensteiner S (2005) Chlorophyll breakdown in senescent Arabidopsis leaves. characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139(1):52–63. doi:10.1104/pp.105.065870
Ren D, Yang K, Li G, Liu Y, Zhang S (2006) Activation of Ntf4, a tobacco mitogen-activated protein kinase, during plant defense response and its involvement in hypersensitive response-like cell death. Plant Physiol 141(4):1482–1493. doi:10.1104/pp.106.080697
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132(3):365–386. doi:10.1385/1-59259-192-2:365
Sanchez JP, Chua NH (2001) Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 13(5):1143–1154. doi:10.1105/tpc.13.5.1143
Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129(15):3533–3544
Seo PJ, Park JM, Kang SK, Kim SG, Park CM (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233(1):189–200. doi:10.1007/s00425-010-1293-8
Su T, Xu J, Li Y, Lei L, Zhao L, Yang H, Feng J, Liu G, Ren D (2011) Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23(1):364–380. doi:10.1105/tpc.110.079145
Tasma IM, Brendel V, Whitham SA, Bhattacharyya MK (2008) Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol Biochem 46(7):627–637. doi:10.1016/j.plaphy.2008.04.015
Vossen JH, Abd-El-Haliem A, Fradin EF, Van Den Berg G, Ekengren SK, Meijer HJG, Seifi A, Bai Y, Ten Have A, Munnik T (2010) Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J 62(2):224–239. doi:10.1111/j.1365-313X.2010.04136.x
Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37(3):455–469. doi:10.1023/A:1005934428906
Xu X, Cao Z, Liu G, Bhattacharrya MK, Ren D (2004) Cloning and expression of AtPLC6, a gene encoding a phosphatidylinositol-specific phospholipase C in Arabidopsis thaliana. Chin Sci Bull 49(6):567–573. doi:10.1360/03wc0514
Xu M, Sheng J, Wang H, Dong J (2011) Involvement of NADPH oxidase-mediated H2O2 signaling in PB90-induced hypericin accumulation in Hypericum perforatum cells. Plant Cell Tiss Org 105(1):47–53. doi:10.1007/s11240-010-9837-y
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572. doi:10.1038/nprot.2007.199
Zhai J, Xu H, Cong X, Deng Y, Xia Z, Huang X, Hao G, Jiang X (2013) Ca2+/H+ exchange in the plasma membrane of Arabidopsis thaliana leaves. Acta Physiol Plant 35(1):161–173. doi:10.1007/s11738-012-1059-y
Zhang TG, Chen QQ, Wang N, Xia XH, Wang J, Chang Y, Yang YL, Yang N, Sun WC (2013) Molecular cloning and characterization of the mitogen-activated protein kinase kinase gene (MKK4) and its promoter sequence from oilseed rape (Brassica campestris L.). Plant Cell Tiss Org 115(3):341–353. doi:10.1007/s11240-013-0366-3
Zheng SZ, Liu YL, Li B, Shang Z, Zhou RG, Sun DY (2012) Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance in Arabidopsis. Plant J 69(4):689–700. doi:10.1111/j.1365-313X.2011.04823.x
Acknowledgments
This work was supported by grants from the State Basic Research Program (2012CB114200 to D.R.), the National Natural Science Foundation of China (31030010 to D.R., 30771124 to H.Y.).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, J., Xia, K., Yang, Y. et al. Overexpression of Arabidopsis phosphoinositide-specific phospholipase C5 induces leaf senescence. Plant Cell Tiss Organ Cult 120, 585–595 (2015). https://doi.org/10.1007/s11240-014-0625-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11240-014-0625-y