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Cloning of Phospholipase D from Grape Berry and Its Expression under Heat Acclimation

  • Wan, Si-Bao (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Wang, Wei (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Wen, Peng-Fei (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Chen, Jian-Ye (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Kong, Wei-Fu (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Pan, Qiu-Hong (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Zhan, Ji-Cheng (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Tian, Li (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Liu, Hong-Tao (College of Food Science & Nutritional Engineering, China Agricultural University) ;
  • Huang, Wei-Dong (College of Food Science & Nutritional Engineering, China Agricultural University)
  • Published : 2007.07.31

Abstract

To investigate whether phospholipase D (PLD, EC 3.1.4.4) plays a role in adaptive response of post-harvest fruit to environment, a PLD gene was firstly cloned from grape berry (Vitis Vinifera L. cv. Chardonnay) using RT-PCR and 3'- and 5'-RACE. The deduced amino acid sequence (809 residues) showed 84.7% identity with that of PLD from Ricinus communis. The secondary structures of this protein showed the characteristic C2 domain and two active sites of a phospholipid-metabolizing enzyme. The PLD activity and its expression in response to heat acclimation were then assayed. The results indicated PLD was significantly activated at enzyme activity, as well as accumulation of PLD mRNA and synthesis of new PLD protein during the early of heat acclimation, primary suggesting that the grape berry PLD may be involved in the heat response in post-harvest grape berry. This work offers an important basis for further investigating the mechanism of post-harvest fruit adaptation to environmental stresses.

Keywords

Cloning;Gene expression;Grape berry;Heat acclimation;Phospholipase D

References

  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402. https://doi.org/10.1093/nar/25.17.3389
  2. Beruter, J. and Studer, F. M. (1995) Comparison of sorbitol transport in excised tissue discs and cortex tissue of intact apple fruit. J. Plant Physiol. 146, 95-102. https://doi.org/10.1016/S0176-1617(11)81973-5
  3. Bradford, N. M. (1976) A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye bingding. Anal. Biochem. 72, 248-259. https://doi.org/10.1016/0003-2697(76)90527-3
  4. Dhindsa, R. S., Plumb-Dhindsa, P. and Thorpe, T. A. (1981) Leaf senescence: correlated with increased leaves of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J. Exp. Bot. 32, 93-101. https://doi.org/10.1093/jxb/32.1.93
  5. Dyer, J. H., Zheng, L. and Wang, X. M. (1995) Cloning and nucleotide sequence of a cDNA encoding phospholipase D from Arabidopsis (Accession No. U36381). Plant Physiol. 109, 1497. https://doi.org/10.1104/pp.109.4.1497
  6. Famiani, F., Walker, R. P., Tecsi, L., Chen, Z. H., Proietti, P. and Leegood, R. C. (2000) An immunohistochemical study of the compartmentation of metabolism during the development of grape berries. J. Exp. Bot. 51, 675-683. https://doi.org/10.1093/jexbot/51.345.675
  7. Frova, C. (2000) Genetic dissection of thermotolerance in maize; in Physical Stress in Plants, Grillo, S. and Leone, A. (eds.), pp.31-38, Springer-Verlag, New York, USA.
  8. Gottlin, E. B., Rudolph, A. E., Zhao, Y., Matthews, H. R. and Dixon, J. W. (1998) Catalytic mechanism of the phospholipase D superfamily proceeds via a covalent phosphohistidine intermediate. Proc. Natl. Acad. Sci. USA 95, 9202-9. https://doi.org/10.1073/pnas.95.16.9202
  9. Gradiner, J. C., Harper, J. D., Weerakoon, N. D., Collings, D. A., Ritchie, S., Gilroy, S., Cyr, R. J. and Marc, J. (2001) A 90-KD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13, 2143-2158. https://doi.org/10.1105/tpc.13.9.2143
  10. Guo, B. Z., Xu, G., Cao, Y. G. and Holbrook, C. C. (2005) Identification and characterization of phospholipase D and its association with drought susceptibilities in peanut (Arachis hypogaea). Planta 223, 512-520.
  11. Howarth, C. J. and Ougham, H. J. (1993) Gene expression under temperature stress. New Phytol. 125, 1-26. https://doi.org/10.1111/j.1469-8137.1993.tb03862.x
  12. Isla, M. I., Vattuone, M. A. and Sampietro, A. R. (1998) Essential group at the active site of Frapaeolum invertase. Phytochemistry 47, 1189-1193. https://doi.org/10.1016/S0031-9422(97)00757-7
  13. Kopka, J., Christophe, P., Alistair, M. H. and Bernd, M. R. (1998) $Ca^{2+}/phospholipid-binding$ (C2) domain in multiple plant proteins: novel components of the calcium-sensing apparatus. Plant Mol. Biol. 36, 627-637. https://doi.org/10.1023/A:1005915020760
  14. Laemmli, U. K. (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227, 680-685. https://doi.org/10.1038/227680a0
  15. Larkindale, J., Hall, J. D., Knight, M. R. and Vierling, E. (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 88-897.
  16. Larkindale, J. and Huang, B. R. (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J. Plant Physiol. 161, 405-413. https://doi.org/10.1078/0176-1617-01239
  17. Levitt, J. (1980) Responses of plants to environmental stresses; in Physiological Ecology, Kozlowski, T. T. (ed.), pp. 347-448, Academic Press, New York, USA.
  18. Li, W. Q., Li, M. Y., Zhang, W. H., Welti, R. and Wang, X. M. (2004) The plasma membrane-bound phospholipase Da enhances freezing tolerance in Arabidopsis thaliana. Nature Biotech. 22, 427-433. https://doi.org/10.1038/nbt949
  19. Liu, H. T., Huang, W. D., Pan, Q. H., Weng, F. H., Zhan, J. C., Liu, Y., Wan, S. B. and Liu, Y. Y. (2006) Contributions of $PIP_2-specific-phospholipase$ C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves. J. Plant Physiol. 163, 405-416. https://doi.org/10.1016/j.jplph.2005.04.027
  20. Maarouf, H. E., Zuily-Fodil, Y., Gareil, M., d'Arcy-Lameta, A. and PhamThi, A. T. (1999) Enzymatic activity and gene expression under water stress of phospholipase D in two cultivars of Vigna unguiculata L. Walp. Differing in drought tolerance. Plant Mol. Biol. 39, 1257-1265. https://doi.org/10.1023/A:1006165919928
  21. Marchler-Bauer, A., Anderson, J. B., Cherukuri, P. F., DeWeese-Scott, C., Geer, L. Y., Gwadz, M., He, S., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Liebert, C. A., Liu, C., Lu, F., Marchler, G. H., Mullokandov, M., Shoemaker, B. A., Simonyan, V., Song, J. S., Thiessen, P. A., Yamashita, R. A., Yin, J. J., Zhang, D. and Bryant, S. H. (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33, 192-196. https://doi.org/10.1093/nar/gni191
  22. Marchler-Bauer, A. and Bryant, S. H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32, 327-331. https://doi.org/10.1093/nar/gkh454
  23. Munnik, T., Arisz, S. A., de Vrije, T. and Musgrave, A. (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7, 2197-2210. https://doi.org/10.1105/tpc.7.12.2197
  24. Munnik, T., Meijer, H., Riet, B., Hirt, H., Frank, W., Bartels, D. and Musgrave, A. (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J. 22, 147-154. https://doi.org/10.1046/j.1365-313x.2000.00725.x
  25. Nalefski, E. A., Slazas, M. M. and Falke, J. J. (1997) Calcium signaling cycle of a membrane docking C2 domain. Biochemistry 36, 12011-12018. https://doi.org/10.1021/bi9717340
  26. Ochoa, W. F., Garcia-Garcia, J., Fita, I., Corbalan-Garcia, S., Verdaguer, N. and Gomez-Fernandez, J. C. (2001) Structure of the C2 domain from novel protein kinase $C^{\aa}$.A membrane binding model for $Ca^{2+}-independent$ C2 domains. J. Mol. Biol. 311, 837-849. https://doi.org/10.1006/jmbi.2001.4910
  27. Pan, Q. H., Zhan, J. C., Liu, H. T., Zhang, J. H., Chen, J. Y., Wen, P. F. and Huang, W. D. (2006) Salicylic acid synthesized by benzoic acid 2-hydroxylase participates in the development of thermotolerance in pea plants. Plant Sci. 171, 226-233 https://doi.org/10.1016/j.plantsci.2006.03.012
  28. Pappan, K., Zheng, L., Krishnamoorthi, R. and Wang, X. M. (2004) Evidence for and characterization of $Ca^{2+}$ binding to the catalytic region of Arabidopsis thaliana phospholipase Da. J. Biol. Chem. 279, 47833-47839 https://doi.org/10.1074/jbc.M402789200
  29. Pinhero, R. G., Almquist, K. C., Novotna, Z. and Paliyath, G. (2003) Developmental regulation of phospholipase D in tomato fruits. Plant Physiol. Bioch. 41, 223-240. https://doi.org/10.1016/S0981-9428(03)00014-7
  30. Pinhero, R. G., Paliyath, G., Yada, R. Y. and Murr, D. P. (1998) Modulation of phospholipase D and lipoxygenase activities during chilling. Relation to chilling tolerance of maize seedlings. Plant Physiol. Biochem. 36, 213-224. https://doi.org/10.1016/S0981-9428(97)86878-7
  31. Ponting, C. P. and Kerr, I. D. (1996) A novel family of phospholipase D homologues that includes phospholipid synthesis and putative endonucleases. Protein Sci. 5, 914-922. https://doi.org/10.1002/pro.5560050513
  32. Rogers, S. O. and Bendlich A. L. (1994) Extraction of total cellular DNA from plants, algae and fungi; in Plant Molecular Biology Manual, Gelvin, S. B. and Schilperoort, A. R. (eds), pp. 1-8, Kluwer Academic Publishers, Dordrecht, Netherland.
  33. Ruelland, E., Cantrel, C., Gawer, M., Kader, J. C. and Zachowski, A. (2002) Activation of phospholipase C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol. 130, 999-1007. https://doi.org/10.1104/pp.006080
  34. Ryu, S. B. and Wang, X, M. (1996) Activation of phospholipase D and the possible mechanism of activation of wound-induced lipid hydrolysis in castor bean leaves. Biochim. Biophys. Acta 1303, 243-250. https://doi.org/10.1016/0005-2760(96)00096-3
  35. Sang, Y. M., Zheng, S. Q., Li, W. Q., Huang, B. R. and Wang, X. M. (2001) Regulation of plant water loss by manipulating the expression of phospholipase $D{\alpha}$. Plant J. 28, 135-144. https://doi.org/10.1046/j.1365-313X.2001.01138.x
  36. Srikanthbabu, V., Ganeshkumar, Krishnaprasad, B. T., Gopalakrishna, R., Sayitha, M. and Udayakumar, M. (2002) Identification of pea genotypes with enhanced the thermotolerance using temperature induction response technique (TIR). J. Plant Physiol. 159, 535-545. https://doi.org/10.1078/0176-1617-00650
  37. Stuckey, J. A. and Dixon, J. E. (1999) Crystal structure of a phospholipase D family member. Nat. Struct Biol. 6, 278-284. https://doi.org/10.1038/6716
  38. Sung, D. Y., Kaplan, F., Lee, K. J. and Guy, C. L. (2003) Acquired tolerance to temperature extremes. Trends Plant Sci. 8, 179-187. https://doi.org/10.1016/S1360-1385(03)00047-5
  39. Sung, T., Roper, P. L., Zhang, Y., Rudge, S. A., Temel, R., Moss, B., Engebrecht, J. and Frohman, M. A. (1997) Mutagenesis of phospholipase D defines a superfamily including a trans-golgi, viral protein required for poxvirus pathogenicity. EMBO J. 16, 4519-4530. https://doi.org/10.1093/emboj/16.15.4519
  40. Vierling, E. (1991) The roles of heat shock proteins in plants. Plant Mol. Biol. 42,519-620.
  41. Wang, C. X., Zien, C. A., Afitlhile, M., Welti, R., Hildebrand, D. F. and Wang X. M. (2000) Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in Arabidopsis. Plant Cell 12, 2237-2246. https://doi.org/10.1105/tpc.12.11.2237
  42. Wang, L. J., Huang, W. D., Li,, J. Y., Liu, Y. F. and Shi, Y. L. (2004) Peroxidation of membrane lipid and $Ca^{2+}$ homeostasis in grape mesophyll cells during the process of cross-adaptation to temperature stresses. Plant Sci. 167, 71-77. https://doi.org/10.1016/j.plantsci.2004.02.028
  43. Wang, L. J. and Li, S. H. (2006) Salicylic acid-induced heat or cold tolerance in relation to $Ca^{2+}$ homeostasis and antioxidant systems in young grape plants. Plant Sci. 170, 685-694. https://doi.org/10.1016/j.plantsci.2005.09.005
  44. Wang, X. M. (1999) The role of phospholipas D in signaling cascades. Plant Physiol. 120, 645-651. https://doi.org/10.1104/pp.120.3.645
  45. Wang, X. M. (2000) Multiple forms of phospholipase D in plants: The gene family, catalytic and regulatory properties, and cellular functions. Prog. Lipid Res. 39, 109-149. https://doi.org/10.1016/S0163-7827(00)00002-3
  46. Wang, X. M. (2004) Lipid signaling. Curr. Opin. Plant Biol. 7, 329-336. https://doi.org/10.1016/j.pbi.2004.03.012
  47. Wang, X. M., Dyer, J. H. and Zheng, L. (1993) Pruification and immunological analysis of phospholipase D from castor bean endosperm. Arch. Biolchem. Biophys. 306, 386-394.
  48. Wang, X. M., Xu, L. W. and Zheng, L. (1994) Cloning and expression of phosphatidylcholine-hydrolyzing phospholipase D from Ricinus communis L. J. Biol. Chem. 269, 20312-20317.
  49. Welti, R., Li, W. Q., Li, M. Y., Sang, Y. M., Biesiada, H., Zhou, H., Rajashekar, C. B., Williams, T. D. and Wang, X. M. (2002) Profiling membrane lipids in plant stress responses: role of phospholipase Da in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem. 277, 31994-32002. https://doi.org/10.1074/jbc.M205375200
  50. Wen, P. F., Chen, J. Y., Kong, W. F., Pan, Q. H., Wan, S. B. and Huang, W. D. (2005) Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci. 169, 928-934. https://doi.org/10.1016/j.plantsci.2005.06.011
  51. Zhang, J. H., Huang W. D., Pan Q. H. and Liu Y. P. (2005) Improvement of chilling tolerance and accumulation of heat shock proteins in grape berries (Vitis vinifera cv. jingxiu) by heat pretreatment. Postharvest Biol. Tec. 38, 80-90. https://doi.org/10.1016/j.postharvbio.2005.05.008
  52. Zonia, L. and Munnik, T. (2004) Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol. 134, 813-823. https://doi.org/10.1104/pp.103.029454

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