Multiple PLDs required for high salinity and water deficit tolerance in plants

Plant and Cell Physiology

Volumn 50, Issue 1, 2009, Pages 78-89

  Bargmann, Bastiaan O R ^a,d   Laxalt, Ana M ^a,e   Riet, Bas Ter ^a,f   Van Schooten, Bas ^a   Merquiol, Emmanuelle ^b   Testerink, Christa ^a   Haring, Michel A ^a   Bartels, Dorothea ^c   Munnik, Teun ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF BONN   (Germany)

^d NEW YORK UNIVERSITY   (United States)

^e UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

^f NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Arabidopsis; Drought; High salinity; Phosphatidic acid; Phospholipase D; Tomato

Indexed keywords

PHOSPHOLIPASE D; SODIUM CHLORIDE; VEGETABLE PROTEIN; WATER;

ARABIDOPSIS; ARTICLE; CELL CULTURE; DEHYDRATION; DRUG EFFECT; ENZYMOLOGY; GENE INACTIVATION; GENE SILENCING; GENETICS; HALOPHYTE; METABOLISM; PLANT GENE; SALINITY; TOMATO; TRANSGENIC PLANT;

ARABIDOPSIS; CELLS, CULTURED; DEHYDRATION; GENE KNOCKOUT TECHNIQUES; GENE SILENCING; GENES, PLANT; LYCOPERSICON ESCULENTUM; PHOSPHOLIPASE D; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SALINITY; SALT-TOLERANT PLANTS; SODIUM CHLORIDE; WATER;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LYCOPERSICON ESCULENTUM;

EID: 58449085005     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcn173     Document Type: Article

References (59)

1. Bargmann, B.O.R. and Munnik, T. (2006) The role of phospholipase D in plant stress responses. Curr. Opin. Plant Biol. 9: 515-522.
2. Bargmann, B.O.R., Laxalt, A.M., ter Riet, B., Schouten, E., van Leeuwen, W., Dekker, H.L., et al. (2006) LePLDbeta1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J. 45: 58-68.
3. Boudsocq, M., Barbier-Brygoo, H. and Lauriere, C. (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279: 41758-41766.
4. Boudsocq, M. and Laurière, C. (2005) Osmotic signaling in plants: multiple pathways mediated by emerging kinase families. Plant Physiol. 138: 1185-1194.
5. Burza, A.M., Pekala, I., Sikora, J., Siedlecki, P., Małagocki, P., Bucholc, M., et al. (2006) Nicotiana tabacum osmotic stress-activated kinase is regulated by phosphorylation on Ser-154 and Ser-158 in the kinase activation loop. J. Biol. Chem. 281: 34299-34311.
6. Boyer, J.S. (1982) Plant productivity and environment. Science 218: 443-448.
7. DeWald, D.B., Torabinejad, J., Jones, C.A., Shope, J.C., Cangelosi, A.R., Thompson, J.E., et al. (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed arabidopsis. Plant Physiol. 126: 759-769.
8. Distéfano, A.M., García-Mata, C., Lamattina, L. and Laxalt, A.M. (2007) Nitric oxide-induced phosphatidic acid accumulation: a role for phospholipases C and D in stomatal closure. Plant Cell Environ. 31: 187-194.
9. Dhonukshe, P., Laxalt, A.M., Goedhart, J., Gadella, T.W. and Munnik, T. (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15: 2666-2679.
10. Epstein, E., Norlyn, J.D., Rush, D.W., Kingsbury, R.W., Kelley, D.B., Cunningham, G.A., et al. (1980) Saline culture of crops: a genetic approach. Science 210: 399-404.
11. Felix, G., Duran, J.D., Volko, S. and Boller, T. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18: 265-276.
12. Felix, G., Grosskopf, D.G., Regenass, M. and Boller, T. (1991) Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc. Natl Acad. Sci. USA 88: 8831-8834.
13. Felix, G., Regenass, M. and Boller, T. (2000) Sensing of osmotic pressure changes in tomato cells. Plant Physiol. 124: 1169-1180.
14. Flowers, T.J. (2004) Improving crop salt tolerance. J. Exp. Bot. 55: 307-319.
15. Frank, W., Munnik, T., Kerkmann, K., Salamini, F. and Bartels, D. (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12: 111-124.
16. Fricke, W. (2004) Rapid and tissue-specific accumulation of solutes in the growth zone of barley leaves in response to salinity. Planta 219: 515-25.
17. Gigon, A., Matos, A.R., Laffray, D., Zuily-Fodil, Y. and Pham-Ti, A.T. (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Ann. Bot. 94: 345-351.
18. Hong, Y., Pan, X., Welti, R. and Wang, X. (2008) Phospholipase Dalpha3 is involved in the hyperosmotic response in Arabidopsis. Plant Cell 20: 803-816.
19. Hrabak, E.M., Chan, C.W., Gribskov, M., Harper, J.F., Choi, J.H., Halford, N., et al. (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 132: 666-680.
20. Jacob, T., Ritchie, S., Assmann, S.M. and Gilroy, S. (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc. Natl Acad. Sci. USA 96: 12192-12197.
21. Jakab, G., Ton, J., Flors, V., Zimmerli, L., Metraux, J.P. and Mauch-Mani, B. (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol. 139: 267-274.
22. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17: 287-291.
23. Katagiri, T., Takahashi, S. and Shinozaki, K. (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. Plant J. 26: 595-605.
24. Kelner, A., Pekala, I., Kaczanowski, S., Muszynska, G., Hardie, D.G. and Dobrowolska, G. (2004) Biochemical characterization of the tobacco 42-kD protein kinase activated by osmotic stress. Plant Physiol. 136: 3255-3265.
25. Kinraide, T.B. (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol. 118: 513-520.
26. Kusano, H., Testerink, C., Vermeer, J.E.M., Tsuge, T., Oka, A., Shimada, H., et al. (2008) The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator for root hair tip growth. Plant Cell 20: 367-380.
27. Laxalt, A.M., ter Riet, B., Verdonk, J.C., Parigi, L., Tameling, W.I., Vossen, J., et al. (2001) Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase. Plant J. 26: 237-247.
28. Li, S., Assmann, S.M. and Albert, R. (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol. 4: e312.
29. Mane, S.P., Vasquez-Robinet, C., Sioson, A.A., Heath, L.S. and Grene, R. (2007) Early PLDalpha-mediated events in response to progressive drought stress in Arabidopsis: a transcriptome analysis. J. Exp. Bot. 58: 241-252.
30. Mikołajczyk, M., Awotunde, O.S., Muszyńska, G., Klessig, D.F. and Dobrowolska, G. (2000) Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12: 165-178.
31. Mishra, G., Zhang, W., Deng, F., Zhao, J. and Wang, X. (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312: 264-266.
32. Munnik, T. (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci. 6: 227-233.
33. 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.
34. Munnik, T., Irvine, R.F. and Musgrave, A. (1994) Rapid turnover of phosphatidylinositol 3-phosphate in the green alga Chlamydomonas eugametos: signs of a phosphatidylinositide 3-kinase signalling pathway in lower plants? Biochem. J. 298: 269-73.
35. Munnik, T., Ligterink, W., Meskiene, I.I., Calderini, O., Beyerly, J., Musgrave, A., et al. (1999) Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyperosmotic stress. Plant J. 20: 381-388.
36. Munnik, T. and Meijer, H.J. (2001) Osmotic stress activates distinct lipid and MAPK signalling pathways in plants. FEBS Lett. 498: 172-178.
37. Munnik, T., Meijer, H.J., ter Riet, B., Hirt, H., Frank, W., Bartels, D., e t al. (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J. 22: 147-154.
38. Munnik, T., van Himbergen, J.A.J., ter Riet, B., Braun, F.J., Irvine, R.F., van den Ende, H., et al. (1998) Detailed analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipases C and D in Chlamydomonas cells treated with non-permeabilizing concentrations of mastoparan. Planta 207: 133-145.
39. Qin, C. and Wang, X. (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLD zeta 1 with distinct regulatory domains. Plant Physiol. 128: 1057-1068.
40. Sang, Y., Zheng, S., Li, W., Huang, B. and Wang, X. (2001) Regulation of plant water loss by manipulating the expression of phospholipase Dalpha. Plant J. 28: 135-144.
41. Testerink, C., Dekker, H.L., Lim, Z.Y., Johns, M.K., Holmes, A.B., Koster, C.G., et al. (2004) Isolation and identification of phosphatidic acid targets from plants. Plant J. 39: 527-36.
42. Testerink, C. and Munnik, T. (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10: 368-375.
43. Thiery, L., Leprince, A.S., Lefebvre, D., Ghars, M.A., Debarbieux, E. and Savouré, A. (2004) Phospholipase D is a negative regulator of proline biosynthesis in Arabidopsis thaliana. J. Biol. Chem. 279: 14812-14818.
44. van der Luit, A.H., Piatti, T., van Doorn, A., Musgrave, A., Felix, G., Boller, T., et al. (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol. 123: 1507-1516.
45. van Leeuwen, W., Ruttink, T., Borst-Vrenssen, A.W., van der Plas, L.H. and van der Krol, A.R. (2001) Characterization of position-induced spatial and temporal regulation of transgene promoter activity in plants. J. Exp. Bot. 52: 949-995.
46. van Leeuwen, W., Vermeer, J.E.M., Gadella, T.W.J., Jr. and Munnik, T. (2007) Visualisation of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J. 52: 1014-1026.
47. van Roekel, J.S.C., Damm, B., Melchers, L.S. and Hoekema, A. (1993) Factors influencing transformation frequency of tomato (Lycopersicon esculentum). Plant Cell Rep. 12: 644-647.
48. Vermeer, J.E.M, Thole, J.M., Goedhart, J., Nielsen, E., Munnik, T. and Gadella, T.W.J. Jr. (2008) Visualisation of PtdIns4 P dynamics in living plant cells. Plant J. in press.
49. Vermeer, J.E.M, van Leeuwen, W., Tobeña-Santamaria, R., Laxalt, A.M., Jones, D.R., Divecha, N., et al. (2006) Visualisation of PtdIns3P dynamics in living plant cells. Plant J. 47: 687-700.
50. Wang, X. (2002) Phospholipase D in hormonal and stress signaling. Curr. Opin. Plant Biol. 5: 408-414.
51. Wang, X. (2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development and stress responses. Plant Phys. 139: 566-573.
52. Wu, S.J., Ding, L. and Zhu, J.K. (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8: 617-627.
53. Xiong, L., Schumaker, K.S. and Zhu, J.K. (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14 Suppl: S165-S183.
54. Yamaguchi, T. and Blumwald, E. (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci. 10: 615-620.
55. Yancey, P.H., Clark, M.E., Hand, S.C., Bowlus, R.D. and Somero, G.N. (1982) Living with water stress: evolution of osmolyte systems. Science 217: 1214-1222.
56. Zhang, W., Qin, C., Zhao, J. and Wang, X. (2004) Phospholipase D alpha 1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc. Natl Acad. Sci. USA 101: 9508-9513.
57. Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q. and Zhang, W. (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na(+)/H(+) antiport in the tonoplast. Planta 224: 545-555.
58. Zhu, J.K. (2002) Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53: 247-273.
59. Zhu, J.K. (2003) Regulation of ion homeostasis under salt stress. Curr. Opin. Plant. Biol. 6: 441-445.