Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase

Frontiers in Plant Science

Volumn 4, Issue JAN, 2013, Pages

  Arisz, Steven A ^a   van Wijk, Ringo ^a   Roels, Wendy ^a   Zhu, Jian Kang ^b,c   Haring, Michel A ^a   Munnik, Teun ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b PURDUE UNIVERSITY   (United States)

^c INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

Abiotic stress; Cold stress; Diacylglycerol kinase; Lipid signaling; Phosphatidic acid; Phosphoinositide; Phospholipase; Plant signaling

Indexed keywords

EID: 84890555941     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00001     Document Type: Article

References (61)

1. Agarwal, M., Hao, Y., Kapoor, A., Dong, C. H., Fujii, H., Zheng, X., et al. (2006). A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J. Biol. Chem. 281, 37636-37645.
2. Arisz, S. A., and Munnik, T. (2011). The salt stress-induced LPA response in Chlamydomonas is produced via PLA hydrolysis of DGK-generated phosphatidic acid. J. Lipid Res. 52, 2012-2020.
3. Arisz, S. A., Testerink, C., and Munnik, T. (2009). Plant PA signaling via diacylglycerol kinase. Biochim. Biophys. Acta 1791, 869-875.
4. Bargmann, B. O. R., Arisz, S. A., Laxalt, A. M., ter Riet, B., van Schooten, B., Merquiol, E., et al. (2009a). Multiple PLDs required for high salinity-and water deficit tolerance in plants. Plant Cell Physiol. 50, 78-89.
5. Bargmann, B. O. R., Laxalt, A. M., ter Riet, B., Testerink, C., Merquiol, E., Mosblech, A., et al. (2009b). Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant Cell Environ. 32, 837-850.
6. Brice, S. E., Alford, C. W., and Cowart, L. A. (2009). Modulation of sphingolipid metabolism by the phosphatidylinositol-4-phosphate phosphatase Sac1p through regulation of phosphatidylinositol inSaccharomyces cerevisiae. J. Biol. Chem. 284, 7588-7596.
7. Cantrel, C., Vazquez, T., Puyaubert, J., Reze, N., Lesch, M., Kaiser, W. M., et al. (2011). Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol. 189, 415-427.
8. Carpaneto, A., Ivashikina, N., Levchenko, V., Krol, E., Jeworutzki, E., Zhu, J. K., et al. (2007). Cold transiently activates calcium-permeable channels in Arabidopsis mesophyll cells. Plant Physiol. 143, 487-494.
9. Chen, Q. F., Xiao, S., and Chye, M. L. (2008). Overexpression of the Arabidopsis 10-kilodalton acyl-coenzyme A-binding protein ACBP6 enhances freezing tolerance. Plant Physiol. 148, 304-315.
10. Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B. H., Hong, X., Agarwal, M., et al. (2003). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 17, 1043-1054.
11. Chinnusamy, V., Zhu, J., and Zhu, J. K. (2007). Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444-451.
12. Cho, M. H., Shears, S. B., and Boss, W. F. (1993). Changes in phosphatidylinositol metabolism in response to hyperosmotic stress in Daucus carota L. cells grown in suspension culture. Plant Physiol. 103, 637-647.
13. Cook, D., Fowler, S., Fiehn, O., and Thomashow, M. F. (2004). A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 15243-15248.
14. Du, Z. Y., Xiao, S., Chen, Q. F., and Chye, M. L. (2010). Depletion of the membrane-associated acyl-coenzyme A-binding protein ACBP1 enhances the ability of cold acclimation in Arabidopsis. Plant Physiol. 152, 1585-1597.
15. Gawer, M., Norberg, P., Chervin, D., Guern, N., Yaniv, Z., Mazliak, P., et al. (1999). Phosphoinositides and stress-induced changes in lipid metabolism of tobacco cells. Plant Sci. 141, 117-127.
16. Gomez-Merino, F. C., Arana-Ceballos, F. A., Trejo-Tellez, L. I., Skirycz, A., Brearley, C. A., Dormann, P., et al. (2005). Arabidopsis AtDGK7, the smallest member of plant diacylglycerol kinases (DGKs), displays unique biochemical features and saturates at low substrate concentration: the DGK inhibitor R59022 differentially affects AtDGK2 and AtDGK7 activity in vitro and alters plant growth and development. J. Biol. Chem. 280, 34888-34899.
17. Gomez-Merino, F. C., Brearley, C. A., Ornatowska, M., Abdel-Haliem, M. E., Zanor, M. I., and Mueller-Roeber, B. (2004). AtDGK2, a novel diacylglycerol kinase from Arabidopsis thaliana, phosphorylates 1-stearoyl-2-arachidonoyl-sn-glycerol and 1, 2-dioleoyl-sn-glycerol and exhibits cold-inducible gene expression. J. Biol. Chem. 279, 8230-8241.
18. Guo, Y., Xiong, L., Ishitani, M., and Zhu, J. K. (2002). An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc. Natl. Acad. Sci. U.S.A. 99, 7786-7791.
19. Hirayama, T., Ohto, C., Mizoguchi, T., and 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. U.S.A. 92, 3903-3907.
20. Hong, S. M., Bahn, S. C., Lyu, A., Jung, H. S., and Ahn, J. H. (2010). Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. Plant Cell Physiol. 51, 1694-1706.
21. Inatsugi, R., Nakamura, M., and Nishida, I. (2002). Phosphatidylcholine biosynthesis at low temperature: differential expression of CTP: phosphorylcholine cytidylyltransferase isogenes in Arabidopsis thaliana. Plant Cell Physiol. 43, 1342-1350.
22. Ishitani, M., Xiong, L., Lee, H., Stevenson, B., and Zhu, J. K. (1998). HOS1, a genetic locus involved in cold-responsive gene expression in arabidopsis. Plant Cell 10, 1151-1161.
23. Jonak, C., Kiegerl, S., Ligterink, W., Barker, P. J., Huskisson, N. S., and Hirt, H. (1996). Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. U.S.A. 93, 11274-11279.
24. Kargiotidou, A., Kappas, I., Tsaftaris, A., Galanopoulou, D., and Farmaki, T. (2010). Cold acclimation and low temperature resistance in cotton: Gossypium hirsutum phospholipase Dalpha isoforms are differentially regulated by temperature and light. J. Exp. Bot. 61, 2991-3002.
25. Kawamura, Y., and Uemura, M. (2003). Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 36, 141-154.
26. Knight, H., and Knight, M. R. (2000). Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis. J. Exp. Bot. 51, 1679-1686.
27. Knight, H., Trewavas, A. J., and Knight, M. R. (1996). Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8, 489-503.
28. Lee, B. H., Henderson, D. A., and Zhu, J. K. (2005). The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17, 3155-3175.
29. Li, M., Hong, Y., and Wang, X. (2009). Phospholipase D-and phosphatidic acid-mediated signaling in plants. Biochim. Biophys. Acta 1791, 927-935.
30. Li, W., Li, M., Zhang, W., Welti, R., and Wang, X. (2004). The plasma membrane-bound phospholipase Ddelta enhances freezing tolerance in Arabidopsis thaliana. Nat. Biotechnol. 22, 427-433.
31. Mahan, J. R., Dotray, P. A., and Light, G. G. (2004). Thermal dependence of enzyme function and inhibition; implications for, herbicide efficacy and tolerance. Physiol. Plant. 120, 187-195.
32. Malherbe, A., Block, M. A., Joyard, J., and Douce, R. (1992). Feedback inhibition of phosphatidate phosphatase from spinach chloroplast envelope membranes by diacylglycerol. J. Biol. Chem. 267, 23546-23553.
33. Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., Yamaguchi-Shinozaki, K., Matsumoto, K., et al. (1996). A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 93, 765-769.
34. Moellering, E. R., and Benning, C. (2011). Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci. 16, 98-107.
35. Moellering, E. R., Muthan, B., and Benning, C. (2010). Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228.
36. Munnik, T. (2001). Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci. 6, 227-233.
37. 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.
38. Munnik, T., Irvine, R. F., and Musgrave, A. (1998a). Phospholipid signalling in plants. Biochim. Biophys. Acta 1389, 222-272.
39. Munnik, T., van Himbergen, J. A. J., Ter Riet, B., Braun, F.-J., Irvine, R. F., van den Ende, H., et al. (1998b). 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.
40. Munnik, T., and Nielsen, E. (2011). Green light for polyphosphoinositide signals in plants. Curr. Opin. Plant Biol. 14, 489-497.
41. Munnik, T., and Testerink, C. (2009). Plant phospholipid signaling: "in a nutshell. " J. Lipid Res. 50(Suppl.), S260-S265.
42. Munnik, T., and Vermeer, J. E. M. (2009). Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ. 33, 655-669.
43. Peng, Y., Lin, W., Cai, W., and Arora, R. (2007). Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226, 729-740.
44. Peters, C., Li, M., Narasimhan, R., Roth, M., Welti, R., and Wang, X. (2010). Nonspecific phospholipase C NPC4 promotes responses to abscisic acid and tolerance to hyperosmotic stress in Arabidopsis. Plant Cell 22, 2642-2659.
45. Rajashekar, C. B., Zhou, H. E., Zhang, Y., Li, W., and Wang, X. (2006). Suppression of phospholipase Dalpha1 induces freezing tolerance in Arabidopsis: response of cold-responsive genes and osmolyte accumulation. J. Plant Physiol. 163, 916-926.
46. Ruelland, E., Cantrel, C., Gawer, M., Kader, J. C., and Zachowski, A. (2002). Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol. 130, 999-1007.
47. Sui, Z., Niu, L., Yue, G., Yang, A., and Zhang, J. (2008). Cloning and expression analysis of some genes involved in the phosphoinositide and phospholipid signaling pathways from maize (Zea mays L.). Gene 426, 47-56.
48. Tasma, I. M., Brendel, V., Whitham, S. A., and Bhattacharyya, M. K. (2008). Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol. Biochem. 46, 627-637.
49. Teige, M., Scheikl, E., Eulgem, T., Doczi, R., Ichimura, K., Shinozaki, K., et al. (2004). The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell 15, 141-152.
50. Testerink, C., and Munnik, T. (2005). Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10, 368-375.
51. Testerink, C., and Munnik, T. (2011). Molecular, cellular and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 62, 2349-2361.
52. Thomashow, M. F. (1999). PLANT COLD ACCLIMATION: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599.
53. Thorlby, G., Fourrier, N., and Warren, G. (2004). The SENSITIVE TO FREEZING2 gene, required for freezing tolerance in Arabidopsis thaliana, encodes a beta-glucosidase. Plant Cell 16, 2192-2203.
54. Uemura, M., Joseph, R. A., and Steponkus, P. L. (1995). Cold Acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol. 109, 15-30.
55. Van Buskirk, H. A., and Thomashow, M. F. (2006). Arabidopsis transcription factors regulating cold acclimation. Physiol. Plant. 126, 72-80.
56. Vaultier, M. N., Cantrel, C., Guerbette, F., Boutte, Y., Vergnolle, C., Cicek, D., et al. (2008). The hydrophobic segment of Arabidopsis thaliana cluster I diacylglycerol kinases is sufficient to target the proteins to cell membranes. FEBS Lett. 582, 1743-1748.
57. Vergnolle, C., Vaultier, M. N., Taconnat, L., Renou, J. P., Kader, J. C., Zachowski, A., et al. (2005). The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol. 139, 1217-1233.
58. Wang, W., Yang, X., Tangchaiburana, S., Ndeh, R., Markham, J. E., Tsegaye, Y., et al. (2008). An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20, 3163-3179.
59. Welti, R., Li, W., Li, M., Sang, Y., Biesiada, H., Zhou, H. E., et al. (2002). Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem. 277, 31994-32002.
60. Xiong, L., Lee, B., Ishitani, M., Lee, H., Zhang, C., and Zhu, J. K. (2001). FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15, 1971-1984.
61. Xiong, L., Schumaker, K. S., and Zhu, J. K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell14(Suppl.), S165-S183.