Connections between sphingosine kinase and phospholipase D in the abscisic acid signaling pathway in Arabidopsis

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8286-8296

  Guo, Liang ^a,b   Mishra, Girish ^a,b,d   Markham, Jonathan E ^b,e   Li, Maoyin ^a,b   Tawfall, Amanda ^a,b   Welti, Ruth ^c   Wang, Xuemin ^a,b  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^b DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

^d UNIVERSITY OF DELHI   (India)

^e UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS THALIANA; PHOSPHATIDIC ACIDS; PHOSPHOLIPASE D; PHYSIOLOGICAL FUNCTIONS; PHYTOSPHINGOSINES; PLANT RESPONSE; SIGNALING PATHWAYS; SPHINGOSINE KINASE; STOMATAL CLOSURES; WILD-TYPE PLANTS;

ENZYMES; PHYSIOLOGICAL MODELS; PLANTS (BOTANY);

PLANT SHUTDOWNS;

ABSCISIC ACID; PHOSPHATE DERIVATIVE; PHOSPHATIDIC ACID; PHOSPHOLIPASE D; PHYTOSPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; NONHUMAN; PLANT GENE; PLANT LEAF; PLANT STOMA; PLDAPHA1 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTOPLAST; SIGNAL TRANSDUCTION; SPHK1 1 GENE; SPHK2 1 GENE; WILD TYPE;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; PHOSPHATIDIC ACIDS; PHOSPHOLIPASE D; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLANT STOMATA; SIGNAL TRANSDUCTION; SPHINGOSINE;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84863246249     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.274274     Document Type: Article

References (42)

1. Wang, X., Devaiah, S. P., Zhang, W., and Welti, R. (2006) Signaling functions of phosphatidic acid. Prog. Lipid Res. 45, 250-278
2. Bargmann, B. O., and Munnik, T. (2006) The role of phospholipase D in plant stress responses. Curr. Opin. Plant Biol. 9, 515-522 (Pubitemid 44292057)
3. Li, M., Hong, Y., and Wang, X. (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochim. Biophys. Acta 1791, 927-935
4. Hong, Y., Zheng, S., and Wang, X. (2008) Dual functions of phospholipase Dα1 in plant response to drought. Molecular Plant 1, 262-269
5. Ritchie, S., and Gilroy, S. (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc. Natl. Acad. Sci. U.S.A. 95, 2697-2702 (Pubitemid 28146006)
6. 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. U.S.A. 96, 12192-12197 (Pubitemid 29502880)
7. Zhang, W., Qin, C., Zhao, J., and Wang, X. (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc. Natl. Acad. Sci. U.S.A. 101, 9508-9513 (Pubitemid 38812905)
8. Zhang, Y., Zhu, H., Zhang, Q., Li, M., Yan, M., Wang, R., Wang, L., Welti, R., Zhang, W., and Wang, X. (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21, 2357-2377
9. 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
10. Raghavendra, A. S., Gonugunta, V. K., Christmann, A., and Grill, E. (2010) ABA perception and signaling. Trends Plant Sci. 15, 395-401
11. Hubbard, K. E., Nishimura, N., Hitomi, K., Getzoff, E. D., and Schroeder, J. I. (2010) Early abscisic acid signal transduction mechanisms. Newly discovered components and newly emerging questions. Genes Dev. 24, 1695-1708
12. Schroeder, J. I., Kwak, J. M., and Allen, G. J. (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410, 327-330 (Pubitemid 32246041)
13. Hirayama, T., and Shinozaki, K. (2007) Perception and transduction of abscisic acid signals. Keys to the function of the versatile plant hormone ABA. Trends Plant Sci. 12, 343-351 (Pubitemid 47187747)
14. Pandey, S., Nelson, D. C., and Assmann, S. M. (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell 136, 136-148
15. Park, S. Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T. F., Alfred, S. E., Bonetta, D., Finkelstein, R., Provart, N. J., Desveaux, D., Rodriguez, P. L., McCourt, P., Zhu, J. K., Schroeder, J. I., Volkman, B. F., and Cutler, S. R. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071
16. Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., and Grill, E. (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064-1068
17. Nishimura, N., Sarkeshik, A., Nito, K., Park, S. Y., Wang, A., Carvalho, P. C., Lee, S., Caddell, D. F., Cutler, S. R., Chory, J., Yates, J. R., and Schroeder, J. I. (2010) PYR/PYL/RCAR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 61, 290-299
18. Nishimura, N., Hitomi, K., Arvai, A. S., Rambo, R. P., Hitomi, C., Cutler, S. R., Schroeder, J. I., and Getzoff, E. D. (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326, 1373-1379
19. Shen, Y. Y., Wang, X. F., Wu, F. Q., Du, S. Y., Cao, Z., Shang, Y., Wang, X. L., Peng, C. C., Yu, X. C., Zhu, S. Y., Fan, R. C., Xu, Y. H., and Zhang, D. P. (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443, 823-826 (Pubitemid 44622688)
20. Liu, X., Yue, Y., Li, B., Nie, Y., Li, W., Wu, W. H., and Ma, L. (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315, 1712-1716 (Pubitemid 46515625)
21. Lu, B., and Benning, C. (2009) A 25-amino acid sequence of the Arabidopsis TGD2 protein is sufficient for specific binding of phosphatidic acid. J. Biol. Chem. 284, 17420-17427
22. Umezawa, T., Nakashima, K., Miyakawa, T., Kuromori, T., Tanokura, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010) Molecular basis of the core regulatory network in ABA responses. Sensing, signaling, and transport. Plant Cell Physiol. 51, 1821-1839
23. Lynch, D. V., Chen, M., and Cahoon, E. B. (2009) Lipid signaling in Arabidopsis. No sphingosine? No problem! Trends Plant Sci. 14, 463-466
24. Dunn, T. M., Lynch, D. V., Michaelson, L. V., and Napier, J. A. (2004) A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann. Bot. 93, 483-497 (Pubitemid 41295603)
25. Spiegel, S., and Milstien, S. (2003) Sphingosine-1-phosphate. An enigmatic signaling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407
26. Chen, M., Han, G., Dietrich, C. R., Dunn, T. M., and Cahoon, E. B. (2006) The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell 18, 3576-3593 (Pubitemid 46464913)
27. Chen, M., Markham, J. E., Dietrich, C. R., Jaworski, J. G., and Cahoon, E. B. (2008) Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 20, 1862-1878 (Pubitemid 352844538)
28. Ng, C. K., Carr, K., McAinsh, M. R., Powell, B., and Hetherington, A. M. (2001) Drought-induced guard cell signal transduction involves sphingosine 1-phosphate. Nature 410, 596-599 (Pubitemid 32267205)
29. Coursol, S., Fan, L. M., Le Stunff, H., Spiegel, S., Gilroy, S., and Assmann, S. M. (2003) Sphingolipid signaling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423, 651-654 (Pubitemid 36713226)
30. Coursol, S., Le Stunff, H., Lynch, D. V., Gilroy, S., Assmann, S. M., and Spiegel, S. (2005) Arabidopsis sphingosine kinase and the effects of phytosphingosine 1-phosphate on stomatal aperture. Plant Physiol. 137, 724-737 (Pubitemid 43126700)
31. Worrall, D., Liang, Y. K., Alvarez, S., Holroyd, G. H., Spiegel, S., Panagopulos, M., Gray, J. E., and Hetherington, A. M. (2008) Involvement of sphingosine kinase in plant cell signaling. Plant J. 56, 64-72
32. Michaelson, L. V., Zäuner, S., Markham, J. E., Haslam, R. P., Desikan, R., Mugford, S., Albrecht, S., Warnecke, D., Sperling, P., Heinz, E., and Napier, J. A. (2009) Functional characterization of a higher plant sphingolipid Delta4-desaturase. Defining the role of sphingosine and sphingosine 1-phosphate in Arabidopsis. Plant Physiol. 149, 487-498
33. Guo, L., Mishra, G., Taylor, K., and Wang, X. (2011) Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases. J. Biol. Chem. 286, 13336-13345
34. Li, M., Qin, C., Welti, R., and Wang, X. (2006) Double knockouts of phospholipases Dζ1 and Dζ2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol. 140, 761-770 (Pubitemid 43956294)
35. Yoo, S. D., Cho, Y. H., and Sheen, J. (2007) Arabidopsis mesophyll protoplasts. A versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572
36. Xiao, S., Gao, W., Chen, Q. F., Chan, S. W., Zheng, S. X., Ma, J., Wang, M., Welti, R., and Chye, M. L. (2010) Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. Plant Cell 22, 1463-1482
37. Markham, J. E., and Jaworski, J. G. (2007) Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Spectrom. 21, 1304-1314 (Pubitemid 46506586)
38. Devaiah, S. P., Roth, M. R., Baughman, E., Li, M., Tamura, P., Jeannotte, R., Welti, R., and Wang, X. (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dα1 knockout mutant. Phytochemistry 67, 1907-1924 (Pubitemid 44291405)
39. Imai, H., and Nishiura, H. (2005) Phosphorylation of sphingoid long-chain bases in Arabidopsis. Functional characterization and expression of the first sphingoid long-chain base kinase gene in plants. Plant Cell Physiol. 46, 375-380 (Pubitemid 40413241)
40. Liang, H., Yao, N., Song, J. T., Luo, S., Lu, H., and Greenberg, J. T. (2003) Ceramides modulate programmed cell death in plants. Genes Dev. 17, 2636-2641 (Pubitemid 37363068)
41. Anthony, R. G., Henriques, R., Helfer, A., Mészáros, T., Rios, G., Testerink, C., Munnik, T., Deák, M., Koncz, C., and Bögre, L. (2004) A protein kinase target of a PDK1 signaling pathway is involved in root hair growth in Arabidopsis. EMBO J. 23, 572-581 (Pubitemid 38282389)
42. Testerink, C., Larsen, P. B., van der Does, D., van Himbergen, J. A., and Munnik, T. (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J. Exp. Bot. 58, 3905-3914