Acyl chains of phospholipase D transphosphatidylation products in Arabidopsis cells: A study using multiple reaction monitoring mass spectrometry

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Rainteau, Dominique ^a   Humbert, Lydie ^a   Delage, Elise ^b,c   Vergnolle, Chantal ^b,c   Cantrel, Catherine ^b,c   Maubert, Marie Anne ^a   Lanfranchi, Sandrine ^b,c   Maldiney, Régis ^b,c   Collin, Sylvie ^b,c   Wolf, Claude ^a   Zachowski, Alain ^b,c   Ruelland, Eric ^b,c  

^a Centre National de la Recherche Scientifique   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BUTANOL; GLYCEROPHOSPHOLIPID; LIPID; PHOSPHATIDIC ACID; PHOSPHATIDYLBUTANOL; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPASE D; SALICYLIC ACID; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; ENZYME STRUCTURE; ENZYME SUBSTRATE; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; MICROSOME; MULTIPLE REACTION MONITORING MASS SPECTROMETRY; NONHUMAN; PLANT CELL; SIGNAL TRANSDUCTION;

ARABIDOPSIS; GLYCEROPHOSPHOLIPIDS; MASS SPECTROMETRY; PHOSPHATIDIC ACIDS; PHOSPHATIDYLCHOLINES; PHOSPHOLIPASE D; SALICYLIC ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84864356128     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041985     Document Type: Article

References (56)

1. Sun Y, Chen J, (2008) mTOR signaling: PLD takes center stage. Cell Cycle 7 3118-3123: doi.org/10.4161/cc.7.20.6881.
2. Roth MG, (2008) Molecular mechanisms of PLD function in membrane traffic. Traffic 9: 1233-1239 doi:10.1111/j.1600-0854.2008.00742.x.
3. Mane SP, Vasquez-Robinet C, Sioson AA, Heath LS, Grene R, (2007) Early PLDalpha-mediated events in response to progressive drought stress in Arabidopsis: a transcriptome analysis. J Exp Bot 58: 241-252 doi:10.1093/jxb/erl262.
4. Hong Y, Zheng S, Wang X, (2008) Dual functions of phospholipase Dalpha1 in plant response to drought. Mol Plant 1: 262-269 doi:10.1093/mp/ssm025.
5. Mishkind M, Vermeer JEM, Darwish E, Munnik T, (2009) Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J 60: 10-21 doi:10.1111/j.1365-313X.2009.03933.x.
6. Vergnolle C, Vaultier M-N, Taconnat L, Renou J-P, Kader J-C, 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 doi:10.1104/p.105.068171.
7. Krinke O, Flemr M, Vergnolle C, Collin S, Renou J-P, et al. (2009) Phospholipase D activation is an early component of the salicylic acid signaling pathway in Arabidopsis cell suspensions. Plant Physiol 150: 424-436 doi:10.1104/p.108.133595.
8. Bargmann BOR, Laxalt AM, ter Riet B, Testerink C, Merquiol E, et al. (2009) Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant Cell Environ 32: 837-850 doi:10.1111/j.1365-3040.2009.01962.x.
9. Zhang Y, Zhu H, Zhang Q, Li M, Yan M, et al. (2009) Phospholipase dalpha1 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 doi:10.1105/tpc.108.062992.
10. Zhang W, Qin C, Zhao J, 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 doi:10.1073/pnas.0402112101.
11. Testerink C, Larsen PB, van der Does D, van Himbergen JAJ, Munnik T, (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J Exp Bot 58: 3905-3914 doi:10.1093/jxb/erm243.
12. Wang X, Devaiah SP, Zhang W, Welti R, (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45: 250-278 doi:10.1016/j.plipres.2006.01.005.
13. Guo L, Mishra G, Taylor K, Wang X, (2011) Phosphatidic acid binds and stimulates Arabidopsis sphingosine kinases. J Biol Chem 286: 13336-13345 doi:10.1074/jbc.M110.190892.
14. Blom TS, Koivusalo M, Kuismanen E, Kostiainen R, Somerharju P, et al. (2001) Mass spectrometric analysis reveals an increase in plasma membrane polyunsaturated phospholipid species upon cellular cholesterol loading. Biochemistry 40: 14635-14644 doi:10.1021/bi0156714.
15. Fridriksson EK, Shipkova PA, Sheets ED, Holowka D, Baird B, et al. (1999) Quantitative analysis of phospholipids in functionally important membrane domains from RBL-2H3 mast cells using tandem high-resolution mass spectrometry. Biochemistry 38: 8056-8063 doi:10.1021/bi9828324.
16. Brügger B, Erben G, Sandhoff R, Wieland FT, Lehmann WD, (1997) Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 94: 2339-2344.
17. Welti R, Li W, Li M, Sang Y, Biesiada H, 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 doi:10.1074/jbc.M205375200.
18. Ejsing CS, Duchoslav E, Sampaio J, Simons K, Bonner R, et al. (2006) Automated identification and quantification of glycerophospholipid molecular species by multiple precursor ion scanning. Anal Chem 78: 6202-6214 doi:10.1021/ac060545x.
19. Schwudke D, Oegema J, Burton L, Entchev E, Hannich J, et al. (2006) Lipid profiling by multiple precursor and neutral loss scanning driven by the data-dependent acquisition RID A-3472-2009 RID D-2606-2009. Anal Chem 78: 585-595 doi:10.1021/ac051605m.
20. Steinhauer J, Gijón MA, Riekhof WR, Voelker DR, Murphy RC, et al. (2009) Drosophila lysophospholipid acyltransferases are specifically required for germ cell development. Mol Biol Cell 20: 5224-5235 doi:10.1091/mbc.E09-05-0382.
21. Shui G, Guan XL, Gopalakrishnan P, Xue Y, Goh JSY, et al. (2010) Characterization of substrate preference for Slc1p and Cst26p in Saccharomyces cerevisiae using lipidomic approaches and an LPAAT activity assay. PLoS ONE 5: e11956 doi:10.1371/journal.pone.0011956.
22. Arisz SA, Valianpour F, van Gennip AH, Munnik T, (2003) Substrate preference of stress-activated phospholipase D in Chlamydomonas and its contribution to PA formation. Plant J 34: 595-604.
23. Hsu F-F, Turk J, Williams TD, Welti R, (2007) Electrospray ionization multiple stage quadrupole ion-trap and tandem quadrupole mass spectrometric studies on phosphatidylglycerol from Arabidopsis leaves. J Am Soc Mass Spectrom 18: 783-790 doi:10.1016/j.jasms.2006.12.012.
24. Vaultier M-N, Cantrel C, Vergnolle C, Justin A-M, Demandre C, et al. (2006) Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells. FEBS Lett 580: 4218-4223 doi:10.1016/j.febslet.2006.06.083.
25. Burgos A, Szymanski J, Seiwert B, Degenkolbe T, Hannah MA, et al. (2011) Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light. Plant J 66: 656-668 doi:10.1111/j.1365-313X.2011.04531.x.
26. Qin C, 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 doi:10.1104/p.010928.
27. Pappan K, Austin-Brown S, Chapman KD, Wang X, (1998) Substrate selectivities and lipid modulation of plant phospholipase D alpha,-beta, and-gamma. Arch Biochem Biophys 353: 131-140 doi:10.1006/abbi.1998.0640.
28. Devaiah SP, Roth MR, Baughman E, Li M, Tamura P, et al. (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochem 67: 1907-1924 doi:10.1016/j.phytochem.2006.06.005.
29. Li M, Qin C, Welti R, Wang X, (2006) Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140: 761-770 doi:10.1104/p.105.070995.
30. Hong Y, Devaiah SP, Bahn SC, Thamasandra BN, Li M, et al. (2009) Phospholipase Dε and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. Plant J 58: 376-387 doi:10.1111/j.1365-313X.2009.03788.x.
31. Laloi M, Perret A-M, Chatre L, Melser S, Cantrel C, et al. (2006) Insights into the Role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143: 461-472 doi:10.1104/p.106.091496.
32. Tjellstrom H, Hellgren LI, Wieslander A, Sandelius AS, (2009) Lipid asymmetry in plant plasma membranes: phosphate deficiency-induced phospholipid replacement is restricted to the cytosolic leaflet. FASEB J 24: 1128-1138 doi:10.1096/fj.09-139410.
33. López-Marqués RL, Poulsen LR, Hanisch S, Meffert K, Buch-Pedersen MJ, et al. (2010) Intracellular targeting signals and lipid specificity determinants of the ALA/ALIS P4-ATPase complex reside in the catalytic ALA alpha-subunit. Mol Biol Cell 21: 791-801 doi:10.1091/mbc.E09-08-0656.
34. Holte LL, Peter SA, Sinnwell TM, Gawrisch K, (1995) 2H nuclear magnetic resonance order parameter profiles suggest a change of molecular shape for phosphatidylcholines containing a polyunsaturated acyl chain. Biophys J 68: 2396-2403 doi:10.1016/S0006-3495(95)80422-4.
35. Straume M, Litman BJ, (1987) Equilibrium and dynamic structure of large, unilamellar, unsaturated acyl chain phosphatidylcholine vesicles. Higher order analysis of 1,6-diphenyl-1,3,5-hexatriene and 1-[4-(trimethylammonio)phenyl]-6-phenyl-1,3,5-hexatriene anisotropy decay. Biochemistry 26: 5113-5120 doi:10.1021/bi00390a033.
36. Mitchell DC, Litman BJ, (1998) Molecular Order and Dynamics in Bilayers Consisting of Highly Polyunsaturated Phospholipids. Biophys J 74: 879-891 doi:10.1016/S0006-3495(98)74011-1.
37. Stubbs CD, Slater SJ, (1996) The effects of non-lamellar forming lipids on membrane protein-lipid interactions. Chem Phys Lipids 81: 185-195.
38. Wassall SR, Stillwell W, (2009) Polyunsaturated fatty acid-cholesterol interactions: Domain formation in membranes. Biochim Biophys Acta (BBA)- Biomembranes 1788: 24-32 doi:10.1016/j.bbamem.2008.10.011.
39. Han X, (2001) Quantitative analysis and molecular species fingerprinting of triacylglyceride molecular species directly from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry. Anal Biochem 295: 88-100 doi:10.1006/abio.2001.5178.
40. Demandre C, (1985) Analysis of molecular species of plant polar lipids by high-performance and gas liquid chromatography. Phytochem 24: 481-485 doi:10.1016/S0031-9422(00)80752-9.
41. Rouser G, Fkeischer S, Yamamoto A, (1970) Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5: 494-496.
42. Dippe M, Ulbrich-Hofmann R, (2009) Substrate specificity in phospholipid transformations by plant phospholipase D isoenzymes. Phytochem 70: 361-365 doi:10.1016/j.phytochem.2009.01.011.
43. Fan L, Zheng S, Cui D, Wang X, (1999) Subcellular distribution and tissue expression of phospholipase Dalpha, Dbeta, and Dgamma in Arabidopsis. Plant Physiol 119: 1371-1378.
44. Qin C, (2002) Kinetic Analysis of Arabidopsis Phospholipase Ddelta. Substrate Preference and Mechanism of Activation by Ca2+ and Phosphatidylinositol 4,5-Bisphosphate. J Biol Chem 277: 49685-49690 doi:10.1074/jbc.M209598200.
45. Franke WW, Deumling B, Baerbelermen, Jarasch ED, Kleinig H, (1970) Nuclear membranes from mammalian liver. I. Isolation procedure and general characterization. J Cell Biol 46: 379-395.
46. Vaultier M-N, Cantrel C, Guerbette F, Boutté Y, Vergnolle C, 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 doi:10.1016/j.febslet.2008.04.042.
47. Guillot-Salomon T, Farineau N, Cantrel C, Oursel A, Tuquet C, (1987) Isolation and characterisation of developing chloroplasts from light-grown barley leaves. Physiol Plant 69: 113-122 doi:10.1111/j.1399-3054.1987.tb01953.x.
48. Cantrel C, Caiveau O, Moreau F, Zachowski A, (2000) Lipid lateral diffusion and local microviscosity in plant mitochondrial membranes with various length and unsaturation of fatty acids. Physiol Plant 110: 443-449 doi:10.1111/j.1399-3054.2000.1100403.x.
49. Larsson C, Widell S, Kjellbom P, (1987) [52] Preparation of high-purity plasma membranes. Methods in Enzymology. Elsevier, Vol. 148: 558-568.
50. Morré DJ, Penel C, Morré DM, Sandelius AS, Moreau P, et al. (1991) Cell-free transfer and sorting of membrane lipids in spinach. Protoplasma 160: 49-64 doi:10.1007/BF01539956.
51. Whiteman S, Serazetdinova L, Jones AME, Sanders D, Rathjen J, et al. (2008) Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana. Proteomics 8: 3536-3547 doi:10.1002/pmic.200701104.
52. Folch J, Lees M, Sloane Stanley GH, (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
53. Jahn TP, Schulz A, Taipalensuu J, Palmgren MG, (2002) Post-translational modification of plant plasma membrane H(+)-ATPase as a requirement for functional complementation of a yeast transport mutant. J Biol Chem 277: 6353-6358 doi:10.1074/jbc.M109637200.
54. Chatre L, Brandizzi F, Hocquellet A, Hawes C, Moreau P, (2005) Sec22 and Memb11 are v-SNAREs of the anterograde endoplasmic reticulum-Golgi pathway in tobacco leaf epidermal cells. Plant Physiol 139: 1244-1254 doi:10.1104/p.105.067447.
55. Elthon TE, Nickels RL, McIntosh L, (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiol 89: 1311-1317.
56. Boutte Y, Frescatada-Rosa M, Men S, Chow C-M, Ebine K, et al. (2010) Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis RID G-6984-2011. EMBO J 29: 546-558 doi:10.1038/emboj.2009.363.