Lipidomics in situ: Insights into plant lipid metabolism from high resolution spatial maps of metabolites

Progress in Lipid Research

Volumn 54, Issue 1, 2014, Pages 32-52

  Horn, Patrick J ^a   Chapman, Kent D ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Lipids; MALDI; Mass spectrometry imaging; Phospholipids; Seeds; Triacylglycerols

Indexed keywords

LIPIDS; MALDI; MASS SPECTROMETRY IMAGING; PHOSPHOLIPIDS; SEEDS; TRIACYLGLYCEROLS;

LIPID METABOLISM; MASS SPECTROMETRY; METABOLOMICS; MOLECULAR IMAGING; PLANTS;

EID: 84893842377     PISSN: 01637827     EISSN: 18732194     Source Type: Journal    
DOI: 10.1016/j.plipres.2014.01.003     Document Type: Review

References (178)

1. L.A. McDonnell, R. Heeren, P.E. Andrén, M. Stoeckli, and G.L. Corthals Going forward: increasing the accessibility of imaging mass spectrometry J Proteomics 75 2012 5113 5121
2. Y.J. Lee, D.C. Perdian, Z. Song, E.S. Yeung, and B.J. Nikolau Use of mass spectrometry for imaging metabolites in plants Plant J 70 2012 81 95
3. J.L. Norris, and R.M. Caprioli Analysis of tissue specimens by matrix-assisted laser desorption/ionization imaging mass spectrometry in biological and clinical research Chem Rev 113 2013 2309 2342
4. J.H. Jungmann, and R.M.A. Heeren Emerging technologies in mass spectrometry imaging J Proteomics 16 2012 5077 5092
5. S.G. Boxer, M.L. Kraft, and P.K. Weber Advances in imaging secondary ion mass spectrometry for biological samples Annu Rev Biophys 38 2009 53 74
6. M.K. Passarelli, and N. Winograd Lipid imaging with time-of-flight secondary ion mass spectrometry (ToF-SIMS) Biochim Biophys Acta Mol Cell Biol Lipids 1811 2011 976 990
7. R. Castaing, and G. Slodzian Microanalyse par émission ionique secondaire J Microsc 1 1962 395 410
8. A. Benninghoven, and E. Loebach Tandem mass spectrometer for secondary ion studies Rev Sci Instrum 42 1971 49 52
9. B.T. Chait, and K.G. Standing A time-of-flight mass spectrometer for measurement of secondary ion mass spectra Int J Mass Spectrom Ion Phys 40 1981 185 193
10. B. Johansson ToF-SIMS imaging of lipids in cell membranes Surf Interface Anal 38 2006 1401 1412 (Pubitemid 44729087)
11. A. Brunelle, and O. Laprévote Lipid imaging with cluster time-of-flight secondary ion mass spectrometry Anal Bioanal Chem 393 2009 31 35 (Pubitemid 50263826)
12. R.M. Braun, A. Beyder, J. Xu, M.C. Wood, A.G. Ewing, and N. Winograd Spatially resolved detection of attomole quantities of organic molecules localized in picoliter vials using time-of-flight secondary ion mass spectrometry Anal Chem 71 1999 3318 3324
13. H. Nygren, K. Börner, P. Malmberg, E. Tallarek, and B. Hagenhoff Imaging TOF-SIMS of rat kidney prepared by high-pressure freezing Microsc Res Tech 68 2005 329 334 (Pubitemid 46196552)
14. H.-J. Yang, I. Ishizaki, N. Sanada, N. Zaima, Y. Sugiura, and I. Yao et al. Detection of characteristic distributions of phospholipid head groups and fatty acids on neurite surface by time-of-flight secondary ion mass spectrometry Med Mol Morphol 43 2010 158 164
15. J.S. Fletcher, N.P. Lockyer, S. Vaidyanathan, and J.C. Vickerman TOF-SIMS 3D biomolecular imaging of Xenopus laevis oocytes using buckminsterfullerene (C60) primary ions Anal Chem 79 2007 2199 2206 (Pubitemid 46448998)
16. M.K. Passarelli, and N. Winograd Characterizing in situ glycerophospholipids with SIMS and MALDI methodologies Surf Interface Anal 43 2011 269 271
17. A. Seyer, J. Einhorn, A. Brunelle, and O. Laprévote Localization of flavonoids in seeds by cluster time-of-flight secondary ion mass spectrometry imaging Anal Chem 82 2010 2326 2333
18. Z. Takáts, J.M. Wiseman, B. Gologan, and R.G. Cooks Mass spectrometry sampling under ambient conditions with desorption electrospray ionization Science 306 2004 471 473 (Pubitemid 39372443)
19. B. Li, C. Knudsen, N.K. Hansen, K. Jørgensen, R. Kannangara, and S. Bak et al. Visualizing metabolite distribution and enzymatic conversion in plant tissues by desorption electrospray ionization mass spectrometry imaging Plant J 74 2013 1059 1071
20. A.L. Dill, D.R. Ifa, N.E. Manicke, Z. Ouyang, and R.G. Cooks Mass spectrometric imaging of lipids using desorption electrospray ionization J Chrom B 877 2009 2883 2889
21. G.A. Harris, A.S. Galhena, and F.M. Fernández Ambient sampling/ionization mass spectrometry: applications and current trends Anal Chem 83 2011 4508 4538
22. D. Campbell, C. Ferreira, L. Eberlin, and R.G. Cooks Improved spatial resolution in the imaging of biological tissue using desorption electrospray ionization Anal Bioanal Chem 404 2012 389 398
23. S.R. Ellis, S.H. Brown, M. In Het Panhuis, S.J. Blanksby, and T.W. Mitchell Surface analysis of lipids by mass spectrometry: more than just imaging Prog Lipid Res 52 2013 329 353
24. T. Müller, S. Oradu, D.R. Ifa, R.G. Cooks, and B. Kräutler Direct plant tissue analysis and imprint imaging by desorption electrospray ionization mass spectrometry Anal Chem 83 2011 5754 5761
25. B. Li, S.H. Hansen, and C. Janfelt Direct imaging of plant metabolites in leaves and petals by desorption electrospray ionization mass spectrometry Int J Mass Spectrom 348 2013 15 22
26. J. Thunig, S.H. Hansen, and C. Janfelt Analysis of secondary plant metabolites by indirect desorption electrospray ionization imaging mass spectrometry Anal Chem 83 2011 3256 3259
27. D.R. Ifa, A. Srimany, L.S. Eberlin, H.R. Naik, V. Bhat, and R.G. Cooks et al. Tissue imprint imaging by desorption electrospray ionization mass spectrometry Anal Methods 3 2011 1910 1912
28. J.A. Fernandez, B. Ochoa, O. Fresnedo, M.T. Giralt, and R. Rodriguez-Puertas Matrix-assisted laser desorption ionization imaging mass spectrometry in lipidomics Anal Bioanal Chem 401 2011 29 51
29. D. Gode, and D.A. Volmer Lipid imaging by mass spectrometry - a review Analyst 138 2013 1289 1315
30. A. Kiss, J.H. Jungmann, D.F. Smith, and R. Heeren Microscope mode secondary ion mass spectrometry imaging with a Timepix detector Rev Sci Instrum 84 2013 013704-013704
31. W.W. Wu, G. Wang, S.J. Baek, and R.-F. Shen Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel-or LC-MALDI TOF/TOF J Proteome Res 5 2006 651 658 (Pubitemid 43364106)
32. B. Fuchs, R. Süß, and J. Schiller An update of MALDI-TOF mass spectrometry in lipid research Prog Lipid Res 49 2010 450 475
33. H. Zhang, S. Cha, and E.S. Yeung Colloidal graphite-assisted laser desorption/ionization MS and MS(n) of small molecules. 2. Direct profiling and MS imaging of small metabolites from fruits Anal Chem 79 2007 6575 6584 (Pubitemid 47395041)
34. S. Cha, H. Zhang, H.I. Ilarslan, E.S. Wurtele, L. Brachova, and B.J. Nikolau et al. Direct profiling and imaging of plant metabolites in intact tissues by using colloidal graphite-assisted laser desorption ionization mass spectrometry Plant J 55 2008 348 360
35. J.H. Jun, Z. Song, Z. Liu, B.J. Nikolau, E.S. Yeung, and Y.J. Lee High-spatial and high-mass resolution imaging of surface metabolites of Arabidopsis thaliana by laser desorption-ionization mass spectrometry using colloidal silver Anal Chem 82 2010 3255 3265
36. V. Vrkoslav, A. Muck, J. Cvacka, and A. Svatos MALDI imaging of neutral cuticular lipids in insects and plants J Am Soc Mass Spectrom 21 2010 220 231
37. N. Zaima, N. Goto-Inoue, T. Hayasaka, and M. Setou Application of imaging mass spectrometry for the analysis of Oryza sativa rice Rapid Commun Mass Spectrom 24 2010 2723 2729
38. S. Taira, R. Ikeda, N. Yokota, I. Osaka, M. Sakamoto, and M. Kato et al. Mass spectrometric imaging of ginsenosides localization in Panax ginseng root Am J Chin Med 38 2010 485 493
39. S. Taira, S. Shimma, I. Osaka, D. Kaneko, Y. Ichiyanagi, and R. Ikeda et al. Mass spectrometry imaging of the capsaicin localization in the capsicum fruits Int J Biotechnol Wellness Ind 1 2012 61 65
40. H. Ye, E. Gemperline, M. Venkateshwaran, R. Chen, P.M. Delaux, and M. Howes-Podoll et al. MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula-Sinorhizobium meliloti symbiosis Plant J 75 2013 130 145
41. P.J. Horn, A.R. Korte, P.B. Neogi, E. Love, J. Fuchs, and K. Strupat et al. Spatial mapping of lipids at cellular resolution in embryos of cotton Plant Cell 24 2012 622 636
42. P.J. Horn, D. Sturtevant, and K.D. Chapman Modified oleic cottonseeds show altered content, composition and tissue-specific distribution of triacylglycerol molecular species Biochimie 96 2014 28 36
43. P.J. Horn, J.E. Silva, D. Anderson, J. Fuchs, L. Borisjuk, and T.J. Nazarenus et al. Imaging heterogeneity of membrane and storage lipids in transgenic Camelina sativa seeds with altered fatty acid profiles Plant J 76 2013 138 150
44. Vanhercke T, El Tahchy A, Liu Q, Zhou X-R, Shrestha P, Diva U, et al. Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J 2013; doi: 10.1111/pbi.12131. [Epub ahead of print].
45. P.J. Horn, C.N. James, S. Gidda, A. Kilaru, J.M. Dyer, and R.T. Mullen et al. Identification of a new class of lipid droplet-associated proteins in plants Plant Physiol 162 2013 1926 1936
46. P.J. Horn, and K.D. Chapman Metabolite Imager: customized spatial analysis of metabolite distributions in mass spectrometry imaging Metabolomics J 2013 10.1007/s11306-013-0575-0
47. D.C. Perdian, and Y.J. Lee Imaging MS methodology for more chemical information in less data acquisition time utilizing a hybrid linear ion trap-orbitrap mass spectrometer Anal Chem 82 2010 9393 9400
48. Verhaert PEM, Pinkse MH, Strupat K, Conaway MP. Imaging of similar mass neuropeptides in neuronal tissue by enhanced resolution MALDI MS with an ion trap-OrbitrapTM hybrid instrument. In: Rubakhin SS, Sweedler JV, editors. Mass spectrometry imaging. Humana Press; 2010. p. 433-49.
49. L.A. McDonnell, A. van Remoortere, N. de Velde, R.J.M. van Zeijl, and A.M. Deelder Imaging mass spectrometry data reduction: automated feature identification and extraction J Am Soc Mass Spectrom 21 2010 1969 1978
50. P. Källback, M. Shariatgorji, A. Nilsson, and P.E. Andrén Novel mass spectrometry imaging software assisting labeled normalization and quantitation of drugs and neuropeptides directly in tissue sections J Proteomics 75 2012 4941 4951
51. X. Xiong, W. Xu, L. Eberlin, J. Wiseman, X. Fang, and Y. Jiang et al. Data processing for 3D mass spectrometry imaging J Am Soc Mass Spectrom 23 2012 1147 1156
52. T. Schramm, A. Hester, I. Klinkert, J.-P. Both, and R.M.A. Heeren et al. ImzML - a common data format for the flexible exchange and processing of mass spectrometry imaging data J Proteomics 75 2012 5106 5110
53. B.K. Kaletaş, I.M. van der Wiel, J. Stauber, J.D. Lennard, C. Güzel, and J.M. Kros et al. Sample preparation issues for tissue imaging by imaging MS Proteomics 9 2009 2622 2633
54. S.A. Schwartz, M.L. Reyzer, and R.M. Caprioli Direct tissue analysis using matrix-assisted laser desorption/ionization mass spectrometry: practical aspects of sample preparation J Mass Spectrom 38 2003 699 708 (Pubitemid 36950300)
55. R.J. Goodwin Sample preparation for mass spectrometry imaging: small mistakes can lead to big consequences J Proteomics 75 2012 4893 4911
56. Chaurand P, Cornett DS, Angel PM, Caprioli RM. From whole-body sections down to cellular level, multiscale imaging of phospholipids by MALDI mass spectrometry. Mol Cell Proteomics 2011; 10. doi: 10.1074/mcp.O110.004259.
57. P. Hart, S. Francese, E. Claude, M.N. Woodroofe, and M. Clench MALDI-MS imaging of lipids in ex vivo human skin Anal Bioanal Chem 401 2011 115 125
58. P.M. Angel, J.M. Spraggins, H.S. Baldwin, and R. Caprioli Enhanced sensitivity for high spatial resolution lipid analysis by negative ion mode MALDI imaging mass spectrometry Anal Chem 84 2012 1557 1564
59. E.H. Seeley, and R.M. Caprioli MALDI imaging mass spectrometry of human tissue: method challenges and clinical perspectives Trends Biotechnol 29 2011 136 143
60. Y. Sugiura, N. Zaima, M. Setou, S. Ito, and I. Yao Visualization of acetylcholine distribution in central nervous system tissue sections by tandem imaging mass spectrometry Anal Bioanal Chem 403 2012 1851 1861
61. A. Walch, S. Rauser, S.-O. Deininger, and H. Höfler MALDI imaging mass spectrometry for direct tissue analysis: a new frontier for molecular histology Histochem Cell Biol 130 2008 421 434
62. S. Kaspar, M. Peukert, A. Svatos, A. Matros, and H.-P. Mock MALDI-imaging mass spectrometry - an emerging technique in plant biology Proteomics 11 2011 1840 1850
63. Y. Chen, J. Allegood, Y. Liu, E. Wang, B. Cachon-Gonzalez, and T.M. Cox et al. Imaging MALDI mass spectrometry using an oscillating capillary nebulizer matrix coating system and its application to analysis of lipids in brain from a mouse model of Tay-Sachs/Sandhoff disease Anal Chem 80 2008 2780 2788 (Pubitemid 351556439)
64. M.L. Reyzer, P. Chaurand, P.M. Angel, and R.M. Caprioli Direct molecular analysis of whole-body animal tissue sections by MALDI imaging mass spectrometry Methods Mol Biol 656 2010 285 301
65. R. Kruse, and J. Sweedler Spatial profiling invertebrate ganglia using MALDI MS J Am Soc Mass Spectrom 14 2003 752 759 (Pubitemid 36870958)
66. M. Stoeckli, D. Staab, and A. Schweitzer Compound and metabolite distribution measured by MALDI mass spectrometric imaging in whole-body tissue sections Int J Mass Spectrom 260 2007 195 202
67. Y. Sugiura, S. Shimma, and M. Setou Thin sectioning improves the peak intensity and signal-to-noise ratio in direct tissue mass spectrometry J Mass Spectrom Soc Jap 54 2006 45 48
68. N. Goto-Inoue, T. Hayasaka, N. Zaima, and M. Setou Imaging mass spectrometry for lipidomics Biochim Biophys Acta Mol Cell Biol Lipids 1811 2011 961 969
69. T. Kawamoto Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants Arch Histol Cytol 66 2003 123 143 (Pubitemid 36834422)
70. J. Malm, D. Giannaras, M.O. Riehle, N. Gadegaard, and P. Sjövall Fixation and drying protocols for the preparation of cell samples for time-of-flight secondary ion mass spectrometry analysis Anal Chem 81 2009 7197 7205
71. R. Zenobi, and R. Knochenmuss Ion formation in MALDI mass spectrometry Mass Spectrom Rev 17 1998 337 366 (Pubitemid 128628191)
72. J. Schiller, R. Süß, B. Fuchs, M. Müller, M. Petković, and O. Zschörnig et al. The suitability of different DHB isomers as matrices for the MALDI-TOF MS analysis of phospholipids: which isomer for what purpose? Eur Biophys J 36 2007 517 527 (Pubitemid 46626207)
73. G. Sun, K. Yang, Z. Zhao, S. Guan, X. Han, and R.W. Gross Matrix-assisted laser desorption/ionization time-of-flight mass spectrometric analysis of cellular glycerophospholipids enabled by multiplexed solvent dependent analyte-matrix interactions Anal Chem 80 2008 7576 7585
74. B. Fuchs, A. Bischoff, R. Süß, K. Teuber, M. Schürenberg, and D. Suckau et al. Phosphatidylcholines and -ethanolamines can be easily mistaken in phospholipid mixtures: a negative ion MALDI-TOF MS study with 9-aminoacridine as matrix and egg yolk as selected example Anal Bioanal Chem 395 2009 2479 2487
75. G. Stübiger, and O. Belgacem Analysis of lipids using 2,4,6-trihydroxyacetophenone as a matrix for MALDI mass spectrometry Anal Chem 79 2007 3206 3213 (Pubitemid 46640545)
76. P. Lorkiewicz, and M. Cecilia Yappert 2-(2-Aminoethylamino)-5- nitropyridine as a basic matrix for negative-mode matrix-assisted laser desorption/ionization analysis of phospholipids J Mass Spectrom 44 2009 137 143
77. S.N. Jackson, H.-Y.J. Wang, A.S. Woods, M. Ugarov, T. Egan, and J.A. Schultz Direct tissue analysis of phospholipids in rat brain using MALDI-TOFMS and MALDI-ion mobility-TOFMS J Am Soc Mass Spectrom 16 2005 133 138 (Pubitemid 40203136)
78. B. Spengler, D. Kirsch, and R. Kaufmann Fundamental aspects of postsource decay in matrix-assisted laser desorption mass spectrometry. 1. Residual gas effects J Phys Chem 96 1992 9678 9684
79. K.A. Al-Saad, V. Zabrouskov, W.F. Siems, N.R. Knowles, R.M. Hannan, and H.H. Hill Jr. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry of lipids: ionization and prompt fragmentation patterns Rapid Commun Mass Spectrom 17 2003 87 96 (Pubitemid 36019887)
80. G. Picariello, R. Romano, and F. Addeo Nitrocellulose film substrate minimizes fragmentation in matrix-assisted laser desorption ionization time-of-flight mass spectrometry analysis of triacylglycerols Anal Chem 82 2010 5783 5791
81. B. Emerson, J. Gidden, J.O. Lay, and B. Durham A rapid separation technique for overcoming suppression of triacylglycerols by phosphatidylcholine using MALDI-TOF MS J Lipid Res 51 2010 2428 2434
82. K.A.Z. Berry, B. Li, S.D. Reynolds, R.M. Barkley, M.A. Gijón, and J.A. Hankin et al. MALDI imaging MS of phospholipids in the mouse lung J Lipid Res 52 2011 1551 1560
83. D. Hölscher, R. Shroff, K. Knop, M. Gottschaldt, A. Crecelius, and B. Schneider et al. Matrix-free UV-laser desorption/ionization (LDI) mass spectrometric imaging at the single-cell level: distribution of secondary metabolites of Arabidopsis thaliana and Hypericum species Plant J 60 2009 907 918
84. J. Nizioł, W. Rode, Z. Zieliński, and T. Ruman Matrix-free laser desorption-ionization with silver nanoparticle-enhanced steel targets Int J Mass Spectrom 335 2013 22 32
85. S.L. Koeniger, N. Talaty, Y. Luo, D. Ready, M. Voorbach, and T. Seifer et al. A quantitation method for mass spectrometry imaging Rapid Commun Mass Spectrom 25 2011 503 510
86. D.A. Pirman, R.F. Reich, A. Kiss, R.M.A. Heeren, and R.A. Yost Quantitative MALDI tandem mass spectrometric imaging of cocaine from brain tissue with a deuterated internal standard Anal Chem 85 2012 1081 1089
87. T. Kind, and O. Fiehn Metabolomic database annotations via query of elemental compositions: mass accuracy is insufficient even at less than 1 ppm BMC Bioinf 7 2006 234
88. C.F. Taylor, P.A. Binz, R. Aebersold, M. Affolter, R. Barkovich, and E.W. Deutsch et al. Guidelines for reporting the use of mass spectrometry in proteomics Nature 26 2008 860 861
89. O. Fiehn, D. Robertson, J. Griffin, M. van der Werf, B. Nikolau, and N. Morrison et al. The metabolomics standards initiative (MSI) Metabolomics 3 2007 175 178 (Pubitemid 47470685)
90. C. Lu, J.A. Napier, T.E. Clemente, and E.B. Cahoon New frontiers in oilseed biotechnology: meeting the global demand for vegetable oils for food, feed, biofuel, and industrial applications Curr Opin Biotechnol 22 2011 252 259
91. K.D. Chapman, and J.B. Ohlrogge Compartmentation of triacylglycerol accumulation in plants J Biol Chem 287 2012 2288 2294
92. P.D. Bates, S. Stymne, and J. Ohlrogge Biochemical pathways in seed oil synthesis Curr Opin Plant Biol 16 2013 358 364
93. A.R. Snapp, and C. Lu Engineering industrial fatty acids in oilseeds Front Biol 8 2012 1 10
94. Y. Li-Beisson, B. Shorrosh, F. Beisson, M.X. Andersson, V. Arondel, and P.D. Bates et al. Acyl-lipid metabolism Arabidop Book 2013 e0161
95. J.L. Harwood Recent advances in the biosynthesis of plant fatty acids Biochim Biophys Acta 1301 1996 7 56 (Pubitemid 26193061)
96. J.B. Ohlrogge, D.N. Kuhn, and P.K. Stumpf Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea Proc Nat Acad Sci U S A 76 1979 1194 1198 (Pubitemid 9135180)
97. J. Schwender, Y. Shachar-Hill, and J.B. Ohlrogge Mitochondrial metabolism in developing embryos of Brassica napus J Biol Chem 281 2006 34040 34047 (Pubitemid 46036613)
98. J. Ohlrogge, and J. Browse Lipid biosynthesis Plant Cell 7 1995 957 970
99. H. Tjellström, Z. Yang, D.K. Allen, and J.B. Ohlrogge Rapid kinetic labeling of Arabidopsis cell suspension cultures: implications for models of lipid export from plastids Plant Physiol 158 2012 601 611
100. M. Ghanevati, and J.G. Jaworski Engineering and mechanistic studies of the arabidopsis FAE1 β-ketoacyl-CoA synthase, FAE1 KCS Eur J Biochem 269 2002 3531 3539 (Pubitemid 34988997)
101. M. Rossak, M. Smith, and L. Kunst Expression of the FAE1 gene and FAE1 promoter activity in developing seeds of Arabidopsis thaliana Plant Mol Biol 46 2001 717 725 (Pubitemid 32900925)
102. J. Okuley, J. Lightner, K. Feldmann, N. Yadav, E. Lark, and J. Browse Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid synthesis Plant Cell 6 1994 147 158
103. B. Lemieux, M. Miquel, C. Somerville, and J. Browse Mutants of Arabidopsis with alterations in seed lipid fatty acid composition Theor Appl Genet 80 1990 234 240
104. J.A. Napier, and I.A. Graham Tailoring plant lipid composition: designer oilseeds come of age Curr Opin Plant Biol 13 2010 329 336
105. R. Welti, W. Li, M. Li, Y. Sang, H. Biesiada, and H.E. Zhou et al. Profiling membrane lipids in plant stress responses J Biol Chem 277 2002 31994 32002
106. D.T. Canvin The effect of temperature on the oil content and fatty acid composition of the oils from several oil seed crops Can J Bot 43 1965 63 69
107. P.D. Bates, A. Fatihi, A.R. Snapp, A.S. Carlsson, and C. Lu Acyl editing and headgroup exchange are the major mechanisms that direct polyunsaturated fatty acid flux into triacylglycerols Plant Physiol 160 2012 1530 1539
108. X. Bao, S. Katz, M. Pollard, and J. Ohlrogge Carbocyclic fatty acids in plants: Biochemical and molecular genetic characterization of cyclopropane fatty acid synthesis of Sterculia foetida Proc Nat Acad Sci U S A 99 2002 7172 7177 (Pubitemid 34526274)
109. X. Bao, J. Thelen, G. Bonaventure, and J. Ohlrogge Characterization of cyclopropane fatty-acid synthase from Sterculia foetida J Biol Chem 278 2003 12846 12853 (Pubitemid 36800048)
110. X.-H. Yu, R. Rawat, and J. Shanklin Characterization and analysis of the cotton cyclopropane fatty acid synthase family and their contribution to cyclopropane fatty acid synthesis BMC Plant Biol 11 2011 97
111. C. Lu, Z. Xin, Z. Ren, M. Miquel, and J. Browse An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis Proc Nat Acad Sci U S A 106 2009 18837 18842
112. A. Dahlqvist, U. Ståhl, M. Lenman, A. Banas, M. Lee, and L. Sandager et al. Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants Proc Nat Acad Sci U S A 97 2000 6487 6492 (Pubitemid 30412740)
113. K.M. Schmid, and G.W. Patterson Distribution of cyclopropenoid fatty acids in malvaceous plant parts Phytochemistry 27 1988 2831 2834
114. X. Jiao, X. Zhao, X.-R. Zhou, A.G. Green, Y. Fan, and L. Wang et al. Comparative transcriptomic analysis of developing cotton cotyledons and embryo axis PloS One 8 2013 e71756
115. M. Miquel Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase J Biol Chem 267 1992 1502 1509
116. D. Zhang, I.L. Pirtle, S.J. Park, M. Nampaisansuk, P. Neogi, and S.W. Wanjie et al. Identification and expression of a new delta-12 fatty acid desaturase (FAD2-4) gene in upland cotton and its functional expression in yeast and Arabidopsis thaliana plants Plant Physiol Biochem 47 2009 462 471
117. Q. Liu, S.P. Singh, C.L. Brubaker, P.J. Sharp, A.G. Green, and D.R. Marhsall Molecular cloning and expression of a cDNA encoding a microsomal w-6 fatty acid desaturase from cotton (Gossypium hirsutum) Funct Plant Biol 26 1999 101 106
118. J. Shanklin, and E.B. Cahoon Desaturation and related modifications of fatty acids Ann Rev Plant Biol 49 1998 611 641
119. J. Broadwater, E. Whittle, and J. Shanklin Desaturation and hydroxylation. Residues 148 and 324 of Arabidopsis FAD2, in addition to substrate chain length, exert a major influence in partitioning of catalytic specificity J Biol Chem 277 2002 15613 15620 (Pubitemid 34967832)
120. H. Rolletschek, L. Borisjuk, A. Sánchez-García, C. Gotor, L.C. Romero, and J.M. Martínez-Rivas et al. Temperature-dependent endogenous oxygen concentration regulates microsomal oleate desaturase in developing sunflower seeds J Exp Bot 58 2007 3171 3181 (Pubitemid 350060409)
121. A.J. Kinney, E.B. Cahoon, and W.D. Hitz Manipulating desaturase activities in transgenic crop plants Biochem Soc Trans 30 2002 1099
122. R.F. Wilson The role of genomics and biotechnology in achieving global food security for high-oleic vegetable oil J Oleo Sci 61 2012 357 367
123. K.D. Chapman, P.B. Neogi, K.D. Hake, A.A. Stawska, T.R. Speed, and M.Q. Cotter et al. Reduced oil accumulation in cottonseeds transformed with a nonfunctional allele of a delta-12 fatty acid desaturase (FAD2) Crop Sci 48 2008 1470 1481
124. K. Chapman, S. Austin-Brown, S. Sparace, A. Kinney, K. Ripp, and I.L. Pirtle et al. Transgenic cotton plants with increased seed oleic acid content J Am Oil Chem Soc 78 2001 941 947 (Pubitemid 33113985)
125. Q. Liu, S.P. Singh, and A.G. Green High-stearic and high-oleic cottonseed oils produced by hairpin RNA-mediated post-transcriptional gene silencing Plant Physiol 129 2002 1732 1743 (Pubitemid 34923237)
126. C. Jako, A. Kumar, Y. Wei, J. Zou, D.L. Barton, and E.M. Giblin et al. Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight Plant Physiol 126 2001 861 874 (Pubitemid 32568815)
127. M. Zhang, J. Fan, D.C. Taylor, and J.B. Ohlrogge DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development Plant Cell 21 2009 3885 3901
128. U. Ståhl, A.S. Carlsson, M. Lenman, A. Dahlqvist, B. Huang, and A. Banas et al. Cloning and Functional characterization of a phospholipid: diacylglycerol acyltransferase from Arabidopsis Plant Physiol 135 2004 1324 1335 (Pubitemid 39009381)
129. W. Banaś, A.S. Garcia, A. Banaś, and S. Stymne Activities of acyl-CoA: diacylglycerol acyltransferase (DGAT) and phospholipid: diacylglycerol acyltransferase (PDAT) in microsomal preparations of developing sunflower and safflower seeds Planta 6 2013 1 10
130. L. Borisjuk, H. Rolletschek, and T. Neuberger Surveying the plant's world by magnetic resonance imaging Plant J 70 2012 129 146
131. T. Neuberger, N. Sreenivasulu, M. Rokitta, H. Rolletschek, C. Göbel, and T. Rutten et al. Quantitative imaging of oil storage in developing crop seeds Plant Biotechnol J 6 2008 31 45 (Pubitemid 350233583)
132. Neuberger T, Rolletschek H, Webb A, Borisjuk L. Non-invasive mapping of lipids in plant tissue using magnetic resonance imaging. In: Armstrong D, editor. Lipidomics. Humana Press; 2009. p. 485-96.
133. J. Fuchs, T. Neuberger, H. Rolletschek, S. Schiebold, T.H. Nguyen, and N. Borisjuk et al. A non-invasive platform for imaging and quantifying oil storage in sub-millimetre tobacco seed Plant Physiol 161 2013 583 593
134. S. Baud, and L. Lepiniec Physiological and developmental regulation of seed oil production Prog Lipid Res 49 2010 235 249
135. P.D. Bates, and J. Browse The pathway of triacylglycerol synthesis through phosphatidylcholine in Arabidopsis produces a bottleneck for the accumulation of unusual fatty acids in transgenic seeds Plant J 68 2011 387 399
136. J. Browse, N. Warwick, C.R. Somerville, and C.R. Slack Fluxes through the prokaryotic and eukaryotic pathways of lipid synthesis in the '16:3' plant Arabidopsis thaliana Biochem J 235 1986 25 31
137. P.D. Bates, T.P. Durrett, J.B. Ohlrogge, and M. Pollard Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos Plant Physiol 150 2009 55 72
138. J. Mizoi, M. Nakamura, and I. Nishida Defects in CTP: phosphrylethanolamine cytidylyltransferase affect embryonic and postembryonic development in Arabidopsis Plant Cell 18 2006 3370 3385 (Pubitemid 46464899)
139. D. Coulon, L. Faure, M. Salmon, V. Wattelet, and J.-J. Bessoule Occurrence, biosynthesis and functions of N-acylphosphatidylethanolamines (NAPE): not just precursors of N-acylethanolamines (NAE) Biochimie 94 2012 75 85
140. X. Wang, S.P. Devaiah, W. Zhang, and R. Welti Signaling functions of phosphatidic acid Prog Lipid Res 45 2006 250 278
141. C. Testerink, and T. Munnik Phosphatidic acid: a multifunctional stress signaling lipid in plants Trends Plant Sci 10 2005 368 375 (Pubitemid 41059664)
142. S.N. Jackson, H.-Y.J. Wang, and A.S. Woods In situ structural characterization of phosphatidylcholines in brain tissue using MALDI-MS/MS J Am Soc Mass Spectrom 16 2005 2052 2056 (Pubitemid 41642968)
143. T. Katagiri, K. Ishiyama, T. Kato, S. Tabata, M. Kobayashi, and K. Shinozaka An important role of phosphatidic acid in ABA signaling during germination in Arabidopsis thaliana Plant J 43 2005 107 117 (Pubitemid 40962739)
144. A.L. Villasuso, M.A. Di Palma, M. Aveldaño, S.J. Pasquaré, G. Racagni, and N.M. Giusto et al. Differences in phosphatidic acid signalling and metabolism between ABA and GA treatments of barley aleurone cells Plant Physiol Biochem 65 2013 1 8
145. C.D. Cerruti, F. Benabdellah, O. Laprévote, D. Touboul, and A. Brunelle MALDI imaging and structural analysis of rat brain lipid negative ions with 9-aminoacridine matrix Anal Chem 84 2012 2164 2171
146. G. Wang, S. Ryu, and X. Wang Plant phospholipases: an overview. Lipases and phospholipases 2012 Springer p. 123-37
147. W.F. Boss, and Y.J. Im Phosphoinositide signaling Annu Rev Plant Biol 63 2012 409 429
148. Y. Kim, S.R. Shanta, L.-H. Zhou, and K.P. Kim Mass spectrometry based cellular phosphoinositides profiling and phospholipid analysis: a brief review Exp Mol Med 42 2010 1 11
149. A.R. Korte, and Y.J. Lee Multiplex mass spectrometric imaging with polarity switching for concurrent acquisition of positive and negative ion images J Am Soc Mass Spectrom 24 2013 1 7
150. M. Kawashima, N. Iwamoto, N. Kawaguchi-Sakita, M. Sugimoto, T. Ueno, and Y. Mikami et al. High-resolution imaging mass spectrometry reveals detailed spatial distribution of phosphatidylinositols in human breast cancer Cancer Sci 2013 10.1111/cas.12229
151. J.C. Jurchen, S.S. Rubakhin, and J.V. Sweedler MALDI-MS imaging of features smaller than the size of the laser beam J Am Soc Mass Spectrom 16 2005 1654 1659 (Pubitemid 41345157)
152. A. Zavalin, J. Yang, and R. Caprioli Laser beam filtration for high spatial resolution MALDI imaging mass spectrometry J Am Soc Mass Spectrom 24 2013 1 4
153. A.B. Kanu, P. Dwivedi, M. Tam, L. Matz, and H.H. Hill Ion mobility-mass spectrometry J Mass Spectrom 43 2008 1 22 (Pubitemid 351251969)
154. M. Kliman, J.C. May, and J.A. McLean Lipid analysis and lipidomics by structurally selective ion mobility-mass spectrometry Biochim Biophys Acta 1811 2011 935 945
155. S.N. Jackson, M. Ugarov, J.D. Post, T. Egan, D. Langlais, and J.A. Schultz et al. A study of phospholipids by ion mobility TOFMS J Am Soc Mass Spectrom 19 2008 1655 1662
156. C.B. Lietz, E. Gemperline, and L. Li Qualitative and quantitative mass spectrometry imaging of drugs and metabolites Adv Drug Deliv Rev 65 2013 1074 1085
157. K. Hattori, M. Kajimura, T. Hishiki, T. Nakanishi, A. Kubo, and Y. Nagahata et al. Paradoxical ATP elevation in ischemic penumbra revealed by quantitative imaging mass spectrometry Antioxid Redox Signal 13 2010 1157 1167
158. N. Takai, Y. Tanaka, K. Inazawa, and H. Saji Quantitative analysis of pharmaceutical drug distribution in multiple organs by imaging mass spectrometry Rapid Commun Mass Spectrom 26 2012 1549 1556
159. B. Prideaux, and M. Stoeckli Mass spectrometry imaging for drug distribution studies J Proteomics 75 2012 4999 5013
160. P. Nemes, and A. Vertes Ambient mass spectrometry for in vivo local analysis and in situ molecular tissue imaging TrAC Trends Anal Chem 34 2012 22 34
161. L.J. Sweetlove, and A.R. Fernie The spatial organization of metabolism within plant cell Annu Rev Plant Biol 64 2013 723 746
162. P.J. Horn, and K.D. Chapman Lipidomics in tissues, cells, and subcellular compartments Plant J 70 2012 69 80
163. P.J. Horn, N.R. Ledbetter, C.N. James, W.D. Hoffman, C.R. Case, and G.F. Verbeck et al. Visualization of lipid droplet composition by direct organelle mass spectrometry J Biol Chem 286 2011 3298 3306
164. H.-J. van Manen, Y.M. Kraan, D. Roos, and C. Otto Single-cell Raman and fluorescence microscopy reveal the association of lipid bodies with phagosomes in leukocytes Proc Natl Acad Sci U S A 102 2005 10159 10164 (Pubitemid 41023342)
165. Y. Ozeki, W. Umemura, Y. Otsuka, S. Satoh, H. Hashimoto, and K. Sumimura et al. High-speed molecular spectral imaging of tissue with stimulated Raman scattering Nat Photonics 6 2012 845 851
166. B. Wang, A. Karpiouk, D. Yeager, J. Amirian, S. Litovsky, and R. Smalling et al. In vivo intravascular ultrasound-guided photoacoustic imaging of lipid in plaques using an animal model of atherosclerosis Ultraso Med Biol 38 2012 2098 2103
167. Banerjee B, McKeown KR, Skovan B, Ogram E, Ingram P, Ignatenko N, et al. Ultrasound imaging of the mouse pancreatic duct using lipid microbubbles. SPIE Proceedings 2012. p. 832018.
168. M.R. Emmert-Buck, R.F. Bonner, P.D. Smith, R.F. Chuaqui, Z. Zhuang, and S.R. Goldstein et al. Laser capture microdissection Science 274 1996 998 1001 (Pubitemid 26398425)
169. R. Masyuko, E.J. Lanni, J.V. Sweedler, and P.W. Bohn Correlated imaging - a grand challenge in chemical analysis Analyst 7 2013 1925 1939
170. Z. Li, L.-Q. Chu, J.V. Sweedler, and P.W. Bohn Spatial correlation of confocal Raman scattering and secondary ion mass spectrometric molecular images of lignocellulosic materials Anal Chem 82 2010 2608 2611
171. A.L. Dill, L.S. Eberlin, D.R. Ifa, and R.G. Cooks Perspectives in imaging using mass spectrometry Chem Commun 47 2011 2741 2746
172. B. Thomas, and A.V. Akoulitchev Mass spectrometry of RNA Trends Biochem Sci 31 2006 173 181 (Pubitemid 43357997)
173. P. Chaurand Imaging mass spectrometry of thin tissue sections: a decade of collective efforts J Proteomics 75 2012 4883 4892
174. J. de Almeida Engler, R. De Groodt, M. Van Montagu, and G. Engler In situ hybridization to mRNA of Arabidopsis tissue sections Methods 23 2001 325 334 (Pubitemid 32846451)
175. P.B. Brewer, M.G. Heisler, J. Hejátko, J. Friml, and E. Benková In situ hybridization for mRNA detection in Arabidopsis tissue sections Nat Protoc 1 2006 1462 1467
176. E. Nordhoff, R. Cramer, M. Karas, F. Hillenkamp, F. Kirpekar, and K. Kristiansen et al. Ion stability of nucleic acids in infrared matrix-assisted laser desorption/ionization mass spectrometry Nucleic acids Res 21 1993 3347 3357 (Pubitemid 23241464)
177. Douthwaite S, Kirpekar F. Identifying modifications in RNA by MALDI mass spectrometry. In: Jonatha MG, editor. Methods in enzymology. Academic Press; 2007. p. 1-20.
178. E.H. Seeley, and R.M. Caprioli Molecular imaging of proteins in tissues by mass spectrometry Proc Nat Acad Sci U S A 105 2008 18126 18131