Exploring the plant lipidome: techniques, challenges, and prospects

Abstract

Plant lipids are a diverse group of biomolecules that play essential roles in plant architecture, physiology, and signaling. To advance our understanding of plant biology and facilitate innovations in plant-based product development, we must have precise methods for the comprehensive analysis of plant lipids. Here, we present a comprehensive overview of current research investigating plant lipids, including their structures, metabolism, and functions. We explore major lipid classes, i.e. fatty acids, glyceroglycolipids, glycerophospholipids, sphingolipids, and phytosterols, and discuss their subcellular distributions. Furthermore, we emphasize the significance of lipidomics research techniques, particularly chromatography-mass spectrometry, for accurate lipid analysis. Special attention is given to lipids as crucial signal receptors and signaling molecules that influence plant growth and responses to environmental challenges. We address research challenges in lipidomics, such as in identifying and quantifying lipids, separating isomers, and avoiding batch effects and ion suppression. Finally, we delve into the practical applications of lipidomics, including its integration with other omics methodologies, lipid visualization, and innovative analytical approaches. This review thus provides valuable insights into the field of plant lipidomics and its potential contributions to plant biology.

Keywords

Lipidomics / Plant lipids / Biomolecules / Mass spectrometry / Environmental stress

References

[1] Aflaki E, Doddapattar P, Radovic B, Povoden S, Kolb D, Vujic N, Wegscheider M, Koefeler H, Hornemann T, et al. . C16 ceramide is crucial for triacylglycerol-induced apoptosis in macrophages. Cell Death Dis. 2012, 3: e280

[2] Alseekh S, Aharoni A, Brotman Y, Contrepois K, D’Auria J, Ewald J, Ewald CJ, Fraser PD, Giavalisco P, et al. . Mass spectrometry-based metabolomics: a guide for annotation, quantification and best reporting practices. Nature Methods. 2021, 18: 747-756

[3] Annesley TM. Ion suppression in mass spectrometry. Clin Chem. 2003, 49: 1041-1044

[4] Bartels D, Dörmann P. Plant Lipids: Methods and Protocols. 2021, Springer, Humama Press

[5] Beale DJ, Pinu FR, Kouremenos KA, Poojary MM, Narayana VK, Boughton BA, Kanojia K, Dayalan S, Jones O, et al. . Review of recent developments in GC-MS approaches to metabolomics-based research. Metabolomics. 2018, 14: 152

[6] Bi FC, Liu Z, Wu JX, Liang H, Xi XL, Fang C, Sun TJ, Yin J, Dai GY, et al. . Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H₂O₂ bursts. Plant Cell. 2014, 26: 3449-3467

[7] Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959, 37(8): 911-917

[8] Cahoon RE, Solis AG, Markham JE, Cahoon EB. Mass spectrometry-based profiling of plant sphingolipids from typical and aberrant metabolism. Methods Mol Biol. 2021, 2295: 157-177

[9] Cai G, Fan C, Liu S, Yang Q, Liu D, Wu J, Li J, Zhou Y, Guo L, et al. . Nonspecific phospholipase C6 increases seed oil production in oilseed Brassicaceae plants. New Phytol. 2020, 226: 1055-1073

[10] Cajka T, Fiehn O. Comprehensive analysis of lipids in biological systems by liquid chromatography -mass spectrometry. TrAC, Trends Anal Chem. 2014, 61: 192-206

[11] Cajka T, Fiehn O. Increasing lipidomic coverage by selecting optimal mobile-phase modifiers in LC - MS of blood plasma. Metabolomics. 2016, 12: 1-11

[12] Capolupo L, Khven I, Lederer AR, Mazzeo L, Glousker G, Ho S, Russo F, Montoya JP, Bhandari DR, et al. . Sphingolipids control dermal fibroblast heterogeneity. Science.. 2022, 376: eabh1623

[13] Chen P, Wu M, He Y, Jiang B, He ML. Metabolic alterations upon SARS-CoV-2 infection and potential therapeutic targets against coronavirus infection. Signal Transduct Target Ther. 2023, 8(1): 237

[14] Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 2018, 46(W1): W486-W494

[15] Christie WW, Dobson G, Adlof RO. A practical guide to the isolation, analysis and identification of conjugated linoleic acid. Lipids. 2007, 42: 1073-1084

[16] Colantonio V, Ferrao L, Tieman DM, Bliznyuk N, Sims C, Klee HJ, Munoz P, Resende MJ. Metabolomic selection for enhanced fruit flavor. Proc Natl Acad Sci. 2022, 119: e2115865119

[17] Cook R, Lupette J, Benni C. The role of chloroplast membrane lipid metabolism in plant environmental responses. Cells. 2021, 10: 706

[18] Corbacho J, Ines C, Paredes MA, Labrador J, Cordeiro AM, Gallardo M, Gomez-Jimenez MC. Modulation of sphingolipid long-chain base composition and gene expression during early olive-fruit development, and putative role of brassinosteroid. J Plant Physiol. 2018, 231: 383-392

[19] Delude C, Moussu S, Joubes J, Ingram G, Domergue F. Plant surface lipids and epidermis development. Subcell Biochem. 2016, 86: 287-313

[20] Devaiah SP, Roth MR, Baughman E, Li M, Tamura P, Jeannotte R, Welti R, Wang X. Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochemistry. 2006, 67: 1907-1924

[21] Domingo-Almenara X, Montenegro-Burke JR, Ivanisevic J, Thomas A, Sidibe J, Teav T, Guijas C, Aisporna AE, Rinehart D, et al. . XCMS-MRM and METLIN-MRM: a cloud library and public resource for targeted analysis of small molecules. Nat Methods. 2018, 15: 681-684

[22] Duan L, Ma A, Meng X, Shen GA, Qi X. QPMASS: A parallel peak alignment and quantification software for the analysis of large-scale gas chromatography-mass spectrometry (GC-MS)-based metabolomics datasets. J Chromatogr A. 2020, 1620: 460999

[23] Dupree P, Sherrier DJ. The plant Golgi apparatus. Biochim Biophys Acta. 1998, 1404: 259-270

[24] Eastmond PJ, Quettier AL, Kroon JT, Craddock C, Adams N, Slabas AR. Phosphatidic acid phosphohydrolase 1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell. 2010, 22: 2796-2811

[25] Evtyugin DD, Evtuguin DV, Casal S, Domingues MR. Advances and challenges in plant sterol research: fundamentals, analysis, applications and production. Molecules. 2023, 28: 6526

[26] Fan J, Yu L, Xu C. Dual role for autophagy in lipid metabolism in Arabidopsis. Plant Cell. 2019, 31: 1598-1613

[27] Fouillen L, Maneta-Peyret L, Moreau P. ER Membrane lipid composition and metabolism: lipidomic analysis. Methods Mol Biol. 2018, 1691: 125-137

[28] Fujii S, Kobayashi K, Nakamura Y, Wada H. Inducible knockdown of MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE1 reveals roles of galactolipids in organelle differentiation in Arabidopsis cotyledons. Plant Physiol. 2014, 166: 1436-1449

[29] Gachumi G, El-Aneed A. Mass spectrometric approaches for the analysis of phytosterols in biological samples. J Agric Food Chem. 2017, 65: 10141-10156

[30] Gohil VM, Hayes P, Matsuyama S, Schagger H, Schlame M, Greenberg ML. Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J Biol Chem. 2004, 279(41): 42612-42618

[31] Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V, Dormann P, Nacir H, Benitez-Alfonso Y, Claverol S, et al. . Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell. 2015, 27: 1228-1250

[32] Gu Q, Yi X, Zhang Z, Yan H, Shi J, Zhang H, Wang Y, Shao J. A facile method for simultaneous analysis of phytosterols, erythrodiol, uvaol, tocopherols and lutein in olive oils by LC-MS. Anal Methods. 2016, 8: 1373-1380

[33] Guazzotti S, Pagliano C, Dondero F, Manfredi M. Lipidomic profiling of rice bran after green solid-liquid extractions for the development of circular economy approaches. Foods. 2023, 12(2): 384

[34] Gunesekera B, Torabinejad J, Robinson J, Gillaspy GE. Inositol polyphosphate 5-phosphatases 1 and 2 are required for regulating seedling growth. Plant Physiol. 2007, 143: 1408-1417

[35] Have M, Luo J, Tellier F, Balliau T, Cueff G, Chardon F, Zivy M, Rajjou L, Cacas JL, et al. . Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition. New Phytol. 2019, 223: 1461-1477

[36] Hejazi L, Ebrahimi D, Guilhaus M, Hibbert DB. Determination of the composition of fatty acid mixtures using GC x FI-MS: a comprehensive two-dimensional separation approach. Anal Chem. 2009, 81: 1450-1458

[37] Hejazi L, Ebrahimi D, Hibbert DB, Guilhaus M. Compatibility of electron ionization and soft ionization methods in gas chromatography/orthogonal time-of-flight mass spectrometry. Rapid Commun Mass Spectrom. 2009, 23: 2181-2189

[38] Herrfurth C, Liu YT, Feussner I. Targeted analysis of the plant lipidome by UPLC-NanoESI-MS/MS. Methods Mol Biol. 2021, 2295: 135-155

[39] Horvath SE, Daum G. Lipids of mitochondria. Prog Lipid Res. 2013, 52: 590-614

[40] Huang LQ, Chen DK, Li PP, Bao HN, Liu HZ, Yin J, Zeng HY, Yang YB, Li YK, et al. . Jasmonates modulate sphingolipid metabolism and accelerate cell death in the ceramide kinase mutant acd5. Plant Physiol. 2021, 187: 1713-1727

[41] Huang LQ, Li PP, Yin J, Li YK, Chen DK, Bao HN, Fan RY, Liu HZ, Yao N. Arabidopsis alkaline ceramidase ACER functions in defense against insect herbivory. J Exp Bot. 2022, 73: 4954-4967

[42] Hutchins PD, Russell JD, Coon JJ. LipiDex: An integrated software package for high-confidence lipid identification. Cell Syst. 2018, 6: 621-625

[43] Hutchins PD, Russell JD, Coon JJ. Mapping lipid fragmentation for tailored mass spectral libraries. J Am Soc Mass Spectrom. 2019, 30: 659-668

[44] Ischebeck T, Krawczyk HE, Mullen RT, Dyer JM, Chapman KD. Lipid droplets in plants and algae: distribution, formation, turnover and function. Semin Cell Dev Biol. 2020, 108: 82-93

[45] Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, et al. . Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science. 2013, 341: 175-179

[46] Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, Xiang Y, Niu Y, et al. . Plant cell-surface GIPC sphingolipids sense salt to trigger Ca(2+) influx. Nature. 2019, 572: 341-346

[47] Kanehara K, Cho Y, Yu CY. A lipid viewpoint on the plant endoplasmic reticulum stress response. J Exp Bot. 2022, 73: 2835-2847

[48] Katajamaa M, Miettinen J, Oresic M. MZmine: toolbox for processing and visualization of mass spectrometry based molecular profile data. Bioinformatics. 2006, 22: 634-636

[49] Kehelpannala C, Rupasinghe T, Hennessy T, Bradley D, Ebert B, Roessner U. The state of the art in plant lipidomics. Mol Omics. 2021, 17: 894-910

[50] Kind T, Liu KH, Lee DY, DeFelice B, Meissen JK, Fiehn O. LipidBlast in silico tandem mass spectrometry database for lipid identification. Nat Methods. 2013, 10: 755-758

[51] Klein O, Hanke T, Nebrich G, Yan J, Schubert B, Giavalisco P, Noack F, Thiele H, Mohamed SA. Imaging mass spectrometry for characterization of atrial fibrillation subtypes. Proteomics Clin Appl. 2018, 12: e1700155

[52] Kobayashi K, Endo K, Wada H. Roles of lipids in photosynthesis. Subcell Biochem. 2016, 86: 21-49

[53] Laxalt AM, Munnik T. Phospholipid signalling in plant defence. Curr Opin Plant Biol. 2002, 5: 332-338

[54] Lebaron FN, Folch J. The effect of pH and salt concentration on aqueous extraction of brain proteins and lipoproteins. J Neurochem. 1959, 4(1): 1-8

[55] Lenarcic T, Albert I, Bohm H, Hodnik V, Pirc K, Zavec AB, Podobnik M, Pahovnik D, Zagar E, et al. . Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science. 2017, 358(6369): 1431-1434

[56] Li L, Han J, Wang Z, Liu J, Wei J, Xiong S, Zhao Z. Mass spectrometry methodology in lipid analysis. Int J Mol Sci. 2014, 15: 10492-10507

[57] Lim GH, Singhal R, Kachroo A, Kachroo P. Fatty acid- and lipid-mediated signaling in plant defense. Annu Rev Phytopathol. 2017, 55: 505-536

[58] Liu JY, Li P, Zhang YW, Zuo JF, Li G, Han X, Dunwell JM, Zhang YM. Three-dimensional genetic networks among seed oil-related traits, metabolites and genes reveal the genetic foundations of oil synthesis in soybean. Plant J. 2020, 103: 1103-1124

[59] Liu NJ, Zhang T, Liu ZH, Chen X, Guo HS, Ju BH, Zhang YY, Li GZ, Zhou QH, et al. . Phytosphinganine affects plasmodesmata permeability via facilitating PDLP5-stimulated callose accumulation in Arabidopsis. Mol Plant. 2020, 13: 128-143

[60] Liu Y, Liu HZ, Chen DK, Zeng HY, Chen YL, Yao N. PlantMetSuite: a user-friendly web-based tool for metabolomics analysis and visualisation. Plants-Basel. 2023, 12: 2880

[61] Liu YT, Senkler J, Herrfurth C, Braun HP, Feussner I. Defining the lipidome of Arabidopsis leaf mitochondria: Specific lipid complement and biosynthesis capacity. Plant Physiol. 2023, 191(4): 2185-2203

[62] Markham JE, Jaworski JG. 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. 2007, 21: 1304-1314

[63] Markham JE, Li J, Cahoon EB, Jaworski JG. Separation and identification of major plant sphingolipid classes from leaves. J Biol Chem. 2006, 281: 22684-22694

[64] Markham JE, Molino D, Gissot L, Bellec Y, Hematy K, Marion J, Belcram K, Palauqui JC, Satiat-Jeunemaitre B, et al. . Sphingolipids containing very-long-chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in Arabidopsis. Plant Cell. 2011, 23: 2362-2378

[65] Misra BB, Assmann SM, Chen S. Plant single-cell and single-cell-type metabolomics. Trends Plant Sci. 2014;19(10):637–46.

[66] Mo S, Dong L, Hurst WJ, van Breemen RB. Quantitative analysis of phytosterols in edible oils using APCI liquid chromatography-tandem mass spectrometry. Lipids. 2013, 48: 949-956

[67] Ongena M, Duby F, Rossignol F, Fauconnier ML, Dommes J, Thonart P. Stimulation of the lipoxygenase pathway is associated with systemic resistance induced in bean by a nonpathogenic Pseudomonas strain. Mol Plant Microbe Interact. 2004, 17: 1009-1018

[68] Pang Z, Chong J, Zhou G, de Lima MD, Chang L, Barrette M, Gauthier C, Jacques PE, Li S, et al. . MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021, 49: W388-W396

[69] Pata MO, Hannun YA, Ng CK. Plant sphingolipids: decoding the enigma of the Sphinx. New Phytol. 2010, 185: 611-630

[70] Pathmasiri KC, Nguyen T, Khamidova N, Cologna SM. Mass spectrometry-based lipid analysis and imaging. Curr Top Membr. 2021, 88: 315-357

[71] Pati S, Nie B, Arnold RD, Cummings BS. Extraction, chromatographic and mass spectrometric methods for lipid analysis. Biomed Chromatogr. 2016, 30: 695-709

[72] Peer M, Stegmann M, Mueller MJ, Waller F. Pseudomonas syringae infection triggers de novo synthesis of phytosphingosine from sphinganine in Arabidopsis thaliana. FEBS Lett. 2010, 584: 4053-4056

[73] Peyraud R, Dubiella U, Barbacci A, Genin S, Raffaele S, Roby D. Advances on plant-pathogen interactions from molecular toward systems biology perspectives. Plant J. 2017, 90: 720-737

[74] Pluskal T, Castillo S, Villar-Briones A, Oresic M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics. 2010, 11: 395

[75] Raffaele S, Vailleau F, Leger A, Joubes J, Miersch O, Huard C, Blee E, Mongrand S, Domergue F, et al. . A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008, 20: 752-767

[76] Riederer M, Schreiber L. Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot. 2001, 52: 2023-2032

[77] Romsdahl TB, Cocuron J, Pearson MJ, Alonso AP, Chapman KD. A lipidomics platform to analyze the fatty acid compositions of non-polar and polar lipid molecular species from plant tissues: Examples from developing seeds and seedlings of pennycress (Thlaspi arvense). Front Plant Sci. 2022, 13: 1038161

[78] Ryan MJ, Grant-St JA, Lawler NG, Fear MW, Raby E, Wood FM, Maker GL, Wist J, Holmes E. Comprehensive lipidomic workflow for multicohort population phenotyping using stable isotope dilution targeted liquid chromatography-mass spectrometry. J Proteome Res. 2023, 22(5): 1419-1433

[79] Saini RK, Prasad P, Shang X, Keum YS. Advances in lipid extraction methods-a review. Int J Mol Sci. 2021, 22: 13643

[80] Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol. 2008, 59: 683-707

[81] Sanchez-Illana A, Pineiro-Ramos JD, Sanjuan-Herraez JD, Vento M, Quintas G, Kuligowski J. Evaluation of batch effect elimination using quality control replicates in LC-MS metabolite profiling. Anal Chim Acta. 2018, 1019: 38-48

[82] Schmid R, Heuckeroth S, Korf A, Smirnov A, Myers O, Dyrlund TS, Bushuiev R, Murray KJ, Hoffmann N, et al. . Integrative analysis of multimodal mass spectrometry data in MZmine 3. Nat Biotechnol. 2023, 41: 447-449

[83] Shen S, Zhan C, Yang C, Fernie AR, Luo J. Metabolomics-centered mining of plant metabolic diversity and function: Past decade and future perspectives. Mol Plant. 2023, 16: 43-63

[84] Shen X, Wang R, Xiong X, Yin Y, Cai Y, Ma Z, Liu N, Zhu ZJ. Metabolic reaction network-based recursive metabolite annotation for untargeted metabolomics. Nat Commun. 2019, 10: 1516

[85] Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010, 11(10): 688-699

[86] Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem. 2006, 78: 779-787

[87] Sparkes IA, Frigerio L, Tolley N, Hawes C. The plant endoplasmic reticulum: a cell-wide web. Biochem J. 2009, 423: 145-155

[88] Taguchi R, Ishikawa M. Precise and global identification of phospholipid molecular species by an Orbitrap mass spectrometer and automated search engine Lipid Search. J Chromatogr A. 2010, 1217: 4229-4239

[89] Tang H, Lin S, Deng J, Keasling JD, Luo X. Engineering yeast for the de novo synthesis of jasmonates. Nat Synth. 2024;3:224–35.

[90] Tautenhahn R, Patti GJ, Rinehart D, Siuzdak G. XCMS Online: a web-based platform to process untargeted metabolomic data. Anal Chem. 2012, 84: 5035-5039

[91] Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, et al. . MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods. 2015, 12: 523-526

[92] Tsugawa H, Ikeda K, Takahashi M, Satoh A, Mori Y, Uchino H, Okahashi N, Yamada Y, Tada I, et al. . A lipidome atlas in MS-DIAL 4. Nat Biotechnol. 2020, 38(10): 1159-1163

[93] Valitova JN, Sulkarnayeva AG, Minibayeva FV. Plant sterols: diversity, biosynthesis, and physiological functions. Biochemistry-Moscow. 2016, 81(8): 819-834

[94] Vermeer JE, Munnik T. Using genetically encoded fluorescent reporters to image lipid signalling in living plants. Methods Mol Biol. 2013, 1009: 283-289

[95] Wang Z, Cao M, Lam SM, Shui G. Embracing lipidomics at single-cell resolution: Promises and pitfalls. Trac-Trend Anal Chem. 2023;160:116973.

[96] Walia A, Waadt R, Jones AM. Genetically encoded biosensors in plants: pathways to discovery. Annu Rev Plant Biol. 2018, 69: 497-524

[97] Watkins PJ. Characterization of four alkyl-branched fatty acids as methyl, ethyl, propyl, and butyl esters using gas chromatography-quadrupole time of flight mass spectrometry. Anal Sci. 2020, 36: 425-429

[98] Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X. Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem. 2002, 277: 31994-32002

[99] Wewer V, Dombrink I, Vom DK, Dormann P. Quantification of sterol lipids in plants by quadrupole time-of-flight mass spectrometry. J Lipid Res. 2011, 52: 1039-1054

[100] Wu JX, Wu JL, Yin J, Zheng P, Yao N. Ethylene modulates sphingolipid synthesis in Arabidopsis. Front Plant Sci. 2015, 6: 1122

[101] Wu Z, Bagarolo GI, Thoroe-Boveleth S, Jankowski J. "Lipidomics": Mass spectrometric and chemometric analyses of lipids. Adv Drug Deliv Rev. 2020, 159: 294-307

[102] Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. MetaboAnalyst 2.0–a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 2012, 40: W127-W133

[103] Xia J, Psychogios N, Young N, Wishart DS. MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res. 2009, 37: W652-W660

[104] Xia J, Sinelnikov IV, Han B, Wishart DS. MetaboAnalyst 3.0–making metabolomics more meaningful. Nucleic Acids Res. 2015, 43: W251-W257

[105] Xu K, Zou W, Peng B, Guo C, Zou X. Lipid droplets from plants and microalgae: characteristics, extractions, and applications. Biology-Basel. 2023, 12(4): 594

[106] Yang C, Wang LY, Li YK, Lin JT, Chen DK, Yao N. Arabidopsis feaf chloroplasts have a specific sphingolipidome. Plant. 2024, 13: 299

[107] Yang K, Han X. Lipidomics: techniques, applications, and outcomes related to biomedical sciences. Trends Biochem Sci. 2016, 41: 954-969

[108] Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB. A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol. 2012, 160: 638-652

[109] Yang YB, Yin J, Huang LQ, Li J, Chen DK, Yao N. Salt enhances disease resistance and suppresses cell death in ceramide kinase mutants. Plant Physiol. 2019, 181: 319-331

[110] Yeats TH, Huang W, Chatterjee S, Viart HM, Clausen MH, Stark RE, Rose JK. Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J. 2014, 77: 667-675

[111] Zeng HY, Yao N. Sphingolipids in plant immunity. Phytopathology. Research. 2022, 4: 20

[112] Zeng HY, Liu Y, Chen DK, Bao HN, Huang LQ, Yin J, Chen YL, Xiao S, Yao N. The immune components enhanced disease susceptibility 1 and Phytoalexin deficient 4 are required for cell death caused by overaccumulation of ceramides in Arabidopsis. Plant J. 2021, 107: 1447-1465

[113] Zeng HY, Li CY, Yao N. Fumonisin B1: A Tool for Exploring the Multiple Functions of Sphingolipids in  Plants. Front Plant Sci. 2020;11:600458.

[114] Zhang M, Fan J, Taylor DC, Ohlrogge JB. DGAT1 and PDAT1 acyltransferases have overlapping functions in Arabidopsis triacylglycerol biosynthesis and are essential for normal pollen and seed development. Plant Cell. 2009, 21: 3885-3901

[115] Zhou Y, Zhou DM, Yu WW, Shi LL, Zhang Y, Lai YX, Huang LP, Qi H, Chen QF, et al. . Phosphatidic acid modulates MPK3- and MPK6-mediated hypoxia signaling in Arabidopsis. Plant Cell. 2022, 34: 889-909

[116] Zhou Z, Luo M, Zhang H, Yin Y, Cai Y, Zhu Z. Metabolite annotation from knowns to unknowns through knowledge-guided multi-layer metabolic networking. Nat Commun. 2022, 13: 6656

[117] Zhou Z, Shen X, Chen X, Tu J, Xiong X, Zhu ZJ. LipidIMMS Analyzer: integrating multi-dimensional information to support lipid identification in ion mobility-mass spectrometry based lipidomics. Bioinformatics. 2019, 35: 698-700

[118] Zullig T, Kofeler HC. High resolution mass spectrometry in lipidomics. Mass Spectrom Rev. 2021, 40: 162-176

[119] Zullig T, Trotzmuller M, Kofeler HC. Lipidomics from sample preparation to data analysis: a primer. Anal Bioanal Chem. 2020, 412: 2191-2209

Funding

National Natural Science Foundation of China(32070196)

Natural science of foundation of Guangdong Province(2023A1515012051)