Discovery of novel neutral glycosphingolipids in cereal crops: rapid profiling using reversed-phased HPLC-ESI-QqTOF with parallel reaction monitoring.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
19 Dec 2023
19 Dec 2023
Historique:
received:
26
09
2023
accepted:
14
12
2023
medline:
19
12
2023
pubmed:
19
12
2023
entrez:
19
12
2023
Statut:
epublish
Résumé
This study explores the sphingolipid class of oligohexosylceramides (OHCs), a rarely studied group, in barley (Hordeum vulgare L.) through a new lipidomics approach. Profiling identified 45 OHCs in barley (Hordeum vulgare L.), elucidating their fatty acid (FA), long-chain base (LCB) and sugar residue compositions; and was accomplished by monophasic extraction followed by reverse-phased high performance liquid chromatography electrospray ionisation quadrupole-time-of-flight tandem mass spectrometry (HPLC-ESI-QqTOF-MS/MS) employing parallel reaction monitoring (PRM). Results revealed unknown ceramide species and highlighted distinctive FA and LCB compositions when compared to other sphingolipid classes. Structurally, the OHCs featured predominantly trihydroxy LCBs associated with hydroxylated FAs and oligohexosyl residues consisting of two-five glucose units in a linear 1 → 4 linkage. A survey found OHCs in tissues of major cereal crops while noting their absence in conventional dicot model plants. This study found salinity stress had only minor effects on the OHC profile in barley roots, leaving questions about their precise functions in plant biology unanswered.
Identifiants
pubmed: 38110595
doi: 10.1038/s41598-023-49981-7
pii: 10.1038/s41598-023-49981-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
22560Subventions
Organisme : University of Melbourne
ID : Dyson Fellowship
Organisme : Australian Research Council
ID : FT130100326
Informations de copyright
© 2023. The Author(s).
Références
Michaelson, L. V., Napier, J. A., Molino, D. & Faure, J.-D. Plant sphingolipids: Their importance in cellular organization and adaption. Biochim. Biophys. Acta (BBA) Mol. Cell Biol. Lipids. https://doi.org/10.1016/j.bbalip.2016.04.003 (2016).
Haslam, T. M. & Feussner, I. Diversity in sphingolipid metabolism across land plants. J. Exp. Bot. 73, 2785–2798. https://doi.org/10.1093/jxb/erab558 (2022).
doi: 10.1093/jxb/erab558
pubmed: 35560193
pmcid: 9113257
Liu, N. J., Hou, L. P., Bao, J. J., Wang, L. J. & Chen, X. Y. Sphingolipid metabolism, transport, and functions in plants: Recent progress and future perspectives. Plant Commun. 2, 100214. https://doi.org/10.1016/j.xplc.2021.100214 (2021).
doi: 10.1016/j.xplc.2021.100214
pubmed: 34746760
pmcid: 8553973
Svennerholm, L. The quantitative estimation of cerebrosides in nervous tissue. J. Neurochem. 1, 42–53 (1956).
doi: 10.1111/j.1471-4159.1956.tb12053.x
pubmed: 13346373
Sperling, P. & Heinz, E. Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim. Biophys. Acta (BBA) Mol. Cell Biol. Lipids 1632, 1–15 (2003).
Adem, A. A. et al. Structural characterization of plant glucosylceramides and the corresponding ceramides by UHPLC-LTQ-Orbitrap mass spectrometry. J. Pharm. Biomed. Anal. 192, 113677. https://doi.org/10.1016/j.jpba.2020.113677 (2021).
doi: 10.1016/j.jpba.2020.113677
pubmed: 33099117
Lynch, D. V. & Phinney, A. J. in Plant Lipid Metabolism 239–241 (Springer, 1995).
Lynch, D. V. & Dunn, T. M. An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytol. 161, 677–702 (2004).
doi: 10.1111/j.1469-8137.2004.00992.x
pubmed: 33873728
Fujino, Y. & Ohnishi, M. Sphingolipids in wheat grain. J. Cereal Sci. 1, 159–168 (1983).
doi: 10.1016/S0733-5210(83)80033-2
Fujino, Y., Ohnishi, M. & Seisuke, I. Molecular species of ceramide and mono-, di-, tri-, and tetraglycosy leer amide in bran and endosperm of rice grains. Agric. Biol. Chem. 49, 2753–2762 (1985).
Masao, O., Seisuke, I. & Yasuhiko, F. Characterization of sphingolipids in spinach leaves. Biochim. Biophys. Acta (BBA) Lipids Lipid Metab. 752, 416–422 (1983).
Yu, D. et al. A high-resolution HPLC-QqTOF platform using parallel reaction monitoring for in-depth lipid discovery and rapid profiling. Anal. Chim. Acta (2018).
Ohnishi, M., Ito, S. & Fujino, Y. Structural characterization of sphingolipids in leafy stems of rice. Agric. Biol. Chem. 49, 3327–3329 (1985).
Hakomori, S.-I. Structure and function of glycosphingolipids and sphingolipids: recollections and future trends. Biochim. Biophys. Acta (BBA)-General Subjects 1780, 325–346 (2008).
Natera, S. H., Hill, C. B., Rupasinghe, T. W. & Roessner, U. Salt-stress induced alterations in the root lipidome of two barley genotypes with contrasting responses to salinity. Funct. Plant Biol. (2016).
Welti, R. et al. Plant lipidomics: discerning biological function by profiling plant complex lipids using mass spectrometry. Front Biosci. 12, 2494–2506 (2007).
doi: 10.2741/2250
pubmed: 17127258
Tenenboim, H., Burgos, A., Willmitzer, L. & Brotman, Y. Using lipidomics for expanding the knowledge on lipid metabolism in plants. Biochimie 130, 91–96 (2016).
doi: 10.1016/j.biochi.2016.06.004
pubmed: 27292697
Ishikawa, T., Ito, Y. & Kawai‐Yamada, M. Molecular characterization and targeted quantitative profiling of the sphingolipidome in rice. Plant J. (2016).
Lemoine, J. et al. Collision-induced dissociation of alkali metal cationized and permethylated oligosaccharides: Influence of the collision energy and of the collision gas for the assignment of linkage position. J. Am. Soc. Mass Spectrom. 4, 197–203. https://doi.org/10.1016/1044-0305(93)85081-8 (1993).
doi: 10.1016/1044-0305(93)85081-8
pubmed: 24234847
Berg, J. M., Tymoczko, J. L., Stryer, L. & Stryer, L. (WH Freeman and Company New York, 2002).
Guzha, A. et al. Cell wall-localized BETA-XYLOSIDASE4 contributes to immunity of Arabidopsis against Botrytis cinerea. Plant Physiol. 189, 1794–1813. https://doi.org/10.1093/plphys/kiac165 (2022).
doi: 10.1093/plphys/kiac165
pubmed: 35485198
pmcid: 9237713
Blaas, N. & Humpf, H.-U. Structural profiling and quantitation of glycosyl inositol phosphoceramides in plants with Fourier transform mass spectrometry. J. Agric. Food Chem. 61, 4257–4269 (2013).
doi: 10.1021/jf4001499
pubmed: 23573790
Markham, J. E. & Jaworski, J. G. 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 (2007).
doi: 10.1002/rcm.2962
pubmed: 17340572
Markham, J. E., Li, J., Cahoon, E. B. & Jaworski, J. G. Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 281, 22684–22694 (2006).
doi: 10.1074/jbc.M604050200
pubmed: 16772288
Cacas, J.-L. et al. Re-visiting plant plasma membrane lipids in tobacco: a focus on sphingolipids. Plant Physiol. 00564.02015 (2015).
Gomann, J. et al. Sphingolipid long-chain base hydroxylation influences plant growth and callose deposition in Physcomitrium patens. New Phytol. 231, 297–314. https://doi.org/10.1111/nph.17345 (2021).
doi: 10.1111/nph.17345
pubmed: 33720428
Gomann, J., Herrfurth, C., Zienkiewicz, K., Haslam, T. M. & Feussner, I. Sphingolipid Delta4-desaturation is an important metabolic step for glycosylceramide formation in Physcomitrium patens. J. Exp. Bot. 72, 5569–5583. https://doi.org/10.1093/jxb/erab238 (2021).
doi: 10.1093/jxb/erab238
pubmed: 34111292
pmcid: 8318264
Zenoff, A. M., Hilal, M., Galo, M. & Moreno, H. Changes in roots lipid composition and inhibition of the extrusion of protons during salt stress in two genotypes of soybean resistant or susceptible to stress Varietal differences. Plant Cell Physiol. 35, 729–735 (1994).
doi: 10.1093/oxfordjournals.pcp.a078650
Zhang, J. et al. Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PloS one 7, e30355 (2012).
doi: 10.1371/journal.pone.0030355
pubmed: 22279586
pmcid: 3261201
Natera, S. H., Hill, C. B., Rupasinghe, T. W. & Roessner, U. Salt-stress induced alterations in the root lipidome of two barley genotypes with contrasting responses to salinity. Funct. Plant Biol. 43, 207–219 (2016).
doi: 10.1071/FP15253
pubmed: 32480454
Yang, F. & Chen, G. The nutritional functions of dietary sphingomyelin and its applications in food. Front Nutr. 9, 1002574. https://doi.org/10.3389/fnut.2022.1002574 (2022).
doi: 10.3389/fnut.2022.1002574
pubmed: 36337644
pmcid: 9626766
Behr, M., Neutelings, G., El Jaziri, M. & Baucher, M. You want it sweeter: How glycosylation affects plant response to oxidative stress. Front. Plant Sci. 11, 571399 (2020).
doi: 10.3389/fpls.2020.571399
pubmed: 33042189
pmcid: 7525049
Keymer, A. et al. Lipid transfer from plants to arbuscular mycorrhiza fungi. elife 6, e29107 (2017).
Liang, Y., Huang, Y., Liu, C., Chen, K. & Li, M. Functions and interaction of plant lipid signalling under abiotic stresses. Plant Biol. 25, 361–378 (2023).
doi: 10.1111/plb.13507
pubmed: 36719102
Moore, W. M. et al. Reprogramming sphingolipid glycosylation is required for endosymbiont persistence in Medicago truncatula. Curr. Biol. 31, 2374–2385 (2021).
Fahy, E. et al. A comprehensive classification system for lipids. J. Lipid Res. 46, 839–862. https://doi.org/10.1194/jlr.E400004-JLR200 (2005).
doi: 10.1194/jlr.E400004-JLR200
pubmed: 15722563
Liebisch, G. et al. Shorthand notation for lipid structures derived from mass spectrometry. J. Lipid Res. M033506 (2013).
Adams, J. & Ann, Q. Structure determination of sphingolipids by mass spectrometry. Mass Spectrom. Rev. 12, 51–85 (1993).
doi: 10.1002/mas.1280120103
Levery, S. Glycosphingolipid structural analysis and glycosphingolipidomics mass spectrometry: Modified proteins and glycoconjugates. Methods Enzymol. 405, 300–369 (2005).
doi: 10.1016/S0076-6879(05)05012-3
pubmed: 16413319
Cao, D., Lutz, A., Hill, C. B., Callahan, D. L. & Roessner, U. A quantitative profiling method of phytohormones and other metabolites applied to barley roots subjected to salinity stress. Front. Plant Sci. 7, 2070 (2017).
doi: 10.3389/fpls.2016.02070
pubmed: 28119732
pmcid: 5222860
Grillitsch, K. et al. Isolation and characterization of the plasma membrane from the yeast Pichia pastoris. Biochim. Biophys. Acta (BBA)-Biomembranes 1838, 1889–1897 (2014).
Schilling, B. et al. Multiplexed, scheduled, high-resolution parallel reaction monitoring on a full scan QqTOF instrument with integrated data-dependent and targeted mass spectrometric workflows. Anal. Chem. 87, 10222–10229 (2015).
doi: 10.1021/acs.analchem.5b02983
pubmed: 26398777
pmcid: 5677521
Herrfurth, C., Liu, Y. T. & Feussner, I. Targeted analysis of the plant lipidome by UPLC-NanoESI-MS/MS. Methods Mol. Biol. 2295, 135–155. https://doi.org/10.1007/978-1-0716-1362-7_9 (2021).
doi: 10.1007/978-1-0716-1362-7_9
pubmed: 34047976
Markham, J. E. Detection and quantification of plant sphingolipids by LC-MS. Methods Mol. Biol. 1009, 93–101. https://doi.org/10.1007/978-1-62703-401-2_10 (2013).
doi: 10.1007/978-1-62703-401-2_10
pubmed: 23681527
Sud, M. et al. Lmsd: Lipid maps structure database. Nucleic Acids Res. 35, D527–D532 (2006).
doi: 10.1093/nar/gkl838
pubmed: 17098933
pmcid: 1669719