Plant Sphingolipids

Samuel Belton, UCD Earth Institute, University College Dublin, Belfield, Dublin, Republic of Ireland
Carl KY Ng, UCD Earth Institute, University College Dublin, Belfield, Dublin, Republic of Ireland

Published online: May 2020

DOI: 10.1002/9780470015902.a0028909

Abstract

Sphingolipids, a class of amino alcohol‐based lipids, are major eukaryotic lipids, and they have also been found in some prokaryotes. Since the discovery of sphingolipids by Johann Ludwig Thudichum in 1874, this class of lipids is now less enigmatic, and to date, we have a much better understanding of how they are metabolised, their structural diversity and the roles they play in regulating eukaryotic cellular processes and physiology. Our understanding of the functional roles of sphingolipids in cells has come largely from studies using mammalian cells and yeast. However, in the past 20 years, we have made great strides in our understanding of plant sphingolipid metabolism, structure and function. Readers are encouraged to refer to the relevant literature for further detailed information.

Key Concepts

  • Sphingolipids are major eukaryotic lipids, and they have been shown to be important in membrane organisation, as well as playing key roles in regulating cellular physiology.
  • The de novo biosynthesis of sphingolipids in all eukaryotes begins in the endoplasmic reticulum (ER) and is catalysed by the pyridoxal 5′‐phosphate (PLP)‐dependent serine palmitoyltransferase (SPT), resulting in the formation of long‐chain bases (LCBs).
  • The LCBs can undergo further metabolism to form more complex sphingolipids, such as ceramides, glucosylceramides and glycosyl inositolphosphoceramides (GIPCs).
  • In addition to the de novo pathway, all eukaryotes also possess the salvage pathway whereby LCBs are recovered from ceramides, and key to this salvage pathway is a class of enzymes known as ceramidases.
  • Plant sphingolipids have been shown to function in membrane organisation, abiotic and biotic stress responses, regulation of developmental processes and plant physiology.

Keywords: sphingolipids; lipid microdomains; GIPCs; ceramides; sphingolipid metabolism; structural diversity; sphingolipidome

Figure 1. Schematic representation of the sphingolipid metabolic pathway in mammals, fungi and plants. The first steps in the de novo synthesis of sphingolipids up to the formation of dihydroceramides are conserved in all eukaryotes.
Figure 2. Schematic representation of complex sphingolipids from plants. The general structure of complex sphingolipids is based on a hydrophobic dihydroceramide core and a hydrophilic head group. The dihydroceramide core comprises two moieties, a long‐chain base (LCB) and a variable chain length fatty acid linked via an amide bond. Cer, ceramide; GlcCer, glucosylceramide; IPC, inositol phosphoceramide; GIPC, glucosyl inositolphosphoceramide.
Figure 3. Structures of some C18 long‐chain bases (LCBs) in plants. The trivial names, systematic names according to IUPAC (International Union of Pure and Applied Chemistry) regulations and shorthand designations are given for each LCB.
Figure 4. (a) Model for GIPC binding to NLP (cytolysin). NLPs (cytolysins) bind to the terminal hexoses of both monocot and eudicot GIPCs. Due to the longer sugar groups (three terminal hexoses) in monocots, the bound NLP (cytolysin) is too distant from the plasma membrane compared to bound NLP (cytolysin) in eudicots, where they are able to physically interact with the plasma membrane and accumulate, leading to subsequent accumulation. (b) Proposed model for salt sensing in plants involving GIPCs. GIPCs function as monovalent ion receptors and through binding of their cognate monovalent ions physically interact with calcium channels, thereby activating calcium influx.
close

References

Aubert A, Marion J, Boulogne C, et al. (2011) Sphingolipids involvement in plant endomembrane differentiation: the BY2 case. Plant Journal 65: 958–971.

Benito B, Haro R, Amtmann A, Cuin TA and Dreyer I (2014) The twins K+ and Na+ in plants? Journal of Plant Physiology 171: 723–731.

Breslow DK, Collins SR, Bodenmiller B, et al. (2010) Orm family proteins mediate sphingolipid homeostasis. Nature 463: 1048–1053.

Cacas JL, Buré C, Furt F, et al. (2013) Biochemical survey of the polar head of glycosyl inositolphosphoceramides unravels broad diversity. Phytochemistry 96: 191–200.

Cacas JL, Buré C, Grosjean K, et al. (2016) Revisiting plant plasma membrane lipids in tobacco: a focus on sphingolipids. Plant Physiology 170: 367–384.

Cassim AM, Gouguet P, Gronnier J, et al. (2019) Plant lipids: key players of plasma membrane organization and function. Progress in Lipid Research 73: 1–27.

Chao D‐Y, Gable K, Chen M, et al. (2011) Sphingolipids in the roots play an important role in regulating the leaf ionome in Arabidopsis thaliana. Plant Cell 23: 1061–1081.

Chen M, Markham JE, Dietrich CR, Jaworski JG and Cahoon EB (2008) Sphingolipid long chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 20: 1862–1878.

Chueasiri C, Chunthong K, Pitnjam K, et al. (2014) Rice ORMDL controls sphingolipid homeostasis affecting fertility resulting from abnormal pollen development. PLoS One 9: e106386.

Ebert B, Rautengarten C, McFarlane HE, et al. (2018) A Golgi UDP‐GlcNAc transporter delivers substrates for N‐linked glycans and sphingolipids. Nature Plants 4: 792–801.

Grison M, Brocard L, Fouillen L, et al. (2015) Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27: 1228–1250.

Hannun YA and Obeid LM (2018) Sphingolipids and their metabolism in physiology and disease. Nature Reviews Molecular Cell Biology 19: 175–191.

Harrison PJ, Dunn TM and Campopiano DJ (2018) Sphingolipid biosynthesis in man and microbes. Natural Product Reports 35: 921–954.

Havé M, Luo J, Tellier F, et al. (2019) Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition. New Phytologist 223: 1461–1477.

Heaver SL, Johnson EL and Ley RE (2018) Sphingolipids in host‐microbial interactions. Current Opinion in Microbiology 43: 92–99.

Huang D, Sun Y, Ma Z, et al. (2019) Salicylic acid‐mediated plasmodesmal closure via Remorin‐dependent lipid organization. Proceedings of the National Academy of Sciences United States of America 116: 21274–21284.

Huby E, Napier JA, Baillieul F, Michaelson LV and Dhondt‐Cordelier S (2020) Sphingolipids: towards an integrated view of metabolism during the plant stress response. New Phytologist 225: 659–670. DOI: 10.1111/nph.15997.

Ishikawa T, Ito Y and Kawai‐Yamada M (2016) Molecular characterization and targeted quantitative profiling of the sphingolipidome in rice. Plant Journal 88: 681–693.

Ishikawa T, Fang L, Rennie EA, et al. (2018) GLUCOSAMINE INOSITOLPHOSPHORYLCERAMIDE TRANSFERASE1 (GINT1) is a Glc‐NAc‐containing glycosylinositol phosphorylceramide glycosyltransferase. Plant Physiology 177: 938–952.

Islam MN, Chambers JP and Ng CKY (2012a) Lipid profiling of the model temperate grass, Brachypodium distachyon. Metabolomics 8: 598–613.

Islam MN, Jacquemot MP, Coursol S and Ng CKY (2012b) Sphingosine in plants – more riddles from the Sphinx? New Phytologist 193: 51–57.

Jiang Z, Zhou X, Tao M, et al. (2019) Plant cell‐surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572: 341–346.

Jing B, Ishikawa T, Soltis N, et al. (2018) CONST2 transports GDP‐Mannose for sphingolipid glycosylation in the Golgi apparatus of Arabidopsis. bioRxiv. DOI: 10.1101/346775.

Kimberlin AN, Majumder S, Han G, et al. (2013) Arabidopsis 56‐amino acid serine palmitoyltransferase‐interacting proteins stimulate sphingolipid synthesis, are essential, and affect mycotoxin sensitivity. Plant Cell 25: 4627–4639.

Lenarčič T, Albert I, Böhm H, et al. (2017) Eudicot plant‐specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science 358: 1431–1434.

Li J, Yin J, Rong C, et al. (2016) Orosomucoid proteins interact with the small subunit of serine palmitoyltransferase and contribute to sphingolipid homeostasis and stress responses in Arabidposis. Plant Cell 28: 3038–3051.

Liang H, Yao N, Song J, Lu H and Greenberg JT (2003) Ceramides modulate programmed cell death in plants. Genes and Development 17: 2636–2641.

Luttegeharm KD, Chen M, Mehra A, et al. (2015) Overexpression of Arabidopsis ceramide synthases differentially affects growth, sphingolipid metabolism, programmed cell death, and mycotoxin resistance. Plant Physiology 169: 1108–1117.

Markham JE and Jaworski JG (2007) Rapid measurement of sphingolipids from Arabidopsis thaliana by reverse‐phase high‐performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Communications in Mass Spectrometry 21: 1304–1314.

Markham JE, Li J, Cahoon EB and Jaworski JG (2006) Separation and identification of major plant sphingolipid classes from leaves. Journal of Biological Chemistry 281: 22684–22694.

Markham JE, Molino D, Gissot L, et al. (2011) Sphingolipids containing very‐long‐chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in Arabidopsis. Plant Cell 23: 2362–2378.

Mashima R, Okuyama T and Ohira M (2019) Biosynthesis of long chain base sphingolipids in animals, plants and fungi. Future Science 6: FSO434.

Michaelson LV, Napier JA, Molino D and Faure JD (2016) Plant sphingolipids: their importance in cellular organization and adaption. Biochimica et Biophysica Acta 1861: 1329–1335.

Mina JG, Okada Y, Wansadhipathi‐Kannanagara NK, et al. (2010) Functional analyses of differentially expressed isoforms of the Arabidopsis inositol phosphorylceramide synthase. Plant Molecular Biology 73: 399–407.

Mortimer JC, Yu X, Albrecht S, et al. (2013) Abnormal glycosphingolipid mannosylation triggers salicylic acid‐mediated responses in Arabidopsis. Plant Cell 25: 1881–1894.

Msanne J, Chen M, Luttgeharm KD, et al. (2015) Glucosylceramide is critical for cell‐type differentiation and organogenesis, but not for cell viability in Arabidopsis. Plant Journal 84: 188–201.

Nicolas WJ, Grison MS, Trépout S, et al. (2017) Architecture and permeability of postcytokinesis plasmodesmata lacking cytoplasmic sleeves. Nature Plants 3: 17082.

Olsen ASB and Færgeman NJ (2017) Sphingolipids: membrane microdomains in brain development, function and neurological diseases. Open Biology 7: 170069.

Ormancey M, Thuleau P, van der Hoorn R, et al. (2019) Sphingolipid‐induced cell death in Arabidopsis is negatively regulated by the papain‐like cysteine protease RD21. Plant Science 280: 12–17.

Ott T (2017) Membrane nanodomains and microdomains in plant‐microbe interactions. Current Opinion in Plant Biology 40: 82–88.

Pata MO, Wu BX, Bielawski J, et al. (2008) Molecular cloning and characterization of OsCDase, a ceramidase enzyme from rice. Plant Journal 55: 1000–1009.

Pata MO, Hannun YA and Ng CKY (2010) Plant sphingolipids: decoding the enigma of the Sphinx. New Phytologist 185: 611–630.

Piantanida L, Bolt HL, Rozatian N, Cobb SL and Voïtchovsky K (2017) Ions modulate stress‐induced nanotexture in supported fluid lipid bilayers. Biophysical Journal 113: 426–439.

Rojko N, Serra MD, Maček P and Anderluh G (2016) Pore formation by actinoporins, cytolysins from sea anemones. Biochimica et Biophysica Acta 1858: 446–456.

Sager RE and Lee JY (2018) Plasmodesmata at a glance. Journal of Cell Science 131: jcs209346.

Sonnino S, Grassi S, Prioni S, et al. (2016) Lipid rafts and neurological diseases. In: eLS. Wiley: Chichester.

Tellier F, Maia‐Grondard A, Schmitz‐Afonso I and Faure JD (2014) Comparative plant sphingolipidomic reveals specific lipids in seeds and oils. Phytochemistry 103: 50–58.

Wang W, Yang X, Tanchaiburana S, et al. (2008) An inositol phophorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20: 3163–3179.

Wu J‐X, Li J, Liu Z, et al. (2015) The Arabidopsis ceramidase AtACER functions in disease resistance and salt tolerance. Plant Journal 81: 767–780.

Yan D, Yadav SR, Paterlini A, et al. (2019) Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading. Nature Plants 5: 601615.

Zheng P, Wu JX, Sahu SK, et al. (2018) Loss of alkaline ceramidase inhibits autophagy in Arabidopsis and plays an important role during environmental stress response. Plant, Cell & Environment 41: 837–849.

Zienkiewicz A, Gömann J, König S, et al. (2020) Disruption of Arabidopsis neutral ceramidases 1 and 2 results in specific sphingolipid imbalances triggering different phytohormone‐dependent plant cell programs. New Phytologist 226: 170.

Further Reading

Corbacho J, Inês C, Oaredes MA, et al. (2018) Modulation of sphingolipid long‐chain base composition and gene expression during early olive‐fruit development, and putative role of brassinosteroid. Journal of Plant Physiology 231: 383–392.

Geiger O, Padilla‐Gómez J and López‐Laran IM (2019) Bacterial sphingolipids and sulfonolipids. In: Geiger O (ed.) Biogenesis of Fatty Acids, Lipids and Membranes, Handbook of Hydrocarbon and Lipid Microbiology. Springer: Cham.

Germain V, Perraki A and Mongrand S (2012) Lipid rafts. In: eLS. Wiley: Chichester.

Gronnier J, Legrand A, Loquet A, et al. (2019) Mechanisms governing subcompartmentalization of biological membranes. Current Opinions in Plant Biology 52: 114–123.

Liu NJ, Zhang T, Liu ZH, et al. (2020) Phytosphinganine affects plasmodesmata permeability via facilitating PDLP5‐stimulated callose accumulation in Arabidopsis. Molecular Plant 13: 128–143. DOI: 10.1016/j.molp.2019.10.013.

Ren J and Hannun YA (2019) Metabolism and roles of sphingolipids in yeast Saccharomyces cerevisiae. In: Geiger O (ed.) Biogenesis of Fatty Acids, Lipids and Membranes, Handbook of Hydrocarbon and Lipid Microbiology. Springer: Cham.

Rolando M and Buchrieser C (2019) A comprehensive review on the manipulation of the sphingolipid pathway by pathogenic bacteria. Frontiers in Cell and Developmental Biology 7: 168.

Rugen MD, Vernet MMJL, Hantouti L, et al. (2018) A chemical genetic screen reveals that iminosugar inhibitors of plant glucosylceramide synthase inhibit root growth in Arabidopsis and cereals. Scientific Report 8: 16421.

Related Sub-Topics:

Plant Secondary Metabolism | Plant Stress Physiology | Lipids: Structure, Function, Metabolism | Lipids and Membrane Structure
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Plant Sphingolipids
 
How to Cite close
Belton, Samuel, and Ng, Carl KY(May 2020) Plant Sphingolipids. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028909]