Sphingolipid long-chain base hydroxylation influences plant growth and callose deposition in Physcomitrium patens.

Physcomitrium patens LCB hydroxylation callose long-chain base (LCB) C-4 hydroxylase microdomain nonvascular plants plant development sphingolipid metabolism

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
07 2021
Historique:
received: 30 10 2020
accepted: 08 03 2021
pubmed: 16 3 2021
medline: 11 6 2021
entrez: 15 3 2021
Statut: ppublish

Résumé

Sphingolipids are enriched in microdomains in the plant plasma membrane (PM). Hydroxyl groups in the characteristic long-chain base (LCB) moiety might be essential for the interaction between sphingolipids and sterols during microdomain formation. Investigating LCB hydroxylase mutants in Physcomitrium patens might therefore reveal the role of certain plant sphingolipids in the formation of PM subdomains. Physcomitrium patens mutants for the LCB C-4 hydroxylase S4H were generated by homologous recombination. Plants were characterised by analysing their sphingolipid and steryl glycoside (SG) profiles and by investigating different gametophyte stages. s4h mutants lost the hydroxyl group at the C-4 position of their LCB moiety. Loss of this hydroxyl group caused global changes in the moss sphingolipidome and in SG composition. Changes in membrane lipid composition may trigger growth defects by interfering with the localisation of membrane-associated proteins that are crucial for growth processes such as signalling receptors or callose-modifying enzymes. Loss of LCB-C4 hydroxylation substantially changes the P. patens sphingolipidome and reveals a key role for S4H during development of nonvascular plants. Physcomitrium patens is a valuable model for studying the diversification of plant sphingolipids. The simple anatomy of P. patens facilitates visualisation of physiological processes in biological membranes.

Identifiants

pubmed: 33720428
doi: 10.1111/nph.17345
doi:

Substances chimiques

Glucans 0
Sphingolipids 0
callose 9064-51-1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

297-314

Informations de copyright

© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.

Références

Abas L, Luschnig C. 2010. Maximum yields of microsomal-type membranes from small amounts of plant material without requiring ultracentrifugation. Analytical Biochemistry 401: 217-227.
Alden KP, Dhondt-Cordelier S, McDonald KL, Reape TJ, Ng CKY, McCabe PF, Leaver CJ. 2011. Sphingolipid long chain base phosphates can regulate apoptotic-like programmed cell death in plants. Biochemical and Biophysical Research Communications 410: 574-580.
de Almeida RF, Fedorov A, Prieto M. 2003. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophysical Journal 85: 2406-2416.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
Ashton NW, Cove DJ. 1977. The isolation and preliminary characterisation of auxotrophic and analogue resistant mutants of the moss, Physcomitrella patens. Molecular and General Genetics 154: 87-95.
Bach L, Gissot L, Marion J, Tellier F, Moreau P, Satiat-Jeunemaitre B, Palauqui J-C, Napier JA, Faure J-D. 2011. Very-long-chain fatty acids are required for cell plate formation during cytokinesis in Arabidopsis thaliana. Journal of Cell Science 124: 3223-3234.
Bai Y, McCoy JG, Levin EJ, Sobrado P, Rajashankar KR, Fox BG, Zhou M. 2015. X-ray structure of a mammalian stearoyl-CoA desaturase. Nature 524: 252-256.
Berdyshev EV, Gorshkova IA, Garcia JG, Natarajan V, Hubbard WC. 2005. Quantitative analysis of sphingoid base-1-phosphates as bisacetylated derivatives by liquid chromatography-tandem mass spectrometry. Analytical Biochemistry 339: 129-136.
Bi F-C, Liu Z, Wu J-X, Liang H, Xi X-L, Fang C, Sun T-J, Yin J, Dai G-Y, Rong C et al. 2014. Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts. Plant Cell 26: 3449-3467.
Buré C, Cacas JL, Wang F, Gaudin K, Domergue F, Mongrand S, Schmitter JM. 2011. Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry. Rapid Communications in Mass Spectrometry 25: 3131-3145.
Cacas J-L, Bure C, Furt F, Maalouf J-P, Badoc A, Cluzet S, Schmitter J-M, Antajan E, Mongrand S. 2013. Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity. Phytochemistry 96: 191-200.
Cacas J-L, Buré C, Grosjean K, Gerbeau-Pissot P, Lherminier J, Rombouts Y, Maes E, Bossard C, Gronnier J, Furt F et al. 2016. Revisiting plant plasma membrane lipids in tobacco: a focus on sphingolipids. Plant Physiology 170: 367-384.
Cacas J-L, Furt F, Le Guédard M, Schmitter J-M, Buré C, Gerbeau-Pissot P, Moreau P, Bessoule J-J, Simon-Plas F, Mongrand S. 2012. Lipids of plant membrane rafts. Progress in Lipid Research 51: 272-299.
Chen M, Markham JE, Dietrich CR, Jaworski JG, 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.
Dunn TM, Lynch DV, Michaelson LV, Napier JA. 2004. A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Annals of Botany 93: 483-497.
Gallagher KL, Sozzani R, Lee CM. 2014. Intercellular protein movement: deciphering the language of development. Annual Review of Cell and Developmental Biology 30: 207-233.
Gietz RD, Schiestl RH. 2007. High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature Protocols 2: 31-34.
Gonzalez Solis A, Han G, Gan L, Liu Y, Markham JE, Cahoon RE, Dunn TM, Cahoon EB. 2020. Unregulated sphingolipid biosynthesis in gene-edited Arabidopsis ORM mutants results in nonviable seeds with strongly reduced oil content. Plant Cell 32: 2474-2490.
Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V, Dörmann P, Nacir H, Benitez-Alfonso Y, Claverol S, Germain V et al. 2015. Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27: 1228-1250.
Grosjean K, Der C, Robert F, Thomas D, Mongrand S, Simon-Plas F, Gerbeau-Pissot P. 2018. Interactions between lipids and proteins are critical for plasma membrane ordered domain organization in BY-2 cells. Journal of Experimental Botany 69: 3545-3557.
Grosjean K, Mongrand S, Beney L, Simon-Plas F, Gerbeau-Pissot P. 2015. Differential effect of plant lipids on membrane organization: SPECIFICITIES OF PHYTOSPHINGOLIPIDS AND PHYTOSTEROLS. Journal of Biological Chemistry 290: 5810-5825.
Haak D, Gable K, Beeler T, Dunn T. 1997. Hydroxylation of Saccharomyces cerevisiae ceramides requires Sur2p and Scs7p. Journal of Biological Chemistry 272: 29704-29710.
Huang D, Sun Y, Ma Z, Ke M, Cui Y, Chen Z, Chen C, Ji C, Tran TM, Yang L et al. 2019. Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization. Proceedings of the National Academy of Sciences, USA 116: 21274-21284.
Huby E, Napier JA, Baillieul F, Michaelson LV, Dhondt-Cordelier S. 2020. Sphingolipids: towards an integrated view of metabolism during the plant stress response. New Phytologist 225: 659-670.
de Keijzer J, Kieft H, Ketelaar T, Goshima G, Janson ME. 2017. Shortening of microtubule overlap regions defines membrane delivery sites during plant cytokinesis. Current Biology 27: 514-520.
Klose C, Ejsing CS, García-Sáez AJ, Kaiser H-J, Sampaio JL, Surma MA, Shevchenko A, Schwille P, Simons K. 2010. Yeast lipids can phase-separate into micrometer-scale membrane domains. Journal of Biological Chemistry 285: 30224-30232.
König S, Feussner K, Schwarz M, Kaever A, Iven T, Landesfeind M, Ternes P, Karlovsky P, Lipka V, Feussner I. 2012. Arabidopsis mutants of sphingolipid fatty acid α-hydroxylases accumulate ceramides and salicylates. New Phytologist 196: 1086-1097.
Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305: 567-580.
Lenarčič T, Albert I, Böhm H, Hodnik V, Pirc K, Zavec AB, Podobnik M, Pahovnik D, Žagar E, Pruitt R et al. 2017. Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science 358: 1431-1434.
Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT. 2003. Ceramides modulate programmed cell death in plants. Genes & Development 17: 2636-2641.
Liu N-J, Zhang T, Liu Z-H, Chen X, Guo H-S, Ju B-H, Zhang Y-Y, Li G-Z, Zhou Q-H, Qin Y-M et al. 2020. Phytosphinganine affects plasmodesmata permeability via facilitating PDLP5-stimulated callose accumulation in Arabidopsis. Molecular Plant 13: 128-143.
Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS et al. 2020. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Research 48: D265-D268.
Luttgeharm KD, Kimberlin AN, Cahoon EB. 2016. Plant sphingolipid metabolism and function. In: Nakamura Y, Li-Beisson Y, eds. Lipids in plant and algae development. Cham: Springer International Publishing, 249-286.
Lynch DV, Dunn TM. 2004. An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytologist 161: 677-702.
Mamode Cassim A, Gouguet P, Gronnier J, Laurent N, Germain V, Grison M, Boutté Y, Gerbeau-Pissot P, Simon-Plas F, Mongrand S. 2019. Plant lipids: Key players of plasma membrane organization and function. Progress in Lipid Research 73: 1-27.
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI et al. 2015. CDD: NCBI's conserved domain database. Nucleic Acids Research 43: D222-226.
Markham JE, Jaworski JG. 2007. Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-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, 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, Bellec Y, Hematy K, Marion J, Belcram K, Palauqui J-C, Satiat-JeuneMaitre B, Faure J-D. 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.
Mizutani Y, Kihara A, Igarashi Y. 2004. Identification of the human sphingolipid C4-hydroxylase, hDES2, and its up-regulation during keratinocyte differentiation. FEBS Letters 563: 93-97.
Molino D, Van der Giessen E, Gissot L, Hématy K, Marion J, Barthelemy J, Bellec Y, Vernhettes S, Satiat-Jeunemaétre B, Galli T et al. 2014. Inhibition of very long acyl chain sphingolipid synthesis modifies membrane dynamics during plant cytokinesis. Biochimica et Biophysica Acta 1841: 1422-1430.
Mombelli E, Morris R, Taylor W, Fraternali F. 2003. Hydrogen-bonding propensities of sphingomyelin in solution and in a bilayer assembly: a molecular dynamics study. Biophysical Journal 84: 1507-1517.
Msanne J, Chen M, Luttgeharm KD, Bradley AM, Mays ES, Paper JM, Boyle DL, Cahoon RE, Schrick K, Cahoon EB. 2015. Glucosylceramides are critical for cell-type differentiation and organogenesis, but not for cell viability in Arabidopsis. The Plant Journal 84: 188-201.
Mueller AO, Blersch KF, Gippert AL, Ischebeck T. 2017. Tobacco pollen tubes - a fast and easy tool for studying lipid droplet association of plant proteins. The Plant Journal 89: 1055-1064.
Mueller SJ, Reski R. 2015. Mitochondrial dynamics and the ER: the plant perspective. Frontiers in Cell and Developmental Biology 3: 78.
Ortiz-Ramírez C, Hernandez-Coronado M, Thamm A, Catarino B, Wang M, Dolan L, Feijó JA, Becker JD. 2016. A transcriptome atlas of Physcomitrella patens provides insights into the evolution and development of land plants. Molecular Plant 9: 205-220.
Pike LJ. 2009. The challenge of lipid rafts. Journal of Lipid Research 50(Suppl): S323-S328.
Quinn PJ, Wolf C. 2009. The liquid-ordered phase in membranes. Biochimica Biophysica Acta 1788: 33-46.
Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P-F, Lindquist EA, Kamisugi Y et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
Resemann HC, Herrfurth C, Feussner K, Hornung E, Ostendorf AK, Gömann J, Mittag J, van Gessel N, de Vries J, Ludwig-Müller J et al. 2021. Convergence of sphingolipid desaturation across over 500 million years of plant evolution. Nature Plants 7: 219-232.
Reski R, Abel WO. 1985. Induction of budding on chloronemata and caulonemata of the moss, Physcomitrella patens, using isopentenyladenine. Planta 165: 354-358.
Schaefer D, Zryd J-P, Knight CD, Cove DJ. 1991. Stable transformation of the moss Physcomitrella patens. Molecular and General Genetics 226: 418-424.
Scherp P, Grotha R, Kutschera U. 2001. Occurrence and phylogenetic significance of cytokinesis-related callose in green algae, bryophytes, ferns and seed plants. Plant Cell Reports 20: 143-149.
Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671-675.
Schuette S, Wood AJ, Geisler M, Geisler-Lee J, Ligrone R, Renzaglia KS. 2009. Novel localization of callose in the spores of Physcomitrella patens and phylogenomics of the callose synthase gene family. Annals of Botany 103: 749-756.
Shanklin J, Cahoon EB. 1998. Desaturation and related modifications of fatty acids. Annual Review of Plant Physiology and Plant Molecular Biology 49: 611-641.
Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA et al. 2007. Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Research 17: 1030-1040.
Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387: 569-572.
Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ. 2009. An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21: 581-594.
Slotte JP. 1999. Sphingomyelin-cholesterol interactions in biological and model membranes. Chemistry and Physics of Lipids 102: 13-27.
Slotte JP. 2016. The importance of hydrogen bonding in sphingomyelin's membrane interactions with co-lipids. Biochimica et Biophysica Acta 1858: 304-310.
Smith WL, Merrill AH Jr. 2002. Sphingolipid metabolism and signaling minireview series. Journal of Biological Chemistry 277: 25841-25842.
Sonnhammer E, von Heijne G, Krogh A. 1998. A hidden Markov model for predicting transmembrane helices in protein sequences. Proceedings on the International Conference on Intelligent Systems Molecular Biology 6: 175-182.
Sperling P, Franke S, Luthje S, Heinz E. 2005. Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? Plant Physiology and Biochemistry 43: 1031-1038.
Sperling P, Ternes P, Moll H, Franke S, Zähringer U, Heinz E. 2001. Functional characterization of sphingolipid C4-hydroxylase genes from Arabidopsis thaliana. FEBS Letters 494: 90-94.
Tarazona P, Feussner K, Feussner I. 2015. An enhanced plant lipidomics method based on multiplexed liquid chromatography-mass spectrometry reveals additional insights into cold- and drought-induced membrane remodeling. The Plant Journal 84: 621-633.
Tartaglio V, Rennie EA, Cahoon R, Wang G, Baidoo E, Mortimer JC, Cahoon EB, Scheller HV. 2017. Glycosylation of inositol phosphorylceramide sphingolipids is required for normal growth and reproduction in Arabidopsis. The Plant Journal 89: 278-290.
Tilsner J, Nicolas W, Rosado A, Bayer EM. 2016. Staying tight: Plasmodesmal membrane contact sites and the control of cell-to-cell connectivity in plants. Annual Review of Plant Biology 67: 337-364.
Vatén A, Dettmer J, Wu S, Stierhof YD, Miyashima S, Yadav SR, Roberts CJ, Campilho A, Bulone V, Lichtenberger R et al. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Developmental Cell 21: 1144-1155.
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. 2007. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
Yan D, Liu Y. 2020. Diverse regulation of plasmodesmal architecture facilitates adaptation to phloem translocation. Journal of Experimental Botany 71: 2505-2512.
Yanagawa D, Ishikawa T, Imai H. 2017. Synthesis and degradation of long-chain base phosphates affect fumonisin B1-induced cell death in Arabidopsis thaliana. Journal of Plant Research 130: 571-585.
Zavaliev R, Ueki S, Epel BL, Citovsky V. 2011. Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma 248: 117-130.
Zienkiewicz A, Gömann J, König S, Herrfurth C, Liu Y-T, Meldau D, Feussner I. 2020. Disruption of Arabidopsis neutral ceramidases 1 and 2 results in specific sphingolipid imbalances triggering different phytohormone-dependent plant cell death programs. New Phytologist 226: 170-188.

Auteurs

Jasmin Gömann (J)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.

Cornelia Herrfurth (C)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.
Service Unit for Metabolomics and Lipidomics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, D-37077, Germany.

Agnieszka Zienkiewicz (A)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.

Till Ischebeck (T)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.
Department of Plant Biochemistry, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, D-37077, Germany.

Tegan M Haslam (TM)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.

Ellen Hornung (E)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.

Ivo Feussner (I)

Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences, University of Göttingen, Göttingen, D-37077, Germany.
Service Unit for Metabolomics and Lipidomics, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, D-37077, Germany.
Department of Plant Biochemistry, Göttingen Center for Molecular Biosciences (GZMB), University of Göttingen, Göttingen, D-37077, Germany.

Articles similaires

Human prolyl hydroxylase domain 2 reacts with O

Giorgia Fiorini, Stephen A Marshall, William D Figg et al.
1.00
Humans Ketoglutaric Acids Hypoxia-Inducible Factor-Proline Dioxygenases Oxygen Hypoxia-Inducible Factor 1, alpha Subunit

Specialized contact sites regulate the fusion of chlamydial inclusion membranes.

Christine Linton, Jordan Wesolowski, Anna Lobley et al.
1.00
Chlamydia trachomatis Inclusion Bodies Membrane Fusion HeLa Cells Humans
Animals Myelin Sheath Charcot-Marie-Tooth Disease Rats Nerve Fibers, Myelinated
Xylans Phylogeny RNA, Ribosomal, 16S Glucans Genome, Bacterial

Classifications MeSH