Abstract
∆8-sphingolipid desaturase catalyzes the C8 desaturation of a long chain base, which is the characteristic structure of various complex sphingolipids. The genes of 20 ∆8-sphingolipid desaturases from 12 plants were identified and functionally detected by using Saccharomyces cerevisiae system to elucidate the relationship between the biochemical function and evolution of this enzyme. Results showed that the 20 genes all can encode a functional ∆8-sphingolipid desaturase, which catalyzes different ratios of two products, namely, 8(Z) and 8(E)-C18-phytosphingenine. The coded enzymes could be divided into two groups on the basis of biochemical functions: ∆8-sphingolipid desaturase with a preference for an E-isomer product and ∆8-sphingolipid desaturase with a preference for a Z-isomer product. The conversion rate of the latter was generally lower than that of the former. Phylogenetic analysis revealed that the 20 desaturases could also be clustered into two groups, and this grouping is consistent with that of the biochemical functions. Thus, the biochemical function of ∆8-sphingolipid desaturase is correlated with its evolution. The two groups of ∆8-sphingolipid desaturases could arise from distinct ancestors in higher plants. However, they might have initially evolved from ∆8-sphingolipid desaturases in lower organisms, such as yeasts, which can produce E-isomer products only. Furthermore, almost all of the transgenic yeasts harboring ∆8-sphingolipid desaturase genes exhibit an improvement in aluminum tolerance. Our study provided new insights into the biochemical function and evolution of ∆8-sphingolipid desaturases in plants.
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Abbreviations
- LCB:
-
Long chain base
- HSP:
-
High score pairs
- PCR:
-
Polymerase chain reaction
- ORF:
-
Open reading frame
- UPLC:
-
Ultra-performance liquid chromatography
- t18:0:
-
C18-phytosphinganine
- t18:18Z :
-
8(Z)-C18-phytosphinganine
- t18:18E :
-
8(E)-C18-phytosphinganine
- HPLC/ESI–MS/MS:
-
High-performance liquid chromatotraphy/electrospray ionization tandem mass spectrometry
References
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. Biochem Biophys Res Commun 410:574–580. doi:10.1016/j.bbrc.2011.06.028
Borner GHH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, MacAskill A, Napier JA, Beale MH, Lilley KS, Dupree P (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol 137:104–116. doi:10.1104/pp.104.053041
Chavez JA, Siddique MM, Wang ST, Ching J, Shayman JA, Summers SA (2014) Ceramides and glucosylceramides are independent antagonists of insulin signaling. J Biol Chem 289:723–734. doi:10.1074/jbc.M113.522847
Chen M, Cahoon EB (2009) Plant sphingolipids: structure, synthesis and function. Lipids in photosynthesis: essential and regulatory functions, pp 77‒115
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. doi:10.1105/tpc.107.057851
Chen M, Markham JE, Cahoon EB (2012) Sphingolipid ∆8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J 69:769–781. doi:10.1111/j.1365-313X.2011.04829.x
Coursol S, Fan LM, Stunff HL, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423:651–654
da Silva ALS, Sperling P, Horst W, Franke S, Ott C, Becker D, Staß A, Lörz H, Heinz E (2006) A possible role of sphingolipids in the aluminium resistance of yeast and maize. J Plant Physiol 163:26–38. doi:10.1016/j.jplph.2005.03.009
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Elble R (1992) A simple and efficient procedure for transformation of yeasts. Biotechniques 13:18–20
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:10.2307/2408678
García-Maroto F, Garrido-Cárdenas JA, Michaelson LV, Napier JA, Alonso DL (2007) Cloning and molecular characterisation of a Δ8-sphingolipid-desaturase from Nicotiana tabacum closely related to Δ6-acyl-desaturases. Plant Mol Biol 64:241–250. doi:10.1007/s11103-007-9148-9
Laloi M, Perret AM, Chatre L, Melser S, Cantrel C, Vaultier MN, Zachowski A, Bathany K, Schmitter JM, Vallet M, Lessire R, Hartmann MA, Moreau P (2007) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143:461–472. doi:10.1104/pp.106.091496
Li SF, Song LY, Zhang GJ, Yin WB, Chen YH, Wang RRC, Hu ZM (2011) Newly identified essential amino acid residues affecting Δ8-sphingolipid desaturase activity revealed by site-directed mutagenesis. Biochem Biophy Res Commun 416:165–171. doi:10.1016/j.bbrc.2011.11.017
Li SF, Song LY, Yin WB, Chen YH, Chen L, Li JL, Wang RRC, Hu ZM (2012) Isolation and functional characterisation of the genes encoding Δ8-sphingolipid desaturase from Brassica rapa. J Genet Genom 39:47–59. doi:10.1016/j.jgg.2011.12.002
Li SF, Zhang GJ, Yuan YC, Wang CH, Gao WJ, Deng CL, Lu LD, Hu ZM (2014) Three homologous genes encoding functional Δ8-sphingolipid desaturase in Populus tomentosa. Gene Genom 36:293–301. doi:10.1007/s13258-013-0167-4
Los DA, Murata N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394:3–15. doi:10.1016/S0005-2760(98)00091-5
Luttgeharm KD, Chen M, Mehra A, Cahoon RE, Markham JE, Cahoon EB (2015) Overexpression of Arabidopsis ceramide synthases differentially affects growth, sphingolipid metabolism, programmed cell death, and mycotoxin resistance. Plant Physiol 169:1108–1117. doi:10.1104/pp.15.00987
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 Commun Mass Spectrom 21:1304–1314. doi:10.1002/rcm.2962
Markham JE, Li J, Cahoon EB, Jaworski JG (2006) Separation and identification of major plant sphingolipid classes from leaves. J Biol Chem 281:22684–22694. doi:10.1074/jbc.M604050200
Michaelson LV, Longman AJ, Sayanova O, Stobart AK, Napier JA (2002) Isolation and characterization of a cDNA encoding a Δ8 sphingolipid desaturase from Aquilegia vulgaris. Biochem Soc Trans 30:1073–1075. doi:10.1042/bst0301073
Michaelson LV, Zäuner S, Markham JE, Haslam RP, Desikan R, Mugford S, Albrecht S, Warnecke D, Sperling P, Heinz E, Napier JA (2009) Functional characterization of a higher plant sphingolipid Δ4-desaturase: defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis. Plant Physiol 149:487–498. doi:10.1104/pp.108.129411
Mongrand S, Stanislas T, Bayer EMF, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656–663. doi:10.1016/j.tplants.2010.09.003
Moreno-Pérez AJ, Martínez-Force E, Garcés R, Salas JJ (2011) Sphingolipid base modifying enzymes in sunflower (Helianthus annuus): cloning and characterization of a C4-hydroxylase gene and a new paralogous Δ8-desaturase gene. J Plant Physiol 168:831–839. doi:10.1016/j.jplph.2010.11.015
Nagano M, Ishikawa T, Ogawa Y, Iwabuchi M, Nakasone A, Shimamoto K, Uchimiya H, Kawai-Yamada M (2014) Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes. Planta 240:77–89. doi:10.1007/s00425-014-2065-7
Paramelle D, Nieves D, Brun B, Kraut RS, Fernig DG (2015) Targeting cell membrane lipid rafts by stoichiometric functionalization of gold nanoparticles with a sphingolipid-binding domain peptide. Adv Healthc Mater 4:911–917. doi:10.1002/adhm.201400730
Pata MO, Hannun YA, Ng CKY (2010) Plant sphingolipids: decoding the enigma of the Sphinx. New Phytol 185:611–630. doi:10.1111/j.1469-8137.2009.03123.x
Ryan PR, Liu Q, Sperling P, Dong B, Franke S, Delhaize E (2007) A higher plant Δ8 sphingolipid desaturase with a preference for (Z)-isomer formation confers aluminum tolerance to yeast and plants. Plant Physiol 144:1968–1977. doi:10.1104/pp.107.100446
Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids. Annu Rev Plant Physiol Plant Mol Biol 49:611–641. doi:10.1146/annurev.arplant.49.1.611
Shanklin J, Whittle E, Fox BG (1994) Eight histidine residues are catalytically essential in a membrane-associated iron enzyme, stearoyl-CoA desaturase, and are conserved in alkane hydroxylase and xylene monooxygenase. Biochemistry 33:12787–12794. doi:10.1021/bi00209a009
Song LY, Lu WX, Hu J, Zhang Y, Yin WB, Chen YH, Hao ST, Wang BL, Wang RRC, Hu ZM (2010) Identification and functional analysis of the genes encoding Δ6-desaturase from Ribes nigrum. J Exp Bot 61:1827–1838. doi:10.1093/jxb/erq051
Sperling P, Heinz E (2003) Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim Biophys Acta Mol Cell Biol Lipids 1632:1–15. doi:10.1016/S1388-1981(03)00033-7
Sperling P, Zähringer U, Heinz E (1998) A sphingolipid desaturase from higher plants. J Biol Chem 273:23590–28596. doi:10.1074/jbc.273.44.28590
Sperling P, Zähringer U, Heinz E (2000) Further characterization of Δ8-sphingolipid desaturases from higher plants. Biochem Soc Trans 28:638–641. doi:10.1042/bst0280638
Sperling P, Libisch B, Zähringer U, Napier JA, Heinz E (2001) Functional identification of a Δ8-sphingolipid desaturase from Borago officinalis. Arch Biochem Biophys 388:293–298. doi:10.1006/abbi.2001.2308
Sperling P, Franke S, Lüthje S, Heinz E (2005) Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? Plant Physiol Biochem 43:1031–1038. doi:10.1016/j.plaphy.2005.10.004
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092
Teng C, Dong H, Shi L, Deng Y, Mu J, Zhang J, Yang X, Zuo J (2008) Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis. Plant Physiol 146:1322–1332. doi:10.1104/pp.107.113506
Worrall D, Ng CKY, Hetherington AM (2003) Sphingolipids, new players in plant signaling. Trends Plant Sci 8:317–320. doi:10.1016/S1360-1385(03)00128-6
Acknowledgments
This work was supported by Grants from the National Natural Science foundation of China (31300202 and 31470334).
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Fig. S1 Alignment of the deduced amino acid sequences of various ∆8-sphingolipid desaturase genes isolated in this study. Only partial sequences representing conserved regions are shown. Numbers on the right denote the number of amino acid residues. Characteristic regions of the N-terminal cytb 5 motif are labeled by dots, and the three conserved histidine boxes are underlined (PDF 8370 kb)
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Li, SF., Zhang, GJ., Zhang, XJ. et al. Genes encoding Δ8-sphingolipid desaturase from various plants: identification, biochemical functions, and evolution. J Plant Res 129, 979–987 (2016). https://doi.org/10.1007/s10265-016-0838-8
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DOI: https://doi.org/10.1007/s10265-016-0838-8