Sphingolipid metabolism is strikingly different between pollen and leaf in Arabidopsis as revealed by compositional and gene expression profiling

Phytochemistry

Volumn 115, Issue 1, 2015, Pages 121-129

  Luttgeharm, Kyle D ^a   Kimberlin, Athen N ^a   Cahoon, Rebecca E ^a   Cerny, Ronald L ^a   Napier, Johnathan A ^b   Markham, Jennifer E ^a   Cahoon, Edgar B ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Arabidopsis thaliana; Brassicaceae; Glucosylceramide; Glycosylinositolphosphoceramide; Lipidomics; Pollen; Sphingolipid

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICACEAE; SPHINGOIDEA;

GLUCOSYLCERAMIDE; SPHINGOLIPID;

ARABIDOPSIS; GENE EXPRESSION PROFILING; METABOLISM; PLANT LEAF; POLLEN;

ARABIDOPSIS; GENE EXPRESSION PROFILING; GLUCOSYLCERAMIDES; PLANT LEAVES; POLLEN; SPHINGOLIPIDS;

EID: 84935020886     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2015.02.019     Document Type: Article

References (41)

1. Alexander, M. P., 1969. Differential staining of aborted and nonaborted pollen. Stain Technol. 44, 117-122.
2. Borner, G. H., Sherrier, D. J., Weimar, T., Michaelson, L. V., Hawkins, N. D., Macaskill, A., Napier, J. A., Beale, M. H., Lilley, K. S., Dupree, P., 2005. Analysis of detergentresistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104-116.
3. Brodersen, P., Petersen, M., Pike, H. M., Olszak, B., Skov, S., Odum, N., Jørgensen, L. B., Brown, R. E., Mundy, J., 2002. Knockout of Arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16, 490-502.
4. Buré, C., Cacas, J.-L., Wang, F., Gaudin, K., Domergue, F., Mongrand, S., Schmitter, J.-M., 2011. Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry. Rapid Comm. Mass Spec. 25, 3131-3145.
5. Buré, C., Cacas, J.-L., Mongrand, S., Schmitter, J.-M., 2014. Characterization of glycosyl inositol phosphoryl ceramides from plants and fungi by mass spectrometry. Anal. Bioanal. Chem. 406, 995-1010.
6. Cacas, J.-L., Buré, 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.
7. Cantrel, C., Vazquez, T., Puyaubert, J., Reze, N., Lesch, M., Kaiser, W. M., Dutilleul, C., Guillas, I., Zachowski, A., Baudouin, E., 2011. Nitric oxide participates in coldresponsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol. 189, 415-427.
8. Chen, M., Cahoon, E. B., Saucedo-García, M., Plasencia, J., Gavilanes-Ruíz, M., 2010. Plant sphingolipids: structure, synthesis and function. In: Wada, H., Murata, N. (Eds.), Lipids in Photosynthesis, vol. 30. Springer, Netherlands, pp. 77-115.
9. Chen, M., Han, G., Dietrich, C. R., Dunn, T. M., Cahoon, E. B., 2006. The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell 18, 3576-3593.
10. Chen, M., Markham, J. E., Cahoon, E. B., 2012. Sphingolipid D8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J. 69, 769-781.
11. Chen, M., Markham, J. E., Dietrich, C. R., Jaworski, J. G., Cahoon, E. B., 2008. Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell 20, 1862-1878.
12. Coursol, S., Fan, L. M., Le Stunff, H., Spiegel, S., Gilroy, S., Assmann, S. M., 2003. Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423, 651-654.
13. Coursol, S., Le Stunff, H., Lynch, D. V., Gilroy, S., Assmann, S. M., Spiegel, S., 2005. Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture. Plant Physiol. 137, 724-737.
14. Dietrich, C. R., Han, G., Chen, M., Berg, R. H., Dunn, T. M., Cahoon, E. B., 2008. Loss-offunction mutations and inducible RNAi suppression of Arabidopsis LCB2 genes reveal the critical role of sphingolipids in gametophytic and sporophytic cell viability. Plant J. 54, 284-298.
15. Guillas, I., Guellim, A., Reze, N., Baudouin, E., 2012. Long chain base changes triggered by a short exposure of Arabidopsis to low temperature are altered by AHb1 non-symbiotic haemoglobin overexpression. Plant Physiol. Biochem. 63 C, 191-195.
16. Honys, D., Twell, D., 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 132, 640-652.
17. Hsieh, T. C., Kaul, K., Laine, R. A., Lester, R. L., 1978. Structure of a major glycophosphoceramide from tobacco leaves, PSL-I:2-deoxy-2-acetamido-D-glucopyranosyl (α1 → 4)-D-glucuronopyranosyl (α1 → 2) myoinositol-1-O-phosphoceramide. Biochemistry 17, 3575-3581.
18. Hsieh, T. C., Lester, R. L., Laine, R. A., 1981. Glycophosphoceramides from plants. Purification and characterization of a novel tetrasaccharide derived from tobacco leaf glycolipids. J. Biol. Chem. 256, 7747-7755.
19. Imai, H., Yamamoto, K., Shibahara, A., Miyatani, S., Nakayama, T., 2000. Determining double-bond positions in monoenoic 2-hydroxy fatty acids of glucosylceramides by gas chromatography-mass spectrometry. Lipids 35, 233-236.
20. Islam, M. N., Jacquemot, M. P., Coursol, S., Ng, C. K., 2012. Sphingosine in plants-more riddles from the Sphinx? New Phytol. 193, 51-57.
21. Johnson-Brousseau, S. A., McCormick, S., 2004. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J. 39, 761-775.
22. Kaul, K., Lester, R. L., 1975. Characterization of inositol-containing phosphosphingolipids from tobacco leaves: isolation and identification of two novel, major lipids: N-acetylglucosamidoglucuronidoinositol phosphorylceramide and glucosamidoglucuronidoinositol phosphorylceramide. Plant Physiol. 55, 120-129.
23. Kaul, K., Lester, R. L., 1978. Isolation of six novel phosphoinositol-containing sphingolipids from tobacco leaves. Biochem. 17, 3569-3575.
24. Kimberlin, A. N., Majumder, S., Han, G., Chen, M., Cahoon, R. E., Stone, J. M., Dunn, T. M., Cahoon, E., 2013. Arabidopsis 56-amino acid serine palmitoyltransferaseinteracting proteins stimulate sphingolipid synthesis, are essential, and affect mycotoxin sensitivity. Plant Cell 25, 4627-4639.
25. Loraine, A. E., McCormick, S., Estrada, A., Patel, K., Qin, P., 2013. RNA-Seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol. 162, 1092-1109.
26. Lynch, D. V., Dunn, T. M., 2004. An introduction to plant sphingolipids and a review of recent advances in understanding their metabolism and function. New Phytol. 161, 677-702.
27. Markham, J. E., Jaworski, J. G., 2007. Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Comm. Mass Spec. 21, 1304-1314.
28. Markham, J. E., Li, J., Cahoon, E. B., Jaworski, J. G., 2006. Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 281, 22684-22694.
29. Markham, J. E., 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.
30. Michaelson, L. V., Zauner, S., Markham, J. E., Haslam, R. P., Desikan, R., Mugford, S., Albrecht, S., Warnecke, D., Sperling, P., Heinz, E., Napier, J. A., 2009. Functional characterization of a higher plant sphingolipid D4-desaturase: defining the role of sphingosine and sphingosine-1-phosphate in Arabidopsis. Plant Physiol. 149, 487-498.
31. Mongrand, S., Morel, J., Laroche, J., Claverol, S., Carde, J.-P., Hartmann, M.-A., Bonneu, M., Simon-Plas, F., Lessire, R., Bessoule, J.-J., 2004. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J. Biol. Chem. 279, 36277-36286.
32. Mortimer, J. C., Yu, X., Albrecht, S., Sicilia, F., Huichalaf, M., Ampuero, D., Michaelson, L. V., Murphy, A. M., Matsunaga, T., Kurz, S., Stephens, E., Baldwin, T. C., Ishii, T., Napier, J. A., Weber, A. P., Handford, M. G., Dupree, P., 2013. Abnormal glycosphingolipid mannosylation triggers salicylic acid-mediated responses in Arabidopsis. Plant Cell 25, 1881-1894.
33. 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 ceramidemodifying enzymes. Planta 240, 77-89.
34. Ng, C. K., Carr, K., McAinsh, M. R., Powell, B., Hetherington, A. M., 2001. Droughtinduced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410, 596-599.
35. Rennie, E. A., Ebert, B., Miles, G. P., Cahoon, R. E., Christiansen, K. M., Stonebloom, S., Khatab, H., Twell, D., Petzold, C. J., Adams, P. D., Dupree, P., Heazlewood, J. L., Cahoon, E. B., Scheller, H. V., 2014. Identification of a sphingolipid aglucuronosyltransferase that is essential for pollen function in Arabidopsis. Plant Cell 26, 3314-3325.
36. Saucedo-García, M., Guevara-García, A., González-Solís, A., Cruz-García, F., Vázquez-Santana, S., Markham, J. E., Lozano-Rosas, M., Dietrich, C. R., Ramos-Vega, M., Cahoon, E. B., Gavilanes-Ruíz, M., 2011. MPK6, sphinganine and the LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis. New Phytol. 191, 943-957.
37. Sperling, P., Franke, S., Luthje, S., Heinz, E., 2005. Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? Plant Physiol. Biochem. 43, 1031-1038.
38. Sperling, P., Zahringer, U., Heinz, E., 1998. A sphingolipid desaturase from higher plants. Identification of a new cytochrome b5 fusion protein. J. Biol. Chem. 273, 28590-28596.
39. Tellier, F., Maia-Grondard, A., Schmitz-Afonso, I., Faure, J. D., 2014. Comparative plant sphingolipidomic reveals specific lipids in seeds and oil. Phytochemistry 103, 50-58.
40. 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.
41. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G. V., Provart, N. J., 2007. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing largescale biological data sets. PLoS ONE 2, e718.