Identification of a sphingolipid α-glucuronosyltransferase that is essential for pollen function in Arabidopsis

Plant Cell

Volumn 26, Issue 8, 2014, Pages 3314-3325

  Rennie, Emilie A ^a,b,c   Ebert, Berit ^a,b   Miles, Godfrey P ^d   Cahoon, Rebecca E ^e   Christiansen, Katy M ^a,b   Stonebloom, Solomon ^a,b   Khatab, Hoda ^e   Twell, David ^f   Petzold, Christopher J ^a,b   Adams, Paul D ^a,b,g   Dupree, Paul ^d   Heazlewood, Joshua L ^a,b   Cahoon, Edgar B ^e   Scheller, Henrik Vibe ^a,b,c  

^a JOINT BIOENERGY INSTITUTE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^f UNIVERSITY OF LEICESTER   (United Kingdom)

^g University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; GLUCURONIC ACID; GLUCURONOSYLTRANSFERASE; IPUT1 PROTEIN, ARABIDOPSIS; SPHINGOLIPID;

ARABIDOPSIS; ENZYMOLOGY; GENE SILENCING; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; POLLEN; SACCHAROMYCES CEREVISIAE; TOBACCO;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE SILENCING; GLUCURONIC ACID; GLUCURONOSYLTRANSFERASE; HUMANS; POLLEN; SACCHAROMYCES CEREVISIAE; SPHINGOLIPIDS; TOBACCO;

EID: 84907450443     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.129171     Document Type: Article

References (70)

1. Beeler, T.J., Fu, D., Rivera, J., Monaghan, E., Gable, K., and Dunn, T.M. (1997). SUR1 (CSG1/BCL21), a gene necessary for growth of Saccharomyces cerevisiae in the presence of high Ca2+ concentrations at 37 ° C, is required for mannosylation of inositolphosphorylceramide. Mol. Gen. Genet. 255: 570-579.
2. Boavida, L.C., and McCormick, S. (2007). Technical advance: temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. 52: 570-582.
3. Borner, G.H.H., Sherrier, D.J., Weimar, T., Michaelson, L.V., Hawkins, N.D., Macaskill, A., Napier, J.A., Beale, M.H., Lilley, K.S., and Dupree, P. (2005). Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137: 104-116.
4. Bromley, P.E., Li, Y.O., Murphy, S.M., Sumner, C.M., and Lynch, D.V. (2003). Complex sphingolipid synthesis in plants: characterization of inositolphosphorylceramide synthase activity in bean microsomes. Arch. Biochem. Biophys. 417: 219-226.
5. Brownfield, L., Hafidh, S., Borg, M., Sidorova, A., Mori, T., and Twell, D. (2009). A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet. 5: e1000430.
6. Burch-Smith, T.M., Anderson, J.C., Martin, G.B., and Dinesh-Kumar, S.P. (2004). Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J. 39: 734-746.
7. Buré, C., Cacas, J.-L., Wang, F., Gaudin, K., Domergue, F., Mongrand, S., and Schmitter, J.-M. (2011). Fast screening of highly glycosylated plant sphingolipids by tandem mass spectrometry. Rapid Commun. Mass Spectrom. 25: 3131-3145.
8. Cacas, J.-L., Buré, C., Furt, F., Maalouf, J.-P., Badoc, A., Cluzet, S., Schmitter, J.-M., Antajan, E., and Mongrand, S. (2013). Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity. Phytochemistry 96: 191-200.
9. Carter, H.E., Strobach, D.R., and Hawthorne, J.N. (1969). Biochemistry of the sphingolipids. 18. Complete structure of tetrasaccharide phytoglycolipid. Biochemistry 8: 383-388.
10. Chao, D.-Y., et al. (2011). Sphingolipids in the root play an important role in regulating the leaf ionome in Arabidopsis thaliana. Plant Cell 23: 1061-1081.
11. Chatterjee, M., Berbezy, P., Vyas, D., Coates, S., and Barsby, T. (2005). Reduced expression of a protein homologous to glycogenin leads to reduction of starch content in Arabidopsis leaves. Plant Sci. 168: 501-509.
12. Chen, M., Markham, J.E., and Cahoon, E.B. (2012). Sphingolipid D8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J. 69: 769-781.
13. Chen, M., Han, G., Dietrich, C.R., Dunn, T.M., and 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.
14. Cheung, A.Y., and Wu, H.M. (2008). Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu. Rev. Plant Biol. 59: 547-572.
15. Coskun, Ü., Grzybek, M., Drechsel, D., and Simons, K. (2011). Regulation of human EGF receptor by lipids. Proc. Natl. Acad. Sci. USA 108: 9044-9048.
16. Coursol, S., Le Stunff, H., Lynch, D.V., Gilroy, S., Assmann, S.M., and Spiegel, S. (2005). Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture. Plant Physiol. 137: 724-737.
17. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.-R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
18. Dietrich, C.R., Han, G., Chen, M., Berg, R.H., Dunn, T.M., and Cahoon, E.B. (2008). Loss-of-function 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.
19. Dunkley, T.P.J., Watson, R., Griffin, J.L., Dupree, P., and Lilley, K.S. (2004). Localization of organelle proteins by isotope tagging (LOPIT). Mol. Cell. Proteomics 3: 1128-1134.
20. Dunn, T.M., Haak, D., Monaghan, E., and Beeler, T.J. (1998). Synthesis of monohydroxylated inositolphosphorylceramide (IPC-C) in Saccharomyces cerevisiae requires Scs7p, a protein with both a cytochrome b5-like domain and a hydroxylase/desaturase domain. Yeast 14: 311-321.
21. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
22. Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797.
23. Eudes, A., Baidoo, E.E., Yang, F., Burd, H., Hadi, M.Z., Collins, F.W., Keasling, J.D., and Loqué, D. (2011). Production of tranilast [N-(39,49-dimethoxycinnamoyl)-anthranilic acid] and its analogs in yeast Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 89: 989-1000.
24. Goubet, F., Misrahi, A., Park, S.K., Zhang, Z., Twell, D., and Dupree, P. (2003). AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol. 131: 547-557.
25. Guan, X.L., and Wenk, M.R. (2006). Mass spectrometry-based profiling of phospholipids and sphingolipids in extracts from Saccharomyces cerevisiae. Yeast 23: 465-477.
26. Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59: 307-321.
27. Hannun, Y.A., and Obeid, L.M. (2008). Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9: 139-150.
28. Hillig, I., Leipelt, M., Ott, C., Zähringer, U., Warnecke, D., and Heinz, E. (2003). Formation of glucosylceramide and sterol glucoside by a UDP-glucose-dependent glucosylceramide synthase from cotton expressed in Pichia pastoris. FEBS Lett. 553: 365-369.
29. Honys, D., and Twell, D. (2004). Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5: R85.
30. Howden, R., Park, S.K., Moore, J.M., Orme, J., Grossniklaus, U., and Twell, D. (1998). Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149: 621-631.
31. Kaul, K., and 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.
32. Kaul, K., and Lester, R.L. (1978). Isolation of six novel phosphoinositol-containing sphingolipids from tobacco leaves. Biochemistry 17: 3569-3575.
33. Kimberlin, A.N., Majumder, S., Han, G., Chen, M., Cahoon, R.E., Stone, J.M., Dunn, T.M., and Cahoon, E.B. (2013). Arabidopsis 56-amino acid serine palmitoyltransferase-interacting proteins stimulate sphingolipid synthesis, are essential, and affect mycotoxin sensitivity. Plant Cell 25: 4627-4639.
34. Klinghammer, M., and Tenhaken, R. (2007). Genome-wide analysis of the UDP-glucose dehydrogenase gene family in Arabidopsis, a key enzyme for matrix polysaccharides in cell walls. J. Exp. Bot. 58: 3609-3621.
35. Kushnirov, V.V. (2000). Rapid and reliable protein extraction from yeast. Yeast 16: 857-860.
36. Lalanne, E., Honys, D., Johnson, A., Borner, G.H.H., Lilley, K.S., Dupree, P., Grossniklaus, U., and Twell, D. (2004). SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell 16: 229-240.
37. Liang, H., Yao, N., Song, J.T., Luo, S., Lu, H., and Greenberg, J.T. (2003). Ceramides modulate programmed cell death in plants. Genes Dev. 17: 2636-2641.
38. Liu, P., Li, R.-L., Zhang, L., Wang, Q.-L., Niehaus, K., Baluška, F., Samaj, J., and Lin, J.-X. (2009). Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J. 60: 303-313.
39. Liu, Y., Schiff, M., Marathe, R., and Dinesh-Kumar, S.P. (2002). Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N- mediated resistance to tobacco mosaic virus. Plant J. 30: 415-429.
40. Loqué, D., Lalonde, S., Looger, L.L., von Wiren, N., and Frommer, W. (2007). A cytosolic trans-activation domain essential for ammonium uptake. Nature 446: 195-198.
41. Markham, J.E., and 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 Commun. Mass Spectrom. 21: 1304-1314.
42. Markham, J.E., Li, J., Cahoon, E.B., and Jaworski, J.G. (2006). Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 281: 22684-22694.
43. Markham, J.E., Lynch, D.V., Napier, J.A., Dunn, T.M., and Cahoon, E.B. (2013). Plant sphingolipids: function follows form. Curr. Opin. Plant Biol. 16: 350-357.
44. Markham, J.E., Molino, D., Gissot, L., Bellec, Y., Hématy, K., Marion, J., Belcram, K., Palauqui, J.-C., Satiat-Jeunemaître, B., and 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.
45. Mortimer, J.C., Miles, G.P., Brown, D.M., Zhang, Z., Segura, M.P., Weimar, T., Yu, X., Seffen, K.A., Stephens, E., Turner, S.R., and Dupree, P. (2010). Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc. Natl. Acad. Sci. USA 107: 17409-17414.
46. Mina, J.G., Okada, Y., Wansadhipathi-Kannangara, N.K., Pratt, S., Shams-Eldin, H., Schwarz, R.T., Steel, P.G., Fawcett, T., and Denny, P.W. (2010). Functional analyses of differentially expressed isoforms of the Arabidopsis inositol phosphorylceramide synthase. Plant Mol. Biol. 73: 399-407.
47. Mortimer, J.C., et al. (2013). Abnormal glycosphingolipid mannosylation triggers salicylic acid-mediated responses in Arabidopsis. Plant Cell 25: 1881-1894.
48. Muraoka, M., Kawakita, M., and Ishida, N. (2001). Molecular characterization of human UDP-glucuronic acid/UDP-N-acetylgalactosamine transporter, a novel nucleotide sugar transporter with dual substrate specificity. FEBS Lett. 495: 87-93.
49. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
50. Obeid, L.M., Okamoto, Y., and Mao, C. (2002). Yeast sphingolipids: metabolism and biology. Biochim. Biophys. Acta 1585: 163-171.
51. Oikawa, A., Joshi, H.J., Rennie, E.A., Ebert, B., Manisseri, C., Heazlewood, J.L., and Scheller, H.V. (2010). An integrative approach to the identification of Arabidopsis and rice genes involved in xylan and secondary wall development. PLoS ONE 5: e15481.
52. Park, S.K., Howden, R., and Twell, D. (1998). The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125: 3789-3799.
53. Parsons, H.T., et al. (2012). Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol. 159: 12-26.
54. Perotto, S., Donovan, N., Drobak, B.K., and Brewin, N.J. (1995). Differential expression of a glycosyl inositol phospholipid antigen on the peribacteroid membrane during pea nodule development. Mol. Plant Microbe Interact. 8: 560-568.
55. Pinto, W.J., Srinivasan, B., Shepherd, S., Schmidt, A., Dickson, R.C., and Lester, R.L. (1992). Sphingolipid long-chain-base auxotrophs of Saccharomyces cerevisiae: genetics, physiology, and a method for their selection. J. Bacteriol. 174: 2565-2574.
56. Rennie, E.A., Hansen, S.F., Baidoo, E.E.K., Hadi, M.Z., Keasling, J.D., and Scheller, H.V. (2012). Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol. 159: 1408-1417.
57. Schmittgen, T.D., and Livak, K.J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3: 1101-1108.
58. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9: 671-675.
59. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
60. Simons, K., and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1: 31-39.
61. Sperling, P., and Heinz, E. (2003). Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim. Biophys. Acta 1632: 1-15.
62. Sperling, P., Franke, S., Lüthje, S., and Heinz, E. (2005). Are glucocerebrosides the predominant sphingolipids in plant plasma membranes? Plant Physiol. Biochem. 43: 1031-1038.
63. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2002). Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29: 417-426.
64. Ternes, P., Feussner, K., Werner, S., Lerche, J., Iven, T., Heilmann, I., Riezman, H., and Feussner, I. (2011). Disruption of the ceramide synthase LOH1 causes spontaneous cell death in Arabidopsis thaliana. New Phytol. 192: 841-854.
65. Tsegaye, Y., Richardson, C.G., Bravo, J.E., Mulcahy, B.J., Lynch, D.V., Markham, J.E., Jaworski, J.G., Chen, M., Cahoon, E.B., and Dunn, T.M. (2007). Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J. Biol. Chem. 282: 28195-28206.
66. Valdivia, E.R., Herrera, M.T., Gianzo, C., Fidalgo, J., Revilla, G., Zarra, I., and Sampedro, J. (2013). Regulation of secondary wall synthesis and cell death by NAC transcription factors in the monocot Brachypodium distachyon. J. Exp. Bot. 64: 1333-1343.
67. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3: H0034.
68. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
69. Wang, W., et al. (2008). An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20: 3163-3179.
70. Zäuner, S., Ternes, P., and Warnecke, D. (2010). Biosynthesis of sphingolipids in plants (and some of their functions). In Sphingolipids as Signaling and Regulatory Molecules, C. Chalfant and M. Poeta, eds (New York: Springer), pp. 249-263.