Multiple n-glycans cooperate in the subcellular targeting and functioning of arabidopsis KORRIGAN1

Plant Cell

Volumn 26, Issue 9, 2014, Pages 3792-3808

  Rips, Stephan ^a   Bentley, Nolan ^b   Jeong, In Sil ^b   Welch, Justin L ^b   von Schaewen, Antje ^a   Koiwa, Hisashi ^b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CELLULASE; DOLICHYL-DIPHOSPHOOLIGOSACCHARIDE - PROTEIN GLYCOTRANSFERASE; GLYCOSYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; KOR1 PROTEIN, ARABIDOPSIS; MEMBRANE PROTEIN; POLYSACCHARIDE;

ARABIDOPSIS; BIOLOGICAL MODEL; CELL FRACTIONATION; CELL MEMBRANE; CHEMICAL STRUCTURE; ENZYMOLOGY; EPISTASIS; GENETICS; GLYCOSYLATION; GOLGI COMPLEX; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; PROTEIN TRANSPORT; PROTOPLAST; REPORTER GENE; SITE DIRECTED MUTAGENESIS; TRANS GOLGI NETWORK;

AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL MEMBRANE; CELLULASE; CONSERVED SEQUENCE; EPISTASIS, GENETIC; GENES, REPORTER; GLYCOSYLATION; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HEXOSYLTRANSFERASES; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; POLYSACCHARIDES; PROTEIN TRANSPORT; PROTOPLASTS; SUBCELLULAR FRACTIONS; TRANS-GOLGI NETWORK;

EID: 84908243917     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.129718     Document Type: Article

References (73)

1. Adney, W. S., Jeoh, T., Beckham, G. T., Chou, Y. C., Baker, J. O., Michener, W., Brunecky, R., and Himmel, M. E. (2009). Probing the role of N-linked glycans in the stability and activity of fungal cellobiohydrolases by mutational analysis. Cellulose 16: 699-709.
2. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006). The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
3. Barre, A., Herve, C., Lescure, B., and Rouge, P. (2002). Lectin receptor kinases in plants. Crit. Rev. Plant Sci. 21: 379-399.
4. Bashline, L., Li, S., Anderson, C. T., Lei, L., and Gu, Y. (2013). The endocytosis of cellulose synthase in Arabidopsis is dependent on μ 2, a clathrin-mediated endocytosis adaptin. Plant Physiol. 163: 150-160.
5. Batistic, O. (2012). Genomics and localization of the Arabidopsis DHHCcysteine-rich domain S-acyltransferase protein family. Plant Physiol. 160: 1597-1612.
6. Borner, G. H., Lilley, K. S., Stevens, T. J., and Dupree, P. (2003). Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol. 132: 568-577.
7. Cheng, M., Fry, J. E., Pang, S., Zhou, H., Hironaka, C. M., Duncan, D. R., Conner, T. W., and Wan, Y. (1997). Genetic transformation of wheat mediated by Agrobacterium tumefaciens. Plant Physiol. 115: 971-980.
8. Chung, M.-H., Chen, M.-K., and Pan, S.-M. (2000). Floral spray transformation can efficiently generate Arabidopsis transgenic plants. Transgenic Res. 9: 471-476.
9. Collings, D. A., Gebbie, L. K., Howles, P. A., Hurley, U. A., Birch, R. J., Cork, A. H., Hocart, C. H., Arioli, T., and Williamson, R. E. (2008). Arabidopsis dynamin-like protein DRP1A: a null mutant with widespread defects in endocytosis, cellulose synthesis, cytokinesis, and cell expansion. J. Exp. Bot. 59: 361-376.
10. Drakakaki, G., van de Ven, W., Pan, S., Miao, Y., Wang, J., Keinath, N. F., Weatherly, B., Jiang, L., Schumacher, K., Hicks, G., and Raikhel, N. (2012). Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 22: 413-424.
11. Feng, Y., Cao, C. M., Vikram, M., Park, S., Kim, H. J., Hong, J. C., Cisneros-Zevallos, L., and Koiwa, H. (2011). A three-component gene expression system and its application for inducible flavonoid overproduction in transgenic Arabidopsis thaliana. PLoSONE 6: e17603.
12. Fitchette-Lainé, A. C., Gomord, V., Cabanes, M., Michalski, J. C., Saint Macary, M., Foucher, B., Cavelier, B., Hawes, C., Lerouge, P., and Faye, L. (1997). N-glycans harboring the Lewis a epitope are expressed at the surface of plant cells. Plant J. 12: 1411-1417.
13. Frank, J., Kaulfürst-Soboll, H., Rips, S., Koiwa, H., and von Schaewen, A. (2008). Comparative analyses of Arabidopsis complex glycan1 mutants and genetic interaction with staurosporin and temperature sensitive3a. Plant Physiol. 148: 1354-1367.
14. Guex, N., and Peitsch, M. C. (1997). SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
15. Häweker, H., Rips, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., Robatzek, S., and von Schaewen, A. (2010). Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285: 4629-4636.
16. Helenius, A., and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291: 2364-2369.
17. Hématy, K., Sado, P. E., Van Tuinen, A., Rochange, S., Desnos, T., Balzergue, S., Pelletier, S., Renou, J. P., and Höfte, H. (2007). A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17: 922-931.
18. Jefferson, R. (1987). Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387-405.
19. Johnson, K. D., and Chrispeels, M. J. (1987). Substrate specificities of N-acetylglucosaminyl-, fucosyl-, and xylosyltransferases that modify glycoproteins in the Golgi apparatus of bean cotyledons. Plant Physiol. 84: 1301-1308.
20. Jung, E. D., Lao, G., Irwin, D., Barr, B. K., Benjamin, A., andWilson, D. B. (1993). DNA sequences and expression in Streptomyces lividans of an exoglucanase gene and an endoglucanase gene from Thermomonospora fusca. Appl. Environ. Microbiol. 59: 3032-3043.
21. Kajiura, H., Koiwa, H., Nakazawa, Y., Okazawa, A., Kobayashi, A., Seki, T., and Fujiyama, K. (2010). Two Arabidopsis thaliana Golgi alpha-mannosidase I enzymes are responsible for plant N-glycan maturation. Glycobiology 20: 235-247.
22. Kang, J. S., et al. (2008). Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl. Acad. Sci. USA 105: 5933-5938.
23. Kaulfürst-Soboll, H., Rips, S., Koiwa, H., Kajiura, H., Fujiyama, K., and von Schaewen, A. (2011). Reduced immunogenicity of Arabidopsis hybrid glycosylation1 (hgl1) N-glycans due to altered accessibility of xylose and core fucose epitopes. J. Biol. Chem. 286: 22955-22964.
24. Kayser, V., Chennamsetty, N., Voynov, V., Forrer, K., Helk, B., and Trout, B. L. (2011). Glycosylation influences on the aggregation propensity of therapeutic monoclonal antibodies. Biotechnol. J. 6: 38-44.
25. Kelleher, D. J., Karaoglu, D., Mandon, E. C., and Gilmore, R. (2003). Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell 12: 101-111.
26. Khademi, S., Guarino, L. A., Watanabe, H., Tokuda, G., and Meyer, E. F. (2002). Structure of an endoglucanase from termite, Nasutitermes takasagoensis. Acta Crystallogr. D Biol. Crystallogr. 58: 653-659.
27. Koiwa, H., Sato, F., and Yamada, Y. (1994). Characterization of accumulation of tobacco PR-5 proteins by IEF-immunoblot analysis. Plant Cell Physiol. 35: 821-827.
28. Koiwa, H., Li, F., McCully, M. G., Mendoza, I., Koizumi, N., Manabe, Y., Nakagawa, Y., Zhu, J., Rus, A., Pardo, J. M., Bressan, R. A., and Hasegawa, P. M. (2003). The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 15: 2273-2284.
29. Lam, S. K., Cai, Y., Tse, Y. C., Wang, J., Law, A. H., Pimpl, P., Chan, H. Y., Xia, J., and Jiang, L. (2009). BFA-induced compartments from the Golgi apparatus and trans-Golgi network/early endosome are distinct in plant cells. Plant J. 60: 865-881.
30. Lane, D. R., et al. (2001). Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1, 4-beta-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol. 126: 278-288.
31. Laurière, M., Laurière, C., Chrispeels, M. J., Johnson, K. D., and Sturm, A. (1989). Characterization of a xylose-specific antiserum that reacts with the complex asparagine-linked glycans of extracellular and vacuolar glycoproteins. Plant Physiol. 90: 1182-1188.
32. Lehle, L., Strahl, S., and Tanner, W. (2006). Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. Engl. 45: 6802-6818.
33. Lei, L., Zhang, T., Strasser, R., Lee, C. M., Gonneau, M., Mach, L., Vernhettes, S., Kim, S. H., J Cosgrove, D., Li, S., and Gu, Y. (2014). The jiaoyao1 mutant is an allele of korrigan1 that abolishes endoglucanase activity and affects the organization of both cellulose microfibrils and microtubules in Arabidopsis. Plant Cell 26: 2601-2616.
34. Léonard, R., Costa, G., Darrambide, E., Lhernould, S., Fleurat-Lessard, P., Carlué, M., Gomord, V., Faye, L., and Maftah, A. (2002). The presence of Lewis a epitopes in Arabidopsis thaliana glycoconjugates depends on an active alpha4-fucosyltransferase gene. Glycobiology 12: 299-306.
35. Liebminger, E., Grass, J., Altmann, F., Mach, L., and Strasser, R. (2013). Characterizing the link between glycosylation state and enzymatic activity of the endo-β 1, 4-glucanase KORRIGAN1 from Arabidopsis thaliana. J. Biol. Chem. 288: 22270-22280.
36. Liebminger, E., Veit, C., Pabst, M., Batoux, M., Zipfel, C., Altmann, F., Mach, L., and Strasser, R. (2011). Beta-N-acetylhexosaminidases HEXO1 and HEXO3 are responsible for the formation of paucimannosidic N-glycans in Arabidopsis thaliana. J. Biol. Chem. 286: 10793-10802.
37. Liebminger, E., Hüttner, S., Vavra, U., Fischl, R., Schoberer, J., Grass, J., Blaukopf, C., Seifert, G. J., Altmann, F., Mach, L., and Strasser, R. (2009). Class I alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. Plant Cell 21: 3850-3867.
38. Maîtrejean, M., Wudick, M. M., Voelker, C., Prinsi, B., Mueller-Roeber, B., Czempinski, K., Pedrazzini, E., and Vitale, A. (2011). Assembly and sorting of the tonoplast potassium channel AtTPK1 and its turnover by internalization into the vacuole. Plant Physiol. 156: 1783-1796.
39. Master, E. R., Rudsander, U. J., Zhou, W., Henriksson, H., Divne, C., Denman, S., Wilson, D. B., and Teeri, T. T. (2004). Recombinant expression and enzymatic characterization of PttCel9A, a KOR homologue from Populus tremula x tremuloides. Biochemistry 43: 10080-10089.
40. Nebenführ, A., Gallagher, L. A., Dunahay, T. G., Frohlick, J. A., Mazurkiewicz, A. M., Meehl, J. B., and Staehelin, L. A. (1999). Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121: 1127-1142.
41. Ni, M., Cui, D., Einstein, J., Narasimhulu, S., Vergara, C. E., and Gelvin, S. B. (1995). Strength and tissue specificity of chimeric promoters derived from the octopine and mannopine synthase genes. Plant J. 7: 661-676.
42. Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H., and Höfte, H. (1998). A plasma membrane-bound putative endo-1, 4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17: 5563-5576.
43. Oliver, J. D., van der Wal, F. J., Bulleid, N. J., and High, S. (1997). Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 275: 86-88.
44. Pedrazzini, E., Komarova, N. Y., Rentsch, D., and Vitale, A. (2013). Traffic routes and signals for the tonoplast. Traffic 14: 622-628.
45. Peng, L., Kawagoe, Y., Hogan, P., and Delmer, D. (2002). Sitosterolbeta-glucoside as primer for cellulose synthesis in plants. Science 295: 147-150.
46. Rath, A., Glibowicka, M., Nadeau, V. G., Chen, G., and Deber, C. M. (2009). Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc. Natl. Acad. Sci. USA 106: 1760-1765.
47. Robert, S., Chary, S. N., Drakakaki, G., Li, S., Yang, Z., Raikhel, N. V., and Hicks, G. R. (2008). Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc. Natl. Acad. Sci. USA 105: 8464-8469.
48. Robert, S., Bichet, A., Grandjean, O., Kierzkowski, D., Satiat-Jeunemaître, B., Pelletier, S., Hauser, M. T., Höfte, H., and Vernhettes, S. (2005). An Arabidopsis endo-1, 4-beta-D-glucanase involved in cellulose synthesis undergoes regulated intracellular cycling. Plant Cell 17: 3378-3389.
49. Roudier, F., Fernandez, A. G., Fujita, M., Himmelspach, R., Borner, G. H., Schindelman, G., Song, S., Baskin, T. I., Dupree, P., Wasteneys, G. O., and Benfey, P. N. (2005). COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17: 1749-1763.
50. Rozwadowski, K., Yang, W., and Kagale, S. (2008). Homologous recombination-mediated cloning and manipulation of genomic DNA regions using Gateway and recombineering systems. BMC Biotechnol. 8: 88.
51. Ruiz-Canada, C., Kelleher, D. J., and Gilmore, R. (2009). Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms. Cell 136: 272-283.
52. Samson, F., Brunaud, V., Balzergue, S., Dubreucq, B., Lepiniec, L., Pelletier, G., Caboche, M., and Lecharny, A. (2002). FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res. 30: 94-97.
53. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003). SWISSMODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31: 3381-3385.
54. Silberstein, S., and Gilmore, R. (1996). Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase. FASEB J. 10: 849-858.
55. Skropeta, D. (2009). The effect of individual N-glycans on enzyme activity. Bioorg. Med. Chem. 17: 2645-2653.
56. Stefanowicz, K., Lannoo, N., Proost, P., and Van Damme, E. J. (2012). Arabidopsis F-box protein containing a Nictaba-related lectin domain interacts with N-acetyllactosamine structures. FEBS Open Bio 2: 151-158.
57. Strasser, R., Altmann, F., Mach, L., Glössl, J., and Steinkellner, H. (2004). Generation of Arabidopsis thaliana plants with complex N-glycans lacking beta1, 2-linked xylose and core alpha1, 3-linked fucose. FEBS Lett. 561: 132-136.
58. Strasser, R., Schoberer, J., Jin, C., Glössl, J., Mach, L., and Steinkellner, H. (2006). Molecular cloning and characterization of Arabidopsis thaliana Golgi alpha-mannosidase II, a key enzyme in the formation of complex N-glycans in plants. Plant J. 45: 789-803.
59. Strasser, R., Steinkellner, H., Borén, M., Altmann, F., Mach, L., Glössl, J., and Mucha, J. (1999). Molecular cloning of cDNA encoding N-acetylglucosaminyltransferase II from Arabidopsis thaliana. Glycoconj. J. 16: 787-791.
60. Strasser, R., Mucha, J., Mach, L., Altmann, F., Wilson, I. B., Glössl, J., and Steinkellner, H. (2000). Molecular cloning and functional expression of beta1, 2-xylosyltransferase cDNA from Arabidopsis thaliana. FEBS Lett. 472: 105-108.
61. Strasser, R., Bondili, J. S., Schoberer, J., Svoboda, B., Liebminger, E., Glössl, J., Altmann, F., Steinkellner, H., and Mach, L. (2007a). Enzymatic properties and subcellular localization of Arabidopsis beta-N-acetylhexosaminidases. Plant Physiol. 145: 5-16.
62. Strasser, R., Bondili, J. S., Vavra, U., Schoberer, J., Svoboda, B., Glössl, J., Léonard, R., Stadlmann, J., Altmann, F., Steinkellner, H., and Mach, L. (2007b). A unique beta1, 3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19: 2278-2292.
63. Szyjanowicz, P. M., McKinnon, I., Taylor, N. G., Gardiner, J., Jarvis, M. C., and Turner, S. R. (2004). The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J. 37: 730-740.
64. Takahashi, J., et al. (2009). KORRIGAN1 and its aspen homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant Cell Physiol. 50: 1099-1115.
65. Vain, T., Crowell, E. F., Timpano, H., Biot, E., Desprez, T., Mansoori, N., Trindade, L. M., Pagant, S., Robert, S., Höfte, H., Gonneau, M., and Vernhettes, S. (2014). The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol. 165: 1521-1532.
66. Varki, A. (2011). Evolutionary forces shaping the Golgi glycosylation machinery: why cell surface glycans are universal to living cells. Cold Spring Harb. Perspect. Biol. 3: 3.
67. Vembar, S. S., and Brodsky, J. L. (2008). One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9: 944-957.
68. von Schaewen, A., Frank, J., and Koiwa, H. (2008). Role of plant complex N-glycans. Plant Signal. Behav. 3: 871-873.
69. von Schaewen, A., Sturm, A., O'Neill, J., and Chrispeels, M. J. (1993). Isolation of a mutant Arabidopsis plant that lacks N-acetyl glucosaminyl transferase I and is unable to synthesize Golgi-modified complex N-linked glycans. Plant Physiol. 102: 1109-1118.
70. Voutilainen, S. P., Murray, P. G., Tuohy, M. G., and Koivula, A. (2010). Expression of Talaromyces emersonii cellobiohydrolase Cel7A in Saccharomyces cerevisiae and rational mutagenesis to improve its thermostability and activity. Protein Eng. Des. Sel. 23: 69-79.
71. Xu, S. L., Rahman, A., Baskin, T. I., and Kieber, J. J. (2008). Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell 20: 3065-3079.
72. Zhou, R., Benavente, L. M., Stepanova, A. N., and Alonso, J. M. (2011). A recombineering-based gene tagging system for Arabidopsis. Plant J. 66: 712-723.
73. Zuo, J., Niu, Q. W., Nishizawa, N., Wu, Y., Kost, B., and Chua, N. H. (2000). KORRIGAN, an Arabidopsis endo-1, 4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12: 1137-1152.