Glycosylphosphatidylinositol-anchored proteins are required for cell wall synthesis and morphogenesis in arabidopsis

Plant Cell

Volumn 17, Issue 4, 2005, Pages 1128-1140

  Stewart Gillmor, C ^a,b,c   Lukowitz, Wolfgang ^a,d   Brininstool, Ginger ^a   Sedbrook, John C ^a,e   Hamann, Thorsten ^a   Poindexter, Patricia ^a   Somerville, Chris ^a,b  

^a GEOPHYSICAL LABORATORY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^e ILLINOIS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CELLS; DEPOSITION; GENES; SEED;

CELL WALL; XYLOGLUCANS;

PROTEINS;

CELLS; DEPOSITION; GENES; PROTEINS; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 31344457271     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.031815     Document Type: Article

References (52)

1. Acosta-Garcia, G., and Vielle-Calzada, J.-P. (2004). A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16, 2614-2628.
2. Beeckman, T., Przemeck, G.H.K., Stamatiou, G., Lau, R., Terryn, N., De Rycke, R., Inzé, D., and Berleth, T. (2002). Genetic complexity of cellulose synthase A gene function in Arabidopsis embryogenesis. Plant Physiol. 130, 1883-1893.
3. Bonifacio, J.S., and Lippincott-Schwartz, J. (1991). Degradation of proteins within the endoplasmic reticulum. Curr. Opin. Cell Biol. 3, 592-600.
4. Borner, G.H., Lilley, K.S., Stephens, T.J., and Dupree, P. (2003). Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiol. 132, 568-577.
5. Borner, G.H., Sherrier, D.J., Stevens, T.J., Arkin, I.T., and Dupree, P. (2002). Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A genomic analysis. Plant Physiol. 129, 486-499.
6. 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., and Dupree, P. (2005). Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 137, 104-116.
7. Burn, J.E., Hurley, U.A., Birch, R.J., Arioli, T., Cork, A., and Williamson, R.E. (2002). The cellulose deficient Arabidopsis mutant rsw3 is defective in a gene encoding a putative glucosidase II, an enzyme processing N-glycans during ER quality control. Plant J. 32, 949-960.
8. Caro, L.H.P., Tettelin, H., Vossen, J.H., Ram, A.F.J., Van Den Ende, H., and Klis, P.M. (1997). In silico identification of glycosyl- phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13, 1477-1489.
9. Delmer, D. (1987). Cellulose biosynthesis. Annu. Rev. Plant Physiol. 38, 259-290.
10. Ding, L., and Zhu, J.-K. (1997). A role for arabinogalactan-proteins in root epidermal cell expansion. Planta 203, 289-294.
11. Eisenhaber, B., Wildpaner, M., Schultz, C.J., Borner, G.H., Dupree, P., and Eisenhaber, F. (2003). Glycosylphosphatidylinositol lipid anchoring of plant proteins. Sensitive prediction from sequence-and genome-wide studies for Arabidopsis and rice. Plant Physiol. 133, 1691-1701.
12. Encina, C.L., Constantin, M., and Botella, J. (2001). An easy and reliable method for establishment and maintenance of leaf and root cell cultures of Arabidopsis thaliana. Plant Mol. Biol. Report. 19, 245-248.
13. Ferguson, M.A.J. (1999). The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J. Cell Sci. 112, 2799-2809.
14. Field, M.C., Moran, P., Li, W., Keller, G.-A., and Caras, I.W. (1994). Retention and degradation of proteins containing an uncleaved glycosylphosphatidylinositol signal. J. Biol. Chem. 269, 10830-10837.
15. Gao, M., and Showalter, A.M. (1999). Yariv reagent treatment incudes programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. Plant J. 19, 321-331.
16. Gaspar, Y., Johnson, K.L., McKenna, J.A., Bacic, A., and Schulz, C.J. (2001). The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol. Biol. 47, 161-176.
17. Gibeaut, D.M., and Carpita, N.C. (1994). Biosynthesis of plant cell wall polysaccharides. FASEB J. 8, 904-915.
18. Gillmor, C.S., Poindexter, P., Lorieau, J., Palcic, M.M., and Somerville, C. (2002). α-Glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J. Cell Biol. 156, 1003-1013.
19. Guan, Y., and Nothnagel, E.A. (2004). Binding of arabinogalactan proteins by Yariv phenylglycoside triggers wound-like responses in Arabidopsis cell cultures. Plant Physiol. 135, 1346-1366.
20. Jürgens, G., and Mayer, U. (1994). Arabidopsis. In Embryos: Color Atlas of Development, J.B.L Bard, ed (London: Wolfe), pp. 7-21.
21. Kapteyn, J.C., Van Den Ende, H., and Klis, F.M. (1999). The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim. Biophys. Acta 1426, 373-383.
22. Kieliszewski, M.J., and Lamport, D.T.A. (1994). Extensin: Repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 5, 157-172.
23. Kinoshita, T., and Inoue, N. (2000). Dissecting and manipulating the pathway for glycosylphosphatidylinositol-anchor biosynthesis. Curr. Opin. Chem. Biol. 4, 632-638.
24. Knox, J.P., Linstead, P.J., King, J., Cooper, C., and Roberts, K. (1990). Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181, 512-521.
25. 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.
26. Leidich, S.D., Drapp, D.A., and Orlean, P. (1994). A conditionally lethal yeast mutant blocked at the first step in glycosyl phosphatidylinositol anchor synthesis. J. Biol. Chem. 269, 10193-10196.
27. Li, Y., Qian, Q., Zhou, Y., Yan, M., Sun, L., Zhang, M., Fu, Z., Wang, Y., Han, B., Pang, X., Chen, M., and Li, J. (2003). BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15, 2020-2031.
28. Lukowitz, W., Gillmor, C.S., and Scheible, W.-R. (2000). Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123, 795-805.
29. Lukowitz, W., Nickle, T.C., Meinke, D.W., Last, R.L., Conklin, P.L., and Somerville, C.R. (2001). Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proc. Natl. Acad. Sci. USA 98, 2262-2267.
30. Maeda, Y., Watanabe, R., Harris, C.L., Hong, Y., Ohishi, K., Kinoshita, K., and Kinoshita, T. (2001). PIG-M transfers the first mannose to glycosylphosphatidylinositol on the lumenal side of the ER. EMBO J. 20, 250-261.
31. Maewska-Sawka, A., and Nothnagel, E.A. (2000). The multiple roles of arabinogalactan proteins in plant development. Plant Physiol. 122, 3-9.
32. Nickle, T.C., and Meinke, D.W. (1998). A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant J. 15, 321-332.
33. Peskan, T., Westermann, M., and Oelmüller, R. (2000). Identification of low-density Triton X-100-insoluble plasma membrane microdomains in higher plants. Eur. J. Biochem. 267, 6989-6995.
34. Puhlmann, J., Bucheli, E., Swain, M.J., Dunning, N., Albersheim, P., Darvill, A.G., and Hahn, M.G. (1994). Generation of monoclonal antibodies against plant cell-wall polysaccharides. I. Characterization of a monclonal antibody to a terminal α-(1->2)-linked fucosyl-containing epitope. Plant Physiol. 104, 699-710.
35. Rhee, S.Y., and Somerville, C.R. (1998). Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J. 15, 79-88.
36. Richmond, T., and Somerville, C.R. (2001). Integrative approaches to determining CsI function. Plant Mol. Biol. 47, 131-143.
37. Roudier, F., Schindelman, G., DeSalle, R., and Benfey, P.N. (2002). The COBRA family of putative GPI-anchored proteins in Arabidopsis: A new fellowship in expansion. Plant Physiol. 130, 538-548.
38. Roy, S., Jauh, G.Y., Hepler, P.K., and Lord, E.M. (1998). Effects of Yariv phenylglycoside on cell wall assembly in the lily pollen tube. Planta 204, 450-458.
39. Schindelman, G., Morikami, A., Jung, J., Baskin, T.I., Carpita, N.C., Derbyshire, P., McCann, M.C., and Benfey, P.N. (2001). COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev. 15, 1115-1127.
40. Schultz, C.J., Johnson, K.L., Currie, G., and Bacic, A. (2000). The classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12, 1751-1767.
41. Sedbrook, J.C., Carroll, K.L., Hung, K.F., Masson, P.H., and Somerville, C.R. (2002). The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositol-anchored glycoprotein involved in directional root growth. Plant Cell 14, 1635-1648.
42. Seifert, G.J., Barber, C., Wells, B., Dolan, L., and Roberts, K. (2002). Galactose biosynthesis in Arabidopsis: Genetic evidence for substrate channeling from UDP-D-Galactose into cell wall polymers. Curr. Biol. 12, 1840-1845.
43. Selleck, S.B. (2000). Proteoglycans and pattern formation. Sugar biochemistry meets developmental genetics. Trends Genet. 16, 206-212.
44. Shi, H., Kim, Y.-S., Guo, Y., Stevenson, B., and Zhu, J.-K. (2003). The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15, 19-32.
45. Stone, B.A., Evans, N.A., Bonig, I., and Clarke, A.E. (1984). The application of Sirofluor, a chemically defined fluorochrome from analine blue for the histochemical detection of callose. Protoplasma 122, 191-195.
46. Sun, W., Kieliszewski, M.J., and Showalter, A.M. (2004a). Overexpression of tomato LeAGP-1 arabinogalactan-protein promotes lateral branching and hampers reproductive development. Plant J. 40, 870-881.
47. Sun, W., Zhao, Z.D., Hare, M.C., Kieliszewski, M.J., and Showalter, A.M. (2004b). Tomato LeAGP-1 is a plasma membrane-bound, glycosylphosphatidylinositol-anhored arabinogalactan-protein. Physiol. Plant. 120, 319-327.
48. Torres-Ruíz, R.A., and Jürgens, G. (1994). Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120, 2967-2978.
49. Vogel, J.P., Raab, T.K., Schiff, C., and Somerville, S.C. (2002). PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14, 2095-2106.
50. Willats, W.G.T., and Knox, J.P. (1996). A role for arabinogalactan- proteins in plant cell expansion: Evidence from studies on the interaction of B-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J. 9, 919-925.
51. Williamson, R.E., Burn, J.E., and Hocart, C.H. (2002). Towards the mechanism of cellulose synthesis. Trends Plant Sci. 7, 461-467.
52. Youl, J.J., Bacic, A., and Oxley, D. (1998). Arabinogalactan-proteins from Nicotiana alata and Pyrus communis contain glycosylphosphatidylinositol membrane anchors. Proc. Natl. Acad. Sci. USA 95, 7921-7926.