Flying saucer1 is a transmembrane RING E3 ubiquitin ligase that regulates the degree of pectin methylesterification in Arabidopsis seed mucilage

Plant Cell

Volumn 25, Issue 3, 2013, Pages 944-959

  Voiniciuc, Cǎtǎlin ^a   Dean, Gillian H ^a   Griffiths, Jonathan S ^a   Kirchsteiger, Kerstin ^b   Hwang, Yeen Ting ^a,c   Gillett, Alan ^a,d   Dow, Graham ^a,e   Western, Tamara L ^a,f   Estelle, Mark ^b   Haughn, George W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^c LETHBRIDGE RESEARCH CENTRE   (Canada)

^d EMD Serono Canada Inc   (Canada)

^e STANFORD UNIVERSITY   (United States)

^f MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84876755289     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.107888     Document Type: Article

References (105)

1. Abramoff, M.D., Magalhaes, P.J., and Ram, S.J. (2004). Image Processing with ImageJ. Biophotonics Int. 11: 36-42.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
3. Anderson, C.T., Carroll, A., Akhmetova, L., and Somerville, C. (2010). Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol. 152: 787-796.
4. Arsovski, A.A., Popma, T.M., Haughn, G.W., Carpita, N.C., McCann, M.C., and Western, T.L. (2009). AtBXL1 encodes a bi- functional b-D-xylosidase/a-L-arabinofuranosidase required for pectic arabinan modification in Arabidopsis mucilage secretory cells. Plant Physiol. 150: 1219-1234.
5. Atmodjo, M.A., Sakuragi, Y., Zhu, X., Burrell, A.J., Mohanty, S.S., Atwood, J.A. III., Orlando, R., Scheller, H.V., and Mohnen, D. (2011). Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proc. Natl. Acad. Sci. USA 108: 20225-20230.
6. Barberon, M., Zelazny, E., Robert, S., Conéjéro, G., Curie, C., Friml, J., and Vert, G. (2011). Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl. Acad. Sci. USA 108: E450-E458.
7. Bhargava, A., Ahad, A., Wang, S., Mansfield, S.D., Haughn, G.W., Douglas, C.J., and Ellis, B.E. (January 18, 2013). The interacting MYB75 and KNAT7 transcription factors modulate secondary cell wall deposition both in stems and seed coat in Arabidopsis. Planta, in press.
8. Batoko, H., Zheng, H.Q., Hawes, C., and Moore, I. (2000). A rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants. Plant Cell 12: 2201-2218.
9. Beeckman, T., De Rycke, R., Viane, R., and Inzé, D. (2000). Histological study of seed coat development in Arabidopsis thaliana. J. Plant Res. V113: 139-148.
10. Brady, S.M., Orlando, D.A., Lee, J.-Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U., and Benfey, P.N. (2007). A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806.
11. Brandizzi, F., Fricker, M., and Hawes, C. (2002). A greener world: The revolution in plant bioimaging. Nat. Rev. Mol. Cell Biol. 3: 520-530.
12. Caffall, K.H., Pattathil, S., Phillips, S.E., Hahn, M.G., and Mohnen, D. (2009). Arabidopsis thaliana T-DNA mutants implicate GAUT genes in the biosynthesis of pectin and xylan in cell walls and seed testa. Mol. Plant 2: 1000-1014.
13. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
14. Dean, G.H., Zheng, H., Tewari, J., Huang, J., Young, D.S., Hwang, Y.T., Western, T.L., Carpita, N.C., McCann, M.C., Mansfield, S.D., and Haughn, G.W. (2007). The Arabidopsis MUM2 gene encodes a bgalactosidase required for the production of seed coat mucilage with correct hydration properties. Plant Cell 19: 4007-4021.
15. DeBono, A.G. (2012). The Role and Behavior of Arabidopsis thaliana Lipid Transfer Proteins during Cuticular Wax Deposition. PhD dissertation (Vancouver, Canada: University of British Columbia).
16. Derbyshire, P., McCann, M.C., and Roberts, K. (2007). Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biol. 7: 31.
17. Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y.D., and Schumacher, K. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730.
18. Dowil, R.T., Lu, X., Saracco, S.A., Vierstra, R.D., and Downes, B.P. (2011). Arabidopsis membrane-anchored ubiquitin-fold (MUB) proteins localize a specific subset of ubiquitin-conjugating (E2) enzymes to the plasma membrane. J. Biol. Chem. 286: 14913-14921.
19. Glickman, M.H., and Ciechanover, A. (2002). The ubiquitin-protea-some proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82: 373-428.
20. Goldberg, R., Morvan, C., Jauneau, A., and Jarvis, M.C. (1996). Methyl-esterification, de-esterification and gelation of pectins in the primary cell wall. In Pectins and Pectinases, Visser J., Voragen A.G.J., eds (Amsterdam: Elsevier Science BV), pp. 151-172.
21. Goodstein, D.M., Shu, S., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D.S. (2012). Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 40 (Database issue): D1178-D1186.
22. Hamilton, J.M.U., Simpson, D.J., Hyman, S.C., Ndimba, B.K., and Slabas, A.R. (2003). Ara12 subtilisin-like protease from Arabidopsis thaliana: Purification, substrate specificity and tissue localization. Biochem. J. 370: 57-67.
23. Hardtke, C.S., Okamoto, H., Stoop-Myer, C., and Deng, X.W. (2002). Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J. 30: 385-394.
24. Harholt, J., Suttangkakul, A., and Vibe Scheller, H. (2010). Biosynthesis of pectin. Plant Physiol. 153: 384-395.
25. Harpaz-Saad, S., McFarlane, H.E., Xu, S., Divi, U.K., Forward, B., Western, T.L., and Kieber, J.J. (2011). Cellulose synthesis via the FEI2 RLK/SOS5 pathway and cellulose synthase 5 is required for the structure of seed coat mucilage in Arabidopsis. Plant J. 68: 941-953.
26. Haughn, G.W., and Somerville, C. (1986). Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204:430-434.
27. Haughn, G.W., and Western, T.L. (2012). Arabidopsis seed coat mucilage is a specialized cell wall that can be used as a model for genetic analysis of plant cell wall structure and function. Front. Plant Sci. 3: 64.
28. Held, M.A., Be, E., Zemelis, S., Withers, S., Wilkerson, C., and Brandizzi, F. (2011). CGR3: A Golgi-localized protein influencing homogalacturonan methylesterification. Mol. Plant 4: 832-844.
29. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and Mullineaux, P.M. (2000). pGreen: A versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42: 819-832.
30. Hicke, L., and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19: 141-172.
31. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., Widmayer, P., Gruissem, W., and Zimmermann, P. (2008). Genevestigator v3: A reference expression database for the metaanalysis of transcriptomes. Adv. Bioinforma. 2008: 420747.
32. Huang, X., and Miller, W. (1991). A time-efficient linear-space local similarity algorithm. Adv. Appl. Math. 12: 337-357.
33. Jander, G., Norris, S.R., Rounsley, S.D., Bush, D.F., Levin, I.M., and Last, R.L. (2002). Arabidopsis map-based cloning in the post-genome era. Plant Physiol. 129: 440-450.
34. Jarvis, M.C. (1984). Structure and properties of pectin gels in plant cell walls. Plant Cell Environ. 7: 153-164.
35. Jolie, R.P., Duvetter, T., Van Loey, A.M., and Hendrickx, M.E. (2010). Pectin methylesterase and its proteinaceous inhibitor: A review. Carbohydr. Res. 345: 2583-2595.
36. Kasajima, I., Ide, Y., Ohkama-Ohtsu, N., Hayashi, H., Yoneyama, T., and Fujiwara, T. (2004). A protocol for rapid DNA extraction from Arabidopsis thaliana for PCR analysis. Plant Mol. Biol. Rep. 22: 49-52.
37. Klavons, J.A., and Bennett, R.D. (1986). Determination of methanol using alcohol oxidase and its application to methyl ester content of pectins. J. Agric. Food Chem. 34: 597-599.
38. Knox, J.P. (1997). The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int. Rev. Cytol. 171: 79-120.
39. 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.
40. Krupková, E., Immerzeel, P., Pauly, M., and Schmülling, T. (2007). The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J. 50: 735-750.
41. Lamesch, P., et al. (2012). The Arabidopsis Information Resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Res. 40 (Database issue): D1202-D1210.
42. Larkin, M.A., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
43. Le, B.H., et al. (2010). Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc. Natl. Acad. Sci. USA 107: 8063-8070.
44. Lee, M.H., Min, M.K., Lee, Y.J., Jin, J.B., Shin, D.H., Kim, D.H., Lee, K.-H., and Hwang, I. (2002). ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol. 129: 1507-1520.
45. Liners, F., Letesson, J.J., Didembourg, C., and Van Cutsem, P. (1989). Monoclonal antibodies against pectin: Recognition of a conformation induced by calcium. Plant Physiol. 91: 1419-1424.
46. Lionetti, V., Raiola, A., Camardella, L., Giovane, A., Obel, N., Pauly, M., Favaron, F., Cervone, F., and Bellincampi, D. (2007). Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol. 143: 1871-1880.
47. Lord, E.M., and Mollet, J.-C. (2002). Plant cell adhesion: A bioassay facilitates discovery of the first pectin biosynthetic gene. Proc. Natl. Acad. Sci. USA 99: 15843-15845.
48. Macquet, A., Ralet, M.-C., Kronenberger, J., Marion-Poll, A., and North, H.M. (2007a). In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant Cell Physiol. 48: 984-999.
49. MacGurn, J.A., Hsu, P.C., and Emr, S.D. (2012). Ubiquitin and membrane protein turnover: From cradle to grave. Annu. Rev. Biochem. 81: 231-259.
50. Macquet, A., Ralet, M.-C., Loudet, O., Kronenberger, J., Mouille, G., Marion-Poll, A., and North, H.M. (2007b). A naturally occurring mutation in an Arabidopsis accession affects a beta-D-galactosidase that increases the hydrophilic potential of rhamnogalacturonan I in seed mucilage. Plant Cell 19: 3990-4006.
51. Mareck, A., Lamour, R., Schaumann, A., Chan, P., Driouich, A., Pelloux, J., and Lerouge, P. (2012). Analysis of LuPME3, a pectin methylesterase from Linum usitatissimum, revealed a variability in PME proteolytic maturation. Plant Signal. Behav. 7: 59-61.
52. Mendu, V., Griffiths, J.S., Persson, S., Stork, J., Downie, A.B., Voiniciuc, C., Haughn, G.W., and DeBolt, S. (2011). Subfunctionalization of cellulose synthases in seed coat epidermal cells mediates secondary radial wall synthesis and mucilage attachment. Plant Physiol. 157: 441-453.
53. Miao, Y., Li, H.-Y., Shen, J., Wang, J., and Jiang, L. (2011). QUA- SIMODO 3 (QUA3) is a putative homogalacturonan methyl-transferase regulating cell wall biosynthesis in Arabidopsis suspension-cultured cells. J. Exp. Bot. 62: 5063-5078.
54. Micheli, F. (2001). Pectin methylesterases: Cell wall enzymes with important roles in plant physiology. Trends Plant Sci. 6: 414-419.
55. Mohnen, D. (2008). Pectin structure and biosynthesis. Curr. Opin. Plant Biol. 11: 266-277.
56. Mouille, G., Ralet, M.-C., Cavelier, C., Eland, C., Effroy, D., Hématy, K., McCartney, L., Truong, H.N., Gaudon, V., Thibault, J.-F., Marchant, A., and Höfte, H. (2007). Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J. 50: 605-614.
57. Moustacas, A.M., Nari, J., Borel, M., Noat, G., and Ricard, J. (1991). Pectin methylesterase, metal ions and plant cell-wall extension. The role of metal ions in plant cell-wall extension. Biochem. J. 279: 351-354.
58. Müller, J., Mettbach, U., Menzel, D., and Samaj, J. (2007). Molecular dissection of endosomal compartments in plants. Plant Physiol. 145: 293-304.
59. Mutwil, M., Debolt, S., and Persson, S. (2008). Cellulose synthesis: A complex complex. Curr. Opin. Plant Biol. 11: 252-257.
60. Obayashi, T., Nishida, K., Kasahara, K., and Kinoshita, K. (2011). ATTED-II updates: Condition-specific gene coexpression to extend coexpression analyses and applications to a broad range of flowering plants. Plant Cell Physiol. 52: 213-219.
61. Oka, T., Nemoto, T., and Jigami, Y. (2007). Functional analysis of Arabidopsis thaliana RHM2/MUM4, a multidomain protein involved in UDP-D-glucose to UDP-L-rhamnose conversion. J. Biol. Chem. 282: 5389-5403.
62. Ostlund, G., Schmitt, T., Forslund, K., Köstler, T., Messina, D.N., Roopra, S., Frings, O., and Sonnhammer, E.L.L. (2010). In-Paranoid 7: New algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res. 38 (Database issue): D196-D203.
63. Pattathil, S., et al. (2010). A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol. 153: 514-525.
64. Pelloux, J., Rustérucci, C., and Mellerowicz, E.J. (2007). New insights into pectin methylesterase structure and function. Trends Plant Sci. 12: 267-277.
65. Penfield, S., Meissner, R.C., Shoue, D.A., Carpita, N.C., and Bevan, M.W. (2001). MYB61 is required for mucilage deposition and extrusion in the Arabidopsis seed coat. Plant Cell 13: 2777-2791.
66. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011). SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786.
67. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., and Lopez, R. (2005). InterProScan: protein domains identifier. Nucleic Acids Res. 33 (Web Server issue): W116-W120.
68. Rautengarten, C., Usadel, B., Neumetzler, L., Hartmann, J., Büssis, D., and Altmann, T. (2008). A subtilisin-like serine protease essential for mucilage release from Arabidopsis seed coats. Plant J. 54: 466-480.
69. Reggiori, F., and Pelham, H.R.B. (2002). A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat. Cell Biol. 4: 117-123.
70. Rensing, K.H., Samuels, A.L., and Savidge, R.A. (2002). Ultra-structure of vascular cambial cell cytokinesis in pine seedlings preserved by cryofixation and substitution. Protoplasma 220: 39-49.
71. Robinson, D.G., Langhans, M., Saint-Jore-Dupas, C., and Hawes, C. (2008). BFA effects are tissue and not just plant specific. Trends Plant Sci. 13: 405-408.
72. Romano, J.M., et al. (2012). AtMYB61, an R2R3-MYB transcription factor, functions as a pleiotropic regulator via a small gene network. New Phytol. 195: 774-786.
73. Saint-Jore-Dupas, C., Gomord, V., and Paris, N. (2004). Protein localization in the plant Golgi apparatus and the trans-Golgi network. Cell. Mol. Life Sci. 61: 159-171.
74. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501-506.
75. Schnell, J.D., and Hicke, L. (2003). Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J. Biol. Chem. 278: 35857-35860.
76. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., Frommer, W.B., Flügge, U.-I., and Kunze, R. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131: 16-26.
77. Sigrist, C.J.A., Cerutti, L., de Castro, E., Langendijk-Genevaux, P.S., Bulliard, V., Bairoch, A., and Hulo, N. (2010). PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 38 (Database issue): D161-D166.
78. Sriamornsak, S. (2003). Chemistry of pectin and its pharmaceutical uses: A review. Silpakorn University International Journal. 3: 206-228.
79. Sterling, C. (1970). Crystal-structure of ruthenium red and stereochemistry of its pectic stain. Am. J. Bot. 57: 172-175.
80. Sterling, J.D., Atmodjo, M.A., Inwood, S.E., Kumar Kolli, V.S., Quigley, H.F., Hahn, M.G., and Mohnen, D. (2006). Functional identification of an Arabidopsis pectin biosynthetic homogalactur-onan galacturonosyltransferase. Proc. Natl. Acad. Sci. USA 103: 5236-5241.
81. Saez-Aguayo, S., Ralet, M.C., Berger, A., Botran, L., Ropartz, D., Marion-Poll, A., and North, H.M. (2013). PECTIN METHYL-ESTERASE INHIBITOR6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. Plant Cell 25: 308-323.
82. Stone, S.L., Hauksdóttir, H., Troy, A., Herschleb, J., Kraft, E., and Callis, J. (2005). Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137: 13-30.
83. Stork, J., Harris, D., Griffiths, J., Williams, B., Beisson, F., Li-Beisson, Y., Mendu, V., Haughn, G., and Debolt, S. (2010). CELLULOSE SYNTHASE9 serves a nonredundant role in secondary cell wall synthesis in Arabidopsis epidermal testa cells. Plant Physiol. 153: 580-589.
84. Sullivan, S., Ralet, M.-C., Berger, A., Diatloff, E., Bischoff, V., Gonneau, M., Marion-Poll, A., and North, H.M. (2011). CESA5 is required for the synthesis of cellulose with a role in structuring the adherent mucilage of Arabidopsis seeds. Plant Physiol. 156: 1725-1739.
85. Usadel, B., Kuschinsky, A.M., Rosso, M.G., Eckermann, N., and Pauly, M. (2004). RHM2 is involved in mucilage pectin synthesis and is required for the development of the seed coat in Arabidopsis. Plant Physiol. 134: 286-295.
86. Van Bel, M., Proost, S., Wischnitzki, E., Movahedi, S., Scheerlinck, C., Van de Peer, Y., and Vandepoele, K. (2012). Dissecting plant genomes with the PLAZA comparative genomics platform. Plant Physiol. 158: 590-600.
87. Vandenbosch, K.A., Bradley, D.J., Knox, J.P., Perotto, S., Butcher, G.W., and Brewin, N.J. (1989). Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J. 8: 335-341.
88. van den Hoogen, B.M., van Weeren, P.R., Lopes-Cardozo, M., van Golde, L.M.G., Barneveld, A., and van de Lest, C.H.A. (1998). A microtiter plate assay for the determination of uronic acids. Anal. Biochem. 257: 107-111.
89. Verollet, R. (2008). A major step towards efficient sample preparation with bead-beating. Biotechniques 44: 832-833.
90. Viotti, C., et al. (2010). Endocytic and secretory traffic in Arabidopsis merge in the trans-Golgi network/early endosome, an independent and highly dynamic organelle. Plant Cell 22: 1344-1357.
91. Wang, J., Cai, Y., Miao, Y., Lam, S.K., and Jiang, L. (2009). Wortmannin induces homotypic fusion of plant prevacuolar compartments. J. Exp. Bot. 60: 3075-3083.
92. Western, T.L., Burn, J., Tan, W.L., Skinner, D.J., Martin-McCaffrey, L., Moffatt, B.A., and Haughn, G.W. (2001). Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol. 127: 998-1011.
93. Western, T.L., Skinner, D.J., and Haughn, G.W. (2000). Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol. 122: 345-356.
94. Western, T.L., Young, D.S., Dean, G.H., Tan, W.L., Samuels, A.L., and Haughn, G.W. (2004). MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, andGLABRA2 in the Arabidopsis seed coat. Plant Physiol. 134: 296-306.
95. Windsor, J.B., Symonds, V.V., Mendenhall, J., and Lloyd, A.M. (2000). Arabidopsis seed coat development: Morphological differentiation of the outer integument. Plant J. 22: 483-493.
96. Willats, W.G., McCartney, L., Mackie, W., and Knox, J.P. (2001a). Pectin: Cell biology and prospects for functional analysis. Plant Mol. Biol. 47: 9-27.
97. Willats, W.G.T., McCartney, L., and Knox, J.P. (2001b). In-situ analysis of pectic polysaccharides in seed mucilage and at the root surface of Arabidopsis thaliana. Planta 213: 37-44.
98. Willats, W.G.T., Orfila, C., Limberg, G., Buchholt, H.C., van Alebeek, G.-J.W.M., Voragen, A.G.J., Marcus, S.E., Christensen, T.M.I.E., Mikkelsen, J.D., Murray, B.S., and Knox, J.P. (2001c). Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J. Biol. Chem. 276: 19404-19413.
99. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J. (2007). An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718.
100. Wolf, S., Mouille, G., and Pelloux, J. (2009a). Homogalacturonan methyl-esterification and plant development. Mol. Plant 2: 851-860.
101. Wolf, S., Rausch, T., and Greiner, S. (2009b). The N-terminal pro region mediates retention of unprocessed type-I PME in the Golgi apparatus. Plant J. 58: 361-375.
102. Xu, C., Zhao, L., Pan, X., and Samaj, J. (2011). Developmental localization and methylesterification of pectin epitopes during somatic embryogenesis of banana (Musa spp. AAA). PLoS ONE 6: e22992.
103. Young, R.E., McFarlane, H.E., Hahn, M.G., Western, T.L., Haughn, G.W., and Samuels, A.L. (2008). Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell 20: 1623-1638.
104. Zhang, G.F., and Staehelin, L.A. (1992). Functional compartmentation of the Golgi apparatus of plant cells: Immunocytochemical analysis of high-pressure frozen and freeze-substituted sycamore maple suspension culture cells. Plant Physiol. 99: 1070-1083.
105. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136: 2621-2632.