Metabolic click-labeling with a fucose analog reveals pectin delivery, architecture, and dynamics in Arabidopsis cell walls

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 4, 2012, Pages 1329-1334

  Anderson, Charles T ^a,c   Wallace, Ian S ^a,b   Somerville, Chris R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Fluorescence; Secretion; Small molecule

Indexed keywords

FUCOSE; FUCOSE ALKYNE; PECTIC RHAMNOGALACTURONAN I; PECTIN; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; CELL MATURATION; CELL METABOLISM; CHEMICAL ANALYSIS; CLICK CHEMISTRY; CYTOARCHITECTURE; DYNAMICS; EPIDERMIS CELL; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SEEDLING;

ALKYNES; ARABIDOPSIS; CELL WALL; CLICK CHEMISTRY; EPIDERMIS; FUCOSE; HYDRAZINES; MICROSCOPY, FLUORESCENCE; PECTINS; PLANT ROOTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84856389100     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120429109     Document Type: Article

References (47)

1. Somerville C, et al. (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206-2211. (Pubitemid 40024448)
2. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850-861.
3. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22: 53-78.
4. Reiter WD, Chapple C, Somerville CR (1997) Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J 12:335-345. (Pubitemid 27389622)
5. Brown DM, et al. (2007) Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J 52:1154-1168. (Pubitemid 350231158)
6. Lerouxel O, et al. (2002) Rapid structural phenotyping of plant cell wall mutants by enzymatic oligosaccharide fingerprinting. Plant Physiol 130:1754-1763. (Pubitemid 36035173)
7. Barton CJ, et al. (2006) Enzymatic fingerprinting of Arabidopsis pectic polysaccharides using polysaccharide analysis by carbohydrate gel electrophoresis (PACE). Planta 224: 163-174. (Pubitemid 43800711)
8. Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR (2006) Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Natl Acad Sci USA 103:11417-11422. (Pubitemid 44156532)
9. Lynch MA, Staehelin LA (1992) Domain-specific and cell type-specific localization of two types of cell wall matrix polysaccharides in the clover root tip. J Cell Biol 118:467-479.
10. Moore PJ, Swords KM, Lynch MA, Staehelin LA (1991) Spatial organization of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants. J Cell Biol 112:589-602. (Pubitemid 121000373)
11. Schmidt M, et al. (2010) Raman imaging of cell wall polymers in Arabidopsis thaliana. Biochem Biophys Res Commun 395:521-523.
12. Pattathil S, et al. (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153:514-525.
13. Lee KJ, Marcus SE, Knox JP (2011) Cell wall biology: Perspectives from cell wall imaging. Mol Plant 4:212-219.
14. Marcus SE, et al. (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60.
15. Chesson A, Gardner PT, Wood TJ (1997) Cell wall porosity and available surface area of wheat straw and wheat grain fractions. J Sci Food Agric 75:289-295. (Pubitemid 27491066)
16. Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152: 787-796.
17. Vissenberg K, Fry SC, Pauly M, Höfte H, Verbelen JP (2005) XTH acts at the microfibrilmatrix interface during cell elongation. J Exp Bot 56:673-683. (Pubitemid 40295154)
18. Laughlin ST, Bertozzi CR (2009) Imaging the glycome. Proc Natl Acad Sci USA 106: 12-17.
19. Hsu TL, et al. (2007) Alkynyl sugar analogs for the labeling and visualization of glycoconjugates in cells. Proc Natl Acad Sci USA 104:2614-2619.
20. McNeil M, Darvill AG, Fry SC, Albersheim P (1984) Structure and function of the primary cell walls of plants. Annu Rev Biochem 53:625-663.
21. Wu Y, et al. (2010) Functional identification of two nonredundant Arabidopsis α(1,2) fucosyltransferases specific to arabinogalactan proteins. J Biol Chem 285:13638-13645.
22. Strasser R, Altmann F, Mach L, Glössl J, Steinkellner H (2004) Generation of Arabidopsis thaliana plants with complex N-glycans lacking α1,2-linked xylose and core α1,3-linked fucose. FEBS Lett 561:132-136. (Pubitemid 38317309)
23. Bonin CP, Potter I, Vanzin GF, Reiter WD (1997) The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proc Natl Acad Sci USA 94: 2085-2090.
24. Kotake T, et al. (2008) A bifunctional enzyme with L-fucokinase and GDP-L-fucose pyrophosphorylase activities salvages free L-fucose in Arabidopsis. J Biol Chem 283: 8125-8135.
25. Nakamura A, Furuta H, Maeda H, Nagamatsu Y, Yoshimoto A (2001) Analysis of structural components and molecular construction of soybean soluble polysaccharides by stepwise enzymatic degradation. Biosci Biotechnol Biochem 65:2249-2258. (Pubitemid 33617197)
26. Glushka JN, et al. (2003) Primary structure of the 2-O-methyl-α-L- fucose-containing side chain of the pectic polysaccharide, rhamnogalacturonan II. Carbohydr Res 338:341-352. (Pubitemid 36135898)
27. Fry SC (1988) The Growing Plant Cell Wall: Chemical and Metabolic Analysis (Longman Scientific and Technical; J. Wiley, Burnt Mill, Harlow, Essex, England; New York) p xviii.
28. Ishii T, Matsunaga T, Hayashi N (2001) Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiol 126:1698-1705. (Pubitemid 32752395)
29. Vanzin GF, et al. (2002) The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proc Natl Acad Sci USA 99:3340-3345. (Pubitemid 34240633)
30. Cavalier DM, et al. (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519-1537. (Pubitemid 352844161)
31. Madson M, et al. (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662-1670. (Pubitemid 36872604)
32. von Schaewen A, Sturm A, O'Neill J, Chrispeels MJ (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.
33. Kang JS, 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.
34. Strasser R, et al. (2007) A unique â1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana. Plant Cell 19:2278-2292. (Pubitemid 47347467)
35. Dolan L, et al. (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71-84. (Pubitemid 23279128)
36. Panchuk-Voloshina N, et al. (1999) Alexa dyes, a series of new fluorescent dyes that yield exceptionally bright, photostable conjugates. J Histochem Cytochem 47:1179-1188. (Pubitemid 29418323)
37. Hinz SW, Verhoef R, Schols HA, Vincken JP, Voragen AG (2005) Type I arabinogalactan contains β-D-Galp-(1→3)-β-D-Galp structural elements. Carbohydr Res 340:2135-2143. (Pubitemid 41139987)
38. Verhoef R, Lu Y, Knox JP, Voragen AG, Schols HA (2009) Fingerprinting complex pectins by chromatographic separation combined with ELISA detection. Carbohydr Res 344:1808-1817.
39. Zablackis E, Huang J, Müller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107:1129-1138.
40. Bush MS, Marry M, Huxham IM, Jarvis MC, McCann MC (2001) Developmental regulation of pectic epitopes during potato tuberisation. Planta 213:869-880. (Pubitemid 32996956)
41. Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300:1715-1718. (Pubitemid 36712561)
42. Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124:1493-1506. (Pubitemid 32053485)
43. Taiz L (1984) Plant cell expansion: Regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585-657.
44. Rounds CM, Lubeck E, Hepler PK, Winship LJ (2011) Propidium iodide competes with Ca (2+) to label pectin in pollen tubes and Arabidopsis root hairs. Plant Physiol 157:175-187.
45. Popper ZA, Fry SC (2008) Xyloglucan-pectin linkages are formed intra-protoplasmically, contribute to wall-assembly, and remain stable in the cell wall. Planta 227:781-794.
46. Abas L, et al. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxinefflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249-256. (Pubitemid 43336066)
47. Soriano Del Amo D, et al. (2010) Biocompatible copper(I) catalysts for in vivo imaging of glycans. J Am Chem Soc 132:16893-16899.