Arabinogalactan proteins: Focus on carbohydrate active enzymes

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Knoch, Eva ^a   Dilokpimol, Adiphol ^a,b   Geshi, Naomi ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

Author keywords

Arabinogalactan proteins; Carbohydrate active enzymes; Glycoside hydrolase; Glycosyltransferase; Plant cell wall; Type II arabinogalactan

Indexed keywords

EID: 84979625970     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00198     Document Type: Review

References (75)

1. Ahn, Y. O., Zheng, M., Bevan, D. R., Esen, A., Shiu, S.-H., Benson, J., et al. (2007). Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry 68, 1510-1520. doi: 10.1016/j.phytochem.2007.03.021
2. Aspinall, G. O., Hirst, E. L., Else, R., and Ramsta, E. (1958). The constitution of larch galactan. J. Chem. Soc. 593-601. doi: 10.1039/jr9580000593
3. Basu, D., Liang, Y., Liu, X., Himmeldirk, K., Faik, A., Kieliszewski, M., et al. (2013). Functional identification of a hydroxyproline-o-galactosyltransferase specific for arabinogalactan protein biosynthesis in Arabidopsis. J. Biol. Chem. 288, 10132-10143. doi: 10.1074/jbc.M112.432609
4. Bonin, C. P., Potter, I., Vanzin, G. F., and Reiter, W.-D. (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. U.S.A. 94, 2085-2090. doi: 10.1073/pnas.94.5.2085
5. Cheung, A. Y., Wang, H., and Wu, H. M. (1995). A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82, 383-393. doi: 10.1016/0092-8674(95)90427-1
6. Dilokpimol, A., and Geshi, N. (2014). Arabidopsis thaliana glucuronosyltransferase in family GT14. Plant Signal. Behav. 9:e28891. doi: 10.4161/psb.28891
7. Dilokpimol, A., Poulsen, C. P., Vereb, G., Kaneko, S., Schulz, A., and Geshi, N. (2014). Galactosyltransferases from Arabidopsis thaliana in the biosynthesis of type II arabinogalactan: molecular interaction enhances enzyme activity. BMC Plant Biol. 14:90. doi: 10.1186/1471-2229-14-90
8. Ellis, M., Egelund, J., Schultz, C. J., and Bacic, A. (2010). Arabinogalactan-proteins (AGPs): key regulators at the cell surface? Plant Physiol. 153, 403-419. doi: 10.1104/pp.110.156000
9. Eudes, A., Mouille, G., Thévenin, J., Goyallon, A., Minic, Z., and Jouanin, L. (2008). Purification, cloning and functional characterization of an endogenous beta-glucuronidase in Arabidopsis thaliana. Plant Cell Physiol. 49, 1331-1341. doi: 10.1093/pcp/pcn108
10. Fujimoto, Z., Ichinose, H., Harazono, K., Honda, M., Uzura, A., and Kaneko, S. (2009). Crystallization and preliminary crystallographic analysis of beta-L-arabinopyranosidase from Streptomyces avermitilis NBRC14893. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65, 632-634. doi: 10.1107/S1744309109017230
11. Fujimoto, Z., Jackson, A., Michikawa, M., Maehara, T., Momma, M., Henrissat, B., et al. (2013). The structure of a Streptomyces avermitilis α-L-rhamnosidase reveals a novel carbohydrate-binding module CBM67 within the six-domain arrangement. J. Biol. Chem. 288, 12376-12385. doi: 10.1074/jbc.M113.460097
12. Gaspar, Y., Johnson, K. L., McKenna, J. A., Bacic, A., and Schultz, C. J. (2001). The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol. Biol. 47, 161-176. doi: 10.1023/A:1010683432529
13. Geshi, N., Johansen, J. N., Dilokpimol, A., Rolland, A., Belcram, K., Verger, S., et al. (2013). A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. Plant J. 76, 128-137. doi: 10.1111/tpj.12281
14. Gibeaut, D. M., and Carpita, N. C. (1991). Tracing cell wall biogenesis in intact cells and plants: selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol. 97, 551-561. doi: 10.1104/pp.97.2.551
15. Gille, S., Hänsel, U., Ziemann, M., and Pauly, M. (2009). Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc. Natl. Acad. Sci. U.S.A. 106, 14699-14704. doi: 10.1073/pnas.0905434106
16. Gille, S., Sharma, V., Baidoo, E. E. K., Keasling, J. D., Scheller, H. V., and Pauly, M. (2013). Arabinosylation of a yariv-precipitable cell wall polymer impacts plant growth as exemplified by the arabidopsis glycosyltransferase mutant ray1. Mol. Plant 6, 1369-1372. doi: 10.1093/mp/sst029
17. Goujon, T., Minic, Z., El Amrani, A., Lerouxel, O., Aletti, E., Lapierre, C., et al. (2003). AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J. 33, 677-690. doi: 10.1046/j.1365-313X.2003.01654.x
18. Groman, E. V., Enriquez, P. M., Jung, C., and Josephson, L. (1994). Arabinogalactan for hepatic drug delivery. Bioconjug. Chem. 5, 547-556. doi: 10.1021/bc00030a010
19. Günl, M., Neumetzler, L., Kraemer, F., de Souza, A., Schultink, A., Pena, M., et al. (2011). AXY8 encodes an α-fucosidase, underscoring the importance of apoplastic metabolism on the fine structure of Arabidopsis cell wall polysaccharides. Plant Cell 23, 4025-4040. doi: 10.1105/tpc.111.089193
20. Haque, M. A., Kotake, T., and Tsumuraya, Y. (2005). Mode of action of beta-glucuronidase from Aspergillus niger on the sugar chains of arabinogalactan-protein. Biosci. Biotechnol. Biochem. 69, 2170-2177. doi: 10.1271/bbb.69.2170
21. Herman, E. M., and Lamb, C. J. (1992). Arabinogalactan-rich glycoproteins are localized on the cell surface and in intravacuolar multivesicular bodies. Plant Physiol. 98, 264-272. doi: 10.1104/pp.98.1.264
22. Ichinose, H., Fujimoto, Z., Honda, M., Harazono, K., Nishimoto, Y., Uzura, A., et al. (2009). A beta-l-Arabinopyranosidase from Streptomyces avermitilis is a novel member of glycoside hydrolase family 27. J. Biol. Chem. 284, 25097-25106. doi: 10.1074/jbc.M109.022723
23. Ichinose, H., Fujimoto, Z., and Kaneko, S. (2013). Characterization of an α-L-Rhamnosidase from Streptomyces avermitilis. Biosci. Biotechnol. Biochem. 77, 213-216. doi: 10.1271/bbb.120735
24. Ichinose, H., Kotake, T., Tsumuraya, Y., and Kaneko, S. (2006a). Characterization of an Exo-β-1,3-D-galactanase from Streptomyces avermitilis NBRC14893 acting on arabinogalactan-proteins. Biosci. Biotechnol. Biochem. 70, 2745-2750. doi: 10.1271/bbb.60365
25. Ichinose, H., Kotake, T., Tsumuraya, Y., and Kaneko, S. (2008). Characterization of an endo-beta-1,6-Galactanase from Streptomyces avermitilis NBRC14893. Appl. Environ. Microbiol. 74, 2379-2383. doi: 10.1128/AEM.01733-07
26. Ichinose, H., Kuno, A., Kotake, T., Yoshida, M., Sakka, K., Hirabayashi, J., et al. (2006b). Characterization of an exo-beta-1,3-galactanase from Clostridium thermocellum. Appl. Environ. Microbiol. 72, 3515-3523. doi: 10.1128/AEM.72.5.3515-3523.2006
27. Ichinose, H., Yoshida, M., Kotake, T., Kuno, A., Igarashi, K., Tsumuraya, Y., et al. (2005). An exo-beta-1,3-galactanase having a novel beta-1,3-galactan-binding module from Phanerochaete chrysosporium. J. Biol. Chem. 280, 25820-25829. doi: 10.1074/jbc.M501024200
28. Ishida, T., Fujimoto, Z., Ichinose, H., Igarashi, K., Kaneko, S., and Samejima, M. (2009). Crystallization of selenomethionyl exo-beta-1,3-galactanase from the basidiomycete Phanerochaete chrysosporium. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65, 1274-1276. doi: 10.1107/S1744309109043395
29. Kaewthai, N., Gendre, D., Eklöf, J. M., Ibatullin, F. M., Ezcurra, I., Bhalerao, R. P., et al. (2013). Group III-A XTH genes of Arabidopsis encode predominant xyloglucan endohydrolases that are dispensable for normal growth. Plant Physiol. 161, 440-454. doi: 10.1104/pp.112.207308
30. Kaulfürst-Soboll, H., Rips, S., Koiwa, H., Kajiura, H., Fujiyama, K., and von Schaewen, A. (2011). Reduced immunogenicity of Arabidopsis hgl1 mutant N-glycans caused by altered accessibility of xylose and core fucose epitopes. J. Biol. Chem. 286, 22955-22964. doi: 10.1074/jbc.M110.196097
31. Kieliszewski, M. J. (2001). The latest hype on Hyp-O-glycosylation codes. Phytochemistry 57, 319-323. doi: 10.1016/S0031-9422(01)00029-2
32. Kitazawa, K., Tryfona, T., Yoshimi, Y., Hayashi, Y., Kawauchi, S., Antonov, L., et al. (2013). β-galactosyl Yariv reagent binds to the β-1,3-galactan of arabinogalactan proteins. Plant Physiol. 161, 1117-1126. doi: 10.1104/pp.112.211722
33. Knoch, E., Dilokpimol, A., Tryfona, T., Poulsen, C. P., Xiong, G., Harholt, J., et al. (2013). A β-glucuronosyltransferase from Arabidopsis thaliana involved in biosynthesis of type II arabinogalactan has a role in cell elongation during seedling growth. Plant J. 76, 1016-1029. doi: 10.1111/tpj.12353
34. Konishi, T., Kotake, T., Soraya, D., Matsuoka, K., Koyama, T., Kaneko, S., et al. (2008). Properties of family 79 beta-glucuronidases that hydrolyze beta-glucuronosyl and 4-O-methyl-beta-glucuronosyl residues of arabinogalactan-protein. Carbohydr. Res. 343, 1191-1201. doi: 10.1016/j.carres.2008.03.004
35. Kotake, T., Dina, S., Konishi, T., Kaneko, S., Igarashi, K., Samejima, M., et al. (2005). Molecular cloning of a b-galactosidase from radish that residues of arabinogalactan protein 1. Plant Physiol. 138, 1563-1576. doi: 10.1104/pp.105.062562
36. Kotake, T., Hirata, N., Degi, Y., Ishiguro, M., Kitazawa, K., Takata, R., et al. (2011). Endo-beta-1,3-galactanase from winter mushroom Flammulina velutipes. J. Biol. Chem. 286, 27848-27854. doi: 10.1074/jbc.M111.251736
37. Kotake, T., Kaneko, S., Kubomoto, A., Haque, M. A., Kobayashi, H., and Tsumuraya, Y. (2004). Molecular cloning and expression in Escherichia coli of a Trichoderma viride endo-beta-(1->6)-galactanase gene. Biochem. J. 377, 749-755. doi: 10.1042/BJ20031145
38. Kotake, T., Kitazawa, K., Takata, R., Okabe, K., Ichinose, H., Kaneko, S., et al. (2009). Molecular cloning and expression in Pichia pastoris of a Irpex lacteus Exo-β-(1→3)-galactanase Gene. Biosci. Biotechnol. Biochem. 73, 2303-2309. doi: 10.1271/bbb.90433
39. Kotake, T., Tsuchiya, K., Aohara, T., Konishi, T., Kaneko, S., Igarashi, K., et al. (2006). An alpha-L-arabinofuranosidase/beta-D-xylosidase from immature seeds of radish (Raphanus sativus L.). J. Exp. Bot. 57, 2353-2362. doi: 10.1093/jxb/erj206
40. Léonard, R., Pabst, M., Bondili, J. S., Chambat, G., Veit, C., Strasser, R., et al. (2008). Identification of an Arabidopsis gene encoding a GH95 alpha1,2-fucosidase active on xyloglucan oligo-and polysaccharides. Phytochemistry 69, 1983-1988. doi: 10.1016/j.phytochem.2008.03.024
41. Liang, Y., Basu, D., Pattathil, S., Xu, W.-L., Venetos, A., Martin, S. L., et al. (2013). Biochemical and physiological characterization of fut4 and fut6 mutants defective in arabinogalactan-protein fucosylation in Arabidopsis. J. Exp. Bot. 64, 5537-5551. doi: 10.1093/jxb/ert321
42. Ling, N. X.-Y., Lee, J., Ellis, M., Liao, M.-L., Mau, S.-L., Guest, D., et al. (2012). An exo-β-(1→3)-d-galactanase from Streptomyces sp. provides insights into type II arabinogalactan structure. Carbohydr. Res. 352, 70-81. doi: 10.1016/j.carres.2012.02.033
43. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M., and Henrissat, B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495. doi: 10.1093/nar/gkt1178
44. Majewska-sawka, A., and Nothnagel, E. A. (2000). The multiple roles of arabinogalactan proteins in plant development. Plant Physiol. 122, 3-9. doi: 10.1104/pp.122.1.3
45. Markovic, O., and Janecek, S. (2001). Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Eng. 14, 615-631. doi: 10.1093/protein/14.9.615
46. Martens-Uzunova, E. S., Zandleven, J. S., Benen, J. A. E., Awad, H., Kools, H. J., Beldman, G., et al. (2006). A new group of exo-acting family 28 glycoside hydrolases of Aspergillus niger that are involved in pectin degradation. Biochem. J. 400, 43-52. doi: 10.1042/BJ20060703
47. Minic, Z., Rihouey, C., Do, C. T., Lerouge, P., and Jouanin, L. (2004). Purification and characterization of enzymes exhibiting beta-D-xylosidase activities in stem tissues of Arabidopsis. Plant Physiol. 135, 867-878. doi: 10.1104/pp.104.041269
48. Miyata, T., Kashige, N., Satho, T., Yamaguchi, T., Aso, Y., and Miake, F. (2005). Cloning, sequence analysis, and expression of the gene encoding Sphingomonas paucimobilis FP2001 alpha-L-rhamnosidase. Curr. Microbiol. 51, 105-109. doi: 10.1007/s00284-005-4487-8
49. Nagae, M., Tsuchiya, A., Katayama, T., Yamamoto, K., Wakatsuki, S., and Kato, R. (2007). Structural basis of the catalytic reaction mechanism of novel 1,2-alpha-L-fucosidase from Bifidobacterium bifidum. J. Biol. Chem. 282, 18497-18509. doi: 10.1074/jbc.M702246200
50. Nothnagel, E. A. (1997). Proteoglycans and related components in plant cells. Int. Rev. Cytol. 174, 195-291. doi: 10.1016/S0074-7696(08)62118-X
51. Odonmazig, P., Ebringerová, A., Machová, E., and Alföldi, J. (1994). Structural and molecular properties of the arabinogalactan isolated from Mongolian larchwood (Larix dahurica L.). Carbohydr. Res. 252, 317-324. doi: 10.1016/0008-6215(94)90028-0
52. Okemoto, K., Uekita, T., Tsumuraya, Y., Hashimoto, Y., and Kasama, T. (2003). Purification and characterization of an endo-beta-(1->6)-galactanase from Trichoderma viride. Carbohydr. Res. 338, 219-230. doi: 10.1016/S0008-6215(02)00405-6
53. Reiter, W.-D., Chapple, C., and Somerville, C. R. (1997). Mutants of Arabidopsis thaliana with altered cell wall polysaccharide composition. Plant J. 12, 335-345. doi: 10.1046/j.1365-313X.1997.12020335.x
54. Rose, J. K. C. (2002). The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol. 43, 1421-1435. doi: 10.1093/pcp/pcf171
55. Sakamoto, T., Taniguchi, Y., Suzuki, S., Ihara, H., and Kawasaki, H. (2007). Characterization of Fusarium oxysporum beta-1,6-galactanase, an enzyme that hydrolyzes larch wood arabinogalactan. Appl. Environ. Microbiol. 73, 3109-3112. doi: 10.1128/AEM.02101-06
56. Schultz, C., Gilson, P., Oxley, D., Youl, J., and Bacic, A. (1998). GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci. 3, 426-431. doi: 10.1016/S1360-1385(98)01328-4
57. Schultz, C. J., Ferguson, K. L., Lahnstein, J., and Bacic, A. (2004). Post-translational modifications of arabinogalactan-peptides of Arabidopsis thaliana. Endoplasmic reticulum and glycosylphosphatidylinositol-anchor signal cleavage sites and hydroxylation of proline. J. Biol. Chem. 279, 45503-45511. doi: 10.1074/jbc.M407594200
58. Seifert, G. J., and Roberts, K. (2007). The biology of arabinogalactan proteins. Annu. Rev. Plant Biol. 58, 137-161. doi: 10.1146/annurev.arplant.58.032806.103801
59. Showalter, A. M. (2001). Arabinogalactan-proteins: structure, expression and function. Cell. Mol. Life Sci. 58, 1399-1417. doi: 10.1007/PL00000784
60. St John, F. J., González, J. M., and Pozharski, E. (2010). Consolidation of glycosyl hydrolase family 30: a dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett. 584, 4435-4441. doi: 10.1016/j.febslet.2010.09.051
61. Sudan, C., Prakash, S., Bhomkar, P., Jain, S., and Bhalla-Sarin, N. (2006). Ubiquitous presence of beta-glucuronidase (GUS) in plants and its regulation in some model plants. Planta 224, 853-864. doi: 10.1007/s00425-006-0276-2
62. Takata, R., Tokita, K., Mori, S., Shimoda, R., Harada, N., Ichinose, H., et al. (2010). Degradation of carbohydrate moieties of arabinogalactan-proteins by glycoside hydrolases from Neurospora crassa. Carbohydr. Res. 345, 2516-2522. doi: 10.1016/j.carres.2010.09.006
63. Tan, L., Qiu, F., Lamport, D. T. A., and Kieliszewski, M. J. (2004). Structure of a hydroxyproline (Hyp)-arabinogalactan polysaccharide from repetitive Ala-Hyp expressed in transgenic Nicotiana tabacum. J. Biol. Chem. 279, 13156-13165. doi: 10.1074/jbc.M311864200
64. Tan, L., Showalter, A. M., Egelund, J., Hernandez-Sanchez, A., Doblin, M. S., and Bacic, A. (2012). Arabinogalactan-proteins and the research challenges for these enigmatic plant cell surface proteoglycans. Front. Plant Sci. 3:140. doi: 10.3389/fpls.2012.00140
65. Tan, L., Varnai, P., Lamport, D. T. A., Yuan, C., Xu, J., Qui, F., et al. (2010). Plant O-hydroxyproline arabinogalactans are composed of repeating trigalactosyl subunits with short bifurcated sidechains. J. Biol. Chem. 285, 24575-24583. doi: 10.1074/jbc.M109
66. Torki, M., Mandaron, P., Mache, R., and Falconet, D. (2000). Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana. Gene 242, 427-436. doi: 10.1016/S0378-1119(99)00497-7
67. Tryfona, T., Liang, H.-C., Kotake, T., Kaneko, S., Marsh, J., Ichinose, H., et al. (2010). Carbohydrate structural analysis of wheat flour arabinogalactan protein. Carbohydr. Res. 345, 2648-2656. doi: 10.1016/j.carres.2010.09.018
68. Tryfona, T., Liang, H.-C., Kotake, T., Tsumuraya, Y., Stephens, E., and Dupree, P. (2012). Structural characterization of Arabidopsis leaf arabinogalactan polysaccharides. Plant Physiol. 160, 653-666. doi: 10.1104/pp.112.202309
69. Tryfona, T., Theys, T. E., Wagner, T., Stott, K., Keegstra, K., and Dupree, P. (2014). Characterisation of FUT4 and FUT6 α-(1→2)-Fucosyltransferases reveals that absence of root arabinogalactan fucosylation increases arabidopsis root growth salt sensitivity. PLoS ONE 9:e93291. doi: 10.1371/journal.pone.0093291
70. Tsumuraya, Y., Mochizuki, N., Hashimoto, Y., and Kovac, P. (1990). Purification of an exo-beta-(1—3)-D-galactanase of Irpex lacteus (Polyporus tulipiferae) and its action on arabinogalactan-proteins. J. Biol. Chem. 265, 7207-7215.
71. Van Hengel, A. J., and Roberts, K. (2002). Fucosylated arabinogalactan-proteins are required for full root cell elongation in arabidopsis. Plant J. 32, 105-113. doi: 10.1046/j.1365-313X.2002.01406.x
72. Vanzin, G. F., Madson, M., Carpita, N. C., Raikhel, N. V., Keegstra, K., and Reiter, W.-D. (2002). The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proc. Natl. Acad. Sci. U.S.A. 99, 3340-3345. doi: 10.1073/pnas.052450699
73. Wang, X. (2001). PLANT PHOSPHOLIPASES. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 211-231. doi: 10.1146/annurev.arplant.52.1.211
74. Wu, Y., Williams, M., Bernard, S., Driouich, A., Showalter, A. M., and Faik, A. (2010). Functional identification of two nonredundant Arabidopsis alpha(1,2)fucosyltransferases specific to arabinogalactan proteins. J. Biol. Chem. 285, 13638-13645. doi: 10.1074/jbc.M110.102715
75. Zeleny, R., Leonard, R., Dorfner, G., Dalik, T., Kolarich, D., and Altmann, F. (2006). Molecular cloning and characterization of a plant α1,3/4-fucosidase based on sequence tags from almond fucosidase I. Phytochemistry 67, 641-648. doi: 10.1016/j.phytochem.2006.01.021