Suberin: The biopolyester at the frontier of plants

Frontiers in Chemistry

Volumn 3, Issue OCT, 2015, Pages

  Graça, José ^a  

^a Universidade de Lisboa   (Portugal)

Author keywords

Cork; Ferulates of hydroxyacids; Poly(acylglycerol) macromolecule; Potato periderm; Suberin; Suberized cell walls

Indexed keywords

EID: 84969584438     PISSN: None     EISSN: 22962646     Source Type: Journal    
DOI: 10.3389/fchem.2015.00062     Document Type: Review

References (82)

1. Beisson, F., Li-Beisson, Y., and Pollard, M. (2012). Solving the puzzles of cutin and suberin polymer biosynthesis. Curr. Opin. Plant Biol. 15, 329-337. doi: 10.1016/j.pbi.2012.03.003
2. Bernards, M. A. (2002). Demystifying suberin. Canad. J. Bot. Revue 80, 227-240. doi: 10.1139/b02-017
3. Bernards, M. A., and Lewis, N. G. (1998). The macromolecular aromatic domain in suberized tissue: a changing paradigm. Phytochemistry 47, 915-933. doi: 10.1016/s0031-9422(98)80052-6
4. Bernards, M. A., Lopez, M. L., Zajicek, J., and Lewis, N. G. (1995). Hydroxycinnamic acid-derived polymers constitute the polyaromatic domain of suberin. J. Biol. Chem. 270, 7382-7386.
5. Bernards, M. A., and Razem, F. A. (2001). The poly(phenolic) domain of potato suberin: a non-lignin cell wall bio-polymer. Phytochemistry 57, 1115-1122. doi: 10.1016/s0031-9422(01)00046-2
6. Borgolivier, O., and Monties, B. (1993). Lignin, suberin, phenolic-acids and tyramine in the suberized, wound-induced potato periderm. Phytochemistry 32, 601-606. doi: 10.1016/s0031-9422(00)95143-4
7. Coquet, C., Bauza, E., Oberto, G., Berghi, A., Farnet, A. M., Ferré, E., et al. (2005). Quercus suber cork extract displays a tensor and smoothing effect on human skin: an in vivo study. Drugs Exp. Clin. Res. 31, 89-99.
8. Cordeiro, N., Belgacem, M. N., Gandini, A., and Neto, C. P. (1999). Urethanes and polyurethanes from suberin 2: synthesis and characterization. Ind. Crops Prod. 10, 1-10. doi: 10.1016/s0926-6690(98)00029-6
9. Dantas, V. D., and Pausas, J. G. (2013). The lanky and the corky: fire-escape strategies in savanna woody species. J. Ecol. 101, 1265-1272. doi: 10.1111/1365-2745.12118
10. De Geus, M., van der Meulen, I., Goderis, B., van Hecke, K., Dorschu, M., van der Werff, H., et al. (2010). Performance polymers from renewable monomers: high molecular weight poly(pentadecalactone) for fiber applications. Polym. Chem. 1, 525-533. doi: 10.1039/b9py00360f
11. Delaux, P. M., Nanda, A. K., Mathe, C., Sejalon-Delmas, N., and Dunand, C. (2012). Molecular and biochemical aspects of plant terrestrialization. Perspect. Plant Ecol. Evol. Syst. 14, 49-59. doi: 10.1016/j.ppees.2011.09.001
12. Douliez, J. P., Barrault, J., Jerome, F., Heredia, A., Navailles, L., and Nallet, F. (2005). Glycerol derivatives of cutin and suberin monomers: Synthesis and self-assembly. Biomacromolecules 6, 30-34. doi: 10.1021/bm049325o
13. Evert, R. F. (2006). Esau's Plant Anatomy: Meristems, Cells, and Tissues of the Plant Body: Their Structure, Function, and Development. Hoboken, NJ: John Wiley & Sons.
14. Ferreira, R., Garcia, H., Sousa, A. F., Guerreiro, M., Duarte, F. J. S., Freire, C. S. R., et al. (2014). Unveiling the dual role of the cholinium hexanoate ionic liquid as solvent and catalyst in suberin depolymerisation. RSC Adv. 4, 2993-3002. doi: 10.1039/c3ra45910a
15. Franke, R. B., Dombrink, I., and Schreiber, L. (2012). Suberin goes genomics: use of a short living plant to investigate a long lasting polymer. Front. Plant Sci. 3:4. doi: 10.3389/fpls.2012.00004
16. Garbow, J. R., Ferrantello, L. M., and Stark, R. E. (1989). C-13 Nuclear magnetic-resonance study of suberized potato cell-wall. Plant Physiol. 90, 783-787. doi: 10.1104/pp.90.3.783
17. Gil, A. M., Lopes, M. H., Neto, C. P., and Rocha, J. (1999). Very high-resolution H-1 MAS NMR of a natural polymeric material. Solid State Nucl. Magn. Reson. 15, 59-67. doi: 10.1016/s0926-2040(99)00047-8
18. Gil, A. M., Lopes, M., Rocha, J., and Neto, C. P. (1997). A C-13 solid state nuclear magnetic resonance spectroscopic study of cork cell wall structure: the effect of suberin removal. Int. J. Biol. Macromol. 20, 293-305. doi: 10.1016/s0141-8130(97)00029-9
19. Gilson, E. (1890). La subérine e les cellules du liège. La Cell. (Louvain) 6, 63-114.
20. Graça, J. (2010). Hydroxycinnamates in suberin formation. Phytochem. Rev. 9, 85-91. doi: 10.1007/s11101-009-9138-4
21. Graça, J., Cabral, V., Santos, S., Lamosa, P., Serra, O., Molinas, M., et al. (2015). Partial depolymerization of genetically modified potato tuber periderm reveals intermolecular linkages in suberin polyester. Phytochemistry 117, 209-219. doi: 10.1016/j.phytochem.2015.06.010
22. Graça, J., and Pereira, H. (1997). Cork suberin: a glyceryl based polyester. Holzforschung 51, 225-234. doi: 10.1515/hfsg.1997.51.3.225
23. Graça, J., and Pereira, H. (1998). Feruloyl esters of omega-hydroxyacids in cork suberin. J. Wood Chem. Technol. 18, 207-217. doi: 10.1080/02773819809349577
24. Graça, J., and Pereira, H. (1999). Glyceryl-acyl and aryl-acyl dimers in Pseudotsuga menziesii bark suberin. Holzforschung 53, 397-402. doi: 10.1515/hf.1999.066
25. Graça, J., and Pereira, H. (2000a). Methanolysis of bark suberins: analysis of glycerol and acid monomers. Phytochem. Anal. 11, 45-51. doi: 10.1002/(sici)1099-1565(200001/02)11:1<45::aid-pca481>3.0.co;2-8
26. Graça, J., and Pereira, H. (2000b). Suberin structure in potato periderm: glycerol, long-chain monomers, and glyceryl and feruloyl dimers. J. Agric. Food Chem. 48, 5476-5483. doi: 10.1021/jf0006123
27. Graça, J., and Santos, S. (2006a). Glycerol-derived ester oligomers from cork suberin. Chem. Phys. Lipids 144, 96-107. doi: 10.1016/j.chemphyslip.2006.08.001
28. Graça, J., and Santos, S. (2006b). Linear aliphatic dimeric esters from cork suberin. Biomacromolecules 7, 2003-2010. doi: 10.1021/bm060174u
29. Graça, J., and Santos, S. (2007). Suberin: a biopolyester of plants' skin. Macromol. Biosci. 7, 128-135. doi: 10.1002/mabi.200600218
30. Guillemonat, A. (1949). Le liége matière première d'une industrie chimique. Revue du Bois 4, 4-6.
31. Guillemonat, A. (1960). Progrès récents dans l'étude de la constitution chimique du liège. Ann. Fac. Sci. Marseille 30, 43-54.
32. Heinäemäeki, J., Halenius, A., Paavo, M., Alakurtti, S., Pitkäenen, P., Pirttimaa, M., et al. (2015). Suberin fatty acids isolated from outer birch bark improve moisture barrier properties of cellulose ether films intended for tablet coatings. Int. J. Pharm. 489, 91-99. doi: 10.1016/j.ijpharm.2015.04.066
33. Holloway, P. J. (1983). Some variations in the composition of suberin from the cork layers of higher-plants. Phytochemistry 22, 495-502. doi: 10.1016/0031-9422(83)83033-7
34. Huf, S., Kruegener, S., Hirth, T., Rupp, S., and Zibek, S. (2011). Biotechnological synthesis of long-chain dicarboxylic acids as building blocks for polymers. Europ. J. Lipid Sci. Technol. 113, 548-561. doi: 10.1002/ejlt.201000112
35. Jensen, W. (1952). Studies on suberin. IV. Isolation of phloionic acid from suberin of Quercus suber. Paperi ja Puu 34B, 467-479.
36. Koch, K., and Barthlott, W. (2009). Superhydrophobic and superhydrophilic plant surfaces: an inspiration for biomimetic materials. Philos. Trans. R. Soc. 367, 1487-1509. doi: 10.1098/rsta.2009.0022
37. Kolattukudy, P. (2001). "Polyesters in Higher Plants, "in Biopolyesters, eds W. Babel and A. Steinbüchel (Berlin; Heidelberg: Springer), 1-49.
38. Kolattukudy, P. E. (2002). "Suberin from Plants, "in Biopolymers. Polyesters I., eds. Y. Doi and A. Steinbüchel (Weinheim: Wiley-VCH Verlag), 41-73.
39. Kolattukudy, P. E., and Espelie, K. E. (1989). "Chemistry, biochemistry, and function of suberin and associated waxes, "in Natural Products of Woody Plants, ed J. Rowe (Berlin; Heidelberg: Springer), 304-367.
40. Kolattukudy, P. E., Kronman, K., and Poulose, A. J. (1975). Determination of structure and composition of suberin from roots of carrot, parsnip, rutabaga, turnip, red beet, and sweet-potato by combined gas-liquid-chromatography and mass-spectrometry. Plant Physiol. 55, 567-573. doi: 10.1104/pp.55.3.567
41. Krizková, L., Lopes, M. H., Polónyi, J., Belicová, A., Dobias, J., and Ebringer, L. (1999). Antimutagenicity of a suberin extract from Quercus suber cork. Mut. Res. Genet. Toxicol. Environ. Mutagen. 446, 225-230. doi: 10.1016/s1383-5718(99)00190-4
42. Lapierre, C., Pollet, B., and Negrel, J. (1996). The phenolic domain of potato suberin: structural comparison with lignins. Phytochemistry 42, 949-953. doi: 10.1016/0031-9422(96)00097-0
43. Lulai, E. C., and Corsini, D. L. (1998). Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing. Physiol. Mol. Plant Pathol. 53, 209-222. doi: 10.1006/pmpp.1998.0179
44. Lulai, E. C., and Orr, P. H. (1994). Techniques for detecting and measuring developmental and maturational changes in tuber native periderm. Am. Potato J. 71, 489-505. doi: 10.1007/bf02851322
45. Marques, A. V., and Pereira, H. (2013). Lignin monomeric composition of corks from the barks of Betula pendula, Quercus suber and Quercus cerris determined by Py-GC-MS/FID. J. Anal. Appl. Pyrolysis 100, 88-94. doi: 10.1016/j.jaap.2012.12.001
46. Mattinen, M. L., Filpponen, I., Järvinen, R., Li, B., Kallio, H., Lehtinen, P., et al. (2009). Structure of the Polyphenolic Component of Suberin Isolated from Potato (Solanum tuberosum var. Nikola). J. Agric. Food Chem. 57, 9747-9753. doi: 10.1021/jf9020834
47. Molina, I., Li-Beisson, Y., Beisson, F., Ohlrogge, J. B., and Pollard, M. (2009). Identification of an arabidopsis feruloyl-coenzyme a transferase required for suberin synthesis. Plant Physiol. 151, 1317-1328. doi: 10.1104/pp.109.144907
48. Negrel, J., Pollet, B., and Lapierre, C. (1996). Ether-linked ferulic acid amides in natural and wound periderms of potato tuber. Phytochemistry 43, 1195-1199. doi: 10.1016/s0031-9422(96)00500-6
49. Neto, C. P., Cordeiro, N., Seca, A., Domingues, F., Gandini, A., and Robert, D. (1996). Isolation and characterization of a lignin-like polymer of the cork of Quercus suber L. Holzforschung 50, 563-568. doi: 10.1515/hfsg.1996.50.6.563
50. Neto, C. P., Rocha, J., Gil, A., Cordeiro, N., Esculcas, A. P., Rocha, S., et al. (1995). C-13 solid-state nuclear-magnetic-resonance and fourier-transform infrared studies of the thermal-decomposition of cork. Solid State Nucl. Magn. Reson. 4, 143-151. doi: 10.1016/0926-2040(94)00039-f
51. Neubauer, J. D., Lulai, E. C., Thompson, A. L., Suttle, J. C., Bolton, M. D., and Campbell, L. G. (2013). Molecular and cytological aspects of native periderm maturation in potato tubers. J. Plant Physiol. 170, 413-423. doi: 10.1016/j.jplph.2012.10.008
52. Olsson, A., Lindström, M., and Iversen, T. (2007). Lipase-catalyzed synthesis of an epoxy-functionalized polyester from the suberin monomer cis-9, 10-epoxy-18-hydroxyoctadecanoic acid. Biomacromolecules 8, 757-760. doi: 10.1021/bm060965w
53. Pereira, H. (1988). Chemical-composition and variability of cork from quercus-suber L. Wood Sci. Technol. 22, 211-218.
54. Pereira, H. (2007). "Chapter 11-Cork products and uses, "in Cork, ed H. Pereira (Amsterdam: Elsevier Science B.V.), 243-261.
55. Pinot, F., and Beisson, F. (2011). Cytochrome P450 metabolizing fatty acids in plants: characterization and physiological roles. Febs J. 278, 195-205. doi: 10.1111/j.1742-4658.2010.07948.x
56. Pinto, P., Sousa, A. R., Silvestre, A. J. D., Neto, C. P., Gandini, A., Eckerman, C., et al. (2009). Quercus suber and Betula pendula outer barks as renewable sources of oleochemicals: a comparative study. Ind. Crops Prod. 29, 126-132. doi: 10.1016/j.indcrop.2008.04.015
57. Pollard, M., Beisson, F., Li, Y., and Ohlrogge, J. B. (2008). Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13, 236-246. doi: 10.1016/j.tplants.2008.03.003
58. Ribas, I. (1952). étude sur la constitution chimique du liège. Chim. Industr. 68, 333-350.
59. Ribas, I., and Blasco, E. (1940). Investigaciones sobre el corcho. I. Sobre la existencia de glicerina. Anal. Real Soc. Españ. Fís. Quím. 36B, 141-147.
60. Riley, R. G., and Kolattukudy, P. E. (1975). Evidence for covalently attached para-coumaric acid and ferulic acid in cutins and suberins. Plant Physiol. 56, 650-654. doi: 10.1104/pp.56.5.650
61. Rios, P., Cabral, V., Santos, S., Mori, F., and Graça, J. (2014). The chemistry of Kielmeyera coriacea outer bark: a potential source for cork. Europ. J. Wood Wood Prod. 72, 509-519. doi: 10.1007/s00107-014-0811-y
62. Santos, S., Cabral, V., and Graça, J. (2013). Cork suberin molecular structure: stereochemistry of the C-18 Epoxy and vic-diol omega-hydroxyacids and alpha, omega-diacids analyzed by NMR. J. Agric. Food Chem. 61, 7038-7047. doi: 10.1021/jf400577k
63. Santos, S., and Graça, J. (2006). Glycerol-omega-hydroxyacid-ferulic acid oligomers in cork suberin structure. Holzforschung 60, 171-177. doi: 10.1515/hf.2006.028
64. Santos, S., and Graça, J. (2014). Stereochemistry of C-18 monounsaturated cork suberin acids determined by spectroscopic techniques including H-1-NMR multiplet analysis of olefinic protons. Phytochem. Anal. 25, 192-200. doi: 10.1002/pca.2491
65. Schmutz, A., Buchala, A. J., and Ryser, U. (1996). Changing the dimensions of suberin lamellae of green cotton fibers with a specific inhibitor of the endoplasmic reticulum-associated fatty acid elongases. Plant Physiol. 110, 403-411.
66. Schreiber, L. (2010). Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci. 15, 546-553. doi: 10.1016/j.tplants.2010.06.004
67. Schreiber, L., Franke, R., and Hartmann, K. (2005). Wax and suberin development of native and wound periderm of potato (Solanum tuberosum L.) and its relation to peridermal transpiration. Planta 220, 520-530. doi: 10.1007/s00425-004-1364-9
68. Serra, O., Soler, M., Hohn, C., Sauveplane, V., Pinot, F., Franke, R., et al. (2009). CYP86A33-Targeted gene silencing in potato tuber alters suberin composition, distorts suberin lamellae, and impairs the periderm's water barrier function. Plant Physiol. 149, 1050-1060. doi: 10.1104/pp.108.127183
69. Sitte, P. (1959). Mischkorperdoppelbrechung der kork-zellwande. Naturwissenschaften 46, 260-261.
70. Sitte, P. (1962). Zum feinbau der suberinschichten im flaschenkork. Protoplasma 54, 555-559. doi: 10.1007/bf01252642
71. Soliday, C. L., Kolattukudy, P. E., and Davis, R. W. (1979). Chemical and ultrastructural evidence that waxes associated with the suberin polymer constitute the major diffusion barrier to water-vapor in potato-tuber (Solanum-Tuberosum-L). Planta 146, 607-614. doi: 10.1007/bf00388840
72. Sousa, A. F., Gandini, A., Silvestre, A. J. D., Neto, C. P., Pinto, J., Eckerman, C., et al. (2011). Novel suberin-based biopolyesters: from synthesis to properties. J. Pol. Sci. Part A Pol. Chem. 49, 2281-2291. doi: 10.1002/pola.24661
73. Stark, R. E., and Garbow, J. R. (1992). Nuclear-magnetic-resonance relaxation studies of plant polyester dynamics.2. Suberized potato cell-wall. Macromolecules 25, 149-154. doi: 10.1021/ma00027a025
74. Teixeira, R. T., and Pereira, H. (2010). Suberized cell walls of cork from cork oak differ from other species. Micros. Microanal. 16, 569-575. doi: 10.1017/s1431927610093839
75. Torron, S., Semlitsch, S., Martinelle, M., and Johansson, M. (2014). Polymer thermosets from multifunctional polyester resins based on renewable monomers. Macromol. Chem. Phys. 215, 2198-2206. doi: 10.1002/macp.201400192
76. Vandoorn, W. G., and Stead, A. D. (1997). Abscission of flowers and floral parts. J. Exp. Bot. 48, 821-837. doi: 10.1093/jxb/48.4.821
77. Vanwisselingh, C. (1888). Sur la paroi des celules subéreuses. Arch.Neérland. Sci. Exact. Natur. 22, 253-298.
78. Wang, W., Tian, S., and Stark, R. E. (2010). Isolation and identification of triglycerides and ester oligomers from partial degradation of potato suberin. J. Agric. Food Chem. 58, 1040-1045. doi: 10.1021/jf902854y
79. Yan, B., and Stark, R. E. (1998). A WISE NMR approach to heterogeneous biopolymer mixtures: dynamics and domains in wounded potato tissues. Macromolecules 31, 2600-2605. doi: 10.1021/ma9714880
80. Yan, B., and Stark, R. E. (2000). Biosynthesis, molecular structure, and domain architecture of potato suberin: a C-13 NMR study using isotopically labeled precursors. J. Agric. Food Chem. 48, 3298-3304. doi: 10.1021/jf000155q
81. Yang, W., Pollard, M., Li-Beisson, Y., Beisson, F., Feig, M., and Ohlrogge, J. (2010). A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc. Natl. Acad. Sci. U.S.A. 107, 12040-12045. doi: 10.1073/pnas.0914149107
82. Yokota, T., and Watanabe, A. (1990). Process for producing omega-hydroxy fatty acids. European patent EP0357865A3. Available online at: http://www.google.com/patents/EP0357865A3?cl=en