Abstract
Suberin is a lipid-phenolic biopolyester deposited in the cell walls of certain boundary tissue layers of plants, such as root endodermis, root and tuber peridermis, and seed coats. Suberin serves as a protective barrier in these tissue layers, controlling, for example, water and ion transport. It is also a stress-induced anti-microbial barrier. The suberin polymer contains a variety of C16–C24 chain-length aliphatics, such as ω-hydroxy fatty acids, α,ω-dicarboxylic fatty acids, and primary fatty alcohols. Suberin also contains high amounts of glycerol and phenolics, especially ferulic acid. In addition, non-covalently linked waxes are likely associated with the suberin polymer. This review focusses on the suberin biosynthetic enzymes identified to date, which include β-ketoacyl-CoA synthases, fatty acyl reductases, long-chain acyl-CoA synthetases, cytochrome P450 monooxygenases, glycerol 3-phosphate acyltransferases, and phenolic acyltransferases. We also discuss recent advances in our understanding of the transport of suberin components intracellularly and to the cell wall, polymer assembly, and the regulation of suberin deposition.
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Abbreviations
- ABC:
-
ATP-binding cassette
- ASFT:
-
Aliphatic suberin feruloyl transferase
- CoA:
-
Coenzyme A
- CYP:
-
Cytochrome P450 monooxygenase
- DCA:
-
α,ω-Dicarboxylic acid
- ER:
-
Endoplasmic reticulum
- FACT:
-
Fatty alcohol: caffeoyl-CoA caffeoyl transferase
- FAR:
-
Fatty acyl reductase
- FTH:
-
Suberin feruloyl transferase
- GPAT:
-
Glycerol 3-phosphate acyltransferase
- KCS:
-
β-Ketoacyl-CoA synthase
- LACS:
-
Long-chain acyl-CoA synthetase
- LTP:
-
Lipid transfer protein
References
Agrawal V, Kolattukudy P (1978) Purification and characterization of a wound-induced omega-hydroxy fatty acid:NADP oxidoreductase from potato tuber disks (Solanum tuberosum L.). Arch Biochem Biophys 191:452–465
Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, Muthukumar B, Mickelbart MV, Schreiber L, Franke RB, Salt DE (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5:e1000492
Beisson F, Koo AJK, Ruuska S, Schwender J, Pollard M, Thelen JJ, Paddock T, Salas JJ, Savage L, Milcamps A, Mhaske VB, Cho Y, Ohlrogge JB (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol 132:681–697
Beisson F, Li-Beisson Y, Bonaventure G, Pollard M, Ohlrogge JB (2007) The acyltransferase GPAT5 is required for the synthesis of suberin in the seed coat and root of Arabidopsis. Plant Cell 19:351–368
Beisson F, Li-Beisson Y, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol 15:329–337
Bernards MA (2002) Demystifying suberin. Can J Bot 80:227–240
Bernards MA, Lewis NG (1992) Alkyl ferulates in wound-healing potato-tubers. Phytochemistry 31:3409–3412
Bernards MA, Lopez ML, Zajeck J, Lewis NG (1995) Hydroxycinnamic acid-derived polymers constitute the polyaromatic domain of suberin. J Biol Chem 270:7382–7386
Bernards MA, Fleming WD, Llewellyn DB, Priefer R, Yang X, Sabatino A, Plourde GL (1999) Biochemical characterization of the suberization-associated anionic peroxidase of potato. Plant Physiol 121:135–145
Boher P, Serra O, Soler M, Molinas M, Figueras M (2013) The potato suberin feruloyl transferase FHT which accumulates in the phellogen is induced by wounding and regulated by abscisic and salicylic acids. J Exp Bot 64:3225–3236
Choi H, Jin JY, Choi S, Hwang JU, Kim YY, Suh MC, Lee Y (2011) An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J 65:181–193
Compagnon V, Diehl P, Benveniste I, Meyer D, Schaller H, Schreiber L, Franke R, Pinot F (2009) CYP86B1 is required for very long chain ω-hydroxyacid and α,ω-dicarboxylic acid synthesis in root and seed suberin polyester. Plant Physiol 150:1831–1843
Dean BB, Kolattukudy PE (1977) Biochemistry of suberization—incorporation of [1-C-14] oleic acid and [1-C-14] acetate into aliphatic components of suberin in potato tuber disks (Solanum tuberosum). Plant Physiol 59:48–54
Domergue F, Vishwanath SJ, Joubès J, Ono J, Lee J, Bourdon M, Alhattab R, Lowe C, Pascal S, Lessire R, Rowland O (2010) Three Arabidopsis fatty acyl-CoA reductases, FAR1, FAR4, and FAR5, generate primary fatty alcohols associated with suberin deposition. Plant Physiol 153:1539–1554
Edstam MM, Edqvist J (2014) Involvement of GPI-anchored lipid transfer proteins in the development of seed coats and pollen in Arabidopsis thaliana. Physiol Plant 152:32–42
Edstam MM, Blomqvist K, Eklöf A, Wennergren U, Edqvist J (2013) Coexpression patterns indicate that GPI-anchored non-specific lipid transfer proteins are involved in accumulation of cuticular wax, suberin and sporopollenin. Plant Mol Biol 83:625–649
Enstone DE, Peterson CA, Ma F (2003) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351
Espelie KE, Kolattukudy PE (1985) Purification and characterization of an abscisic acid-inducible anionic peroxidase associated with suberization in potato (Solanum tuberosum). Arch Biochem Biophys 240:539–545
Espelie KE, Sadek NZ, Kolattukudy PE (1980) Composition of suberin-associated waxes from the subterranean storage organs of seven plants, parsnip, carrot, rutabaga, turnip, red beet, sweet potato and potato. Planta 148:468–476
Franke R, Schreiber L (2007) Suberin—a biopolyester forming apoplastic plant interfaces. Curr Opin Plant Biol 10:252–259
Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C, Schreiber L (2005) Apoplastic polyesters in Arabidopsis surface tissues—a typical suberin and a particular cutin. Phytochemistry 66:2643–2658
Franke R, Hofer R, Briesen I, Emsermann M, Efremova N, Yephremov A, Schreiber L (2009) The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. Plant J 57:80–95
Franke R, Dombrink I, Schreiber L (2012) Suberin goes genomics: use of a short living plant to investigate a long lasting polymer. Front Plant Sci 3:1–8
Gandini A (2008) Polymers from renewable resources: a challenge for the future of macromolecular materials. Macromolecules 41:9491–9504
Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J, Runavot JL, Quemener B, Petit J, Germain V, Rothan C, Marion D, Bakan B (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24:3119–3134
Gou J-Y, Yu X-H, Liu C-J (2009) A hydroxycinnamoyltransferase responsible for synthesizing suberin aromatics in Arabidopsis. Proc Natl Acad Sci USA 106:18855–18860
Graça J, Pereira H (2000a) Suberin structure in potato periderm: glycerol, long-chain monomers, and glyceryl and feruroyl dimers. J Agri Food Chem 48:5476–5483
Graça J, Pereira H (2000b) Methanolysis of bark suberins: analysis of glycerol and acid monomers. Phytochem Anal 11:45–51
Graça J, Santos S (2006) Glycerol-derived ester oligomers from cork suberin. Chem Phys Lipids 144:96–107
Haslam TM, Mañas-Fernández A, Zhao L, Kunst L (2012) Arabidopsis ECERIFERUM2 is a component of the fatty acid elongation machinery required for fatty acid extension to exceptional lengths. Plant Physiol 160:1164–1174
Höfer R, Briesen I, Beck M, Pinot F, Schreiber L, Franke R (2008) The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid omega-hydroxylase involved in suberin monomer biosynthesis. J Exp Bot 59:2347–2360
Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W (2001) The exodermis—a variable apoplastic barrier. J Exp Bot 52:2245–2264
Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE (2013) Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc Natl Acad Sci USA 110:14498–14503
Huang MD, Chen TL, Huang AH (2013) Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol 163:1218–1229
Kim H, Lee SB, Kim HJ, Min MK, Hwang I, Suh MC (2012) Characterization of glycosylphosphatidylinositol-anchored lipid transfer protein 2 (LTPG2) and overlapping function between LTPG/LTPG1 and LTPG2 in cuticular wax export or accumulation in Arabidopsis thaliana. Plant Cell Physiol 53:1391–1403
Kolattukudy PE (1980) Biopolyester membranes of plants: cutin and suberin. Science 208:990–1000
Kolattukudy PE (1981) Structure, biosynthesis and biodegradation of cutin and suberin. Annu Rev Plant Physiol 32:539–567
Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Eng Biotechnol 71:1–49
Kosma DK, Molina I, Ohlrogge JB, Pollard M (2012) Identification of an Arabidopsis fatty alcohol:caffeoyl-Coenzyme A acyltransferase required for the synthesis of alkyl hydroxycinnamates in root waxes. Plant Physiol 160:237–248
Kosma DK, Murmu J, Razeq FM, Santos P, Bourgault R, Molina I, Rowland O (2014) AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. Plant J 80:216–229
Kurdyukov S, Faust A, Nawrath C, Bar S, Voisin D, Efremova N, Franke R, Schreiber L, Saedler H, Metraux JP, Yephremov A (2006) The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18:321–339
Landgraf R, Smolka U, Altmann S, Eschen-Lippold L, Senning M, Sonnewald S, Weigel B, Frolova N, Strehmel N, Hause G, Scheel D, Böttcher C, Rosahl S (2014) The ABC transporter ABCG1 is required for suberin formation in potato tuber periderm. Plant Cell 26:3403–3415
Lee SB, Jung SJ, Go YS, Kim HU, Kim JK, Cho HJ, Park OK, Suh MC (2009) Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J 60:462–475
Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153:402–412
Li Y, Beisson F, Koo AJ, Molina I, Pollard M, Ohlrogge J (2007a) Identification of acyltransferases required for cutin synthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104:18339–18344
Li Y, Beisson F, Ohlrogge J, Pollard M (2007b) Monoacylglycerols are components of root waxes and can be produced in the aerial cuticle by ectopic expression of a suberin associated acyltransferase. Plant Physiol 144:1267–1277
Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, DeBono A, Durrett TD, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2013) Acyl-lipid metabolism. Arabidopsis Book 11:e0161
Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (2009) Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59:553–564
Matzke K, Reiderer R (1991) A comparative study into the chemical constitution of cutins and suberins from Picea abies (L.) Karst., Quercus robur L., and Fagus sylvatica L. Planta 185:233–245
McFarlane HE, Watanabe Y, Yang W, Huang Y, Ohlrogge J, Samuels AL (2014) Golgi- and trans-Golgi network-mediated vesicle trafficking is required for wax secretion from epidermal cells. Plant Physiol 164:1250–1260
Meyer CJ, Peterson CA, Bernards MA (2011) A comparison of suberin monomers from the multiseriate exodermis of Iris germanica during maturation under differing growth conditions. Planta 233:773–786
Millar AA, Kunst L (1997) Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme. Plant J 12:121–131
Moire L, Schmutz A, Buchala A, Yan B, Stark RE, Ryser U (1999) Glycerol is a suberin monomer: new experimental evidence for an old hypothesis. Plant Physiol 119:1137–1146
Molina I (2010) Biosynthesis of plant lipid polyesters. The AOCS lipid library. http://lipidlibrary.aocs.org/plantbio/polyesters/index.htm. Accessed July 2014
Molina I, Bonaventure G, Ohlrogge J, Pollard M (2006) The lipid polyester composition of Arabidopsis thaliana and Brassica napus seeds. Phytochemistry 67:2597–2610
Molina I, Ohlrogge J, Pollard M (2008) Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana. Plant J 53:437–449
Molina I, Beisson-Li Y, Beisson F, Ohlrogge J, Pollard M (2009) Identification of an Arabidopsis feruloyl-CoA transferase required for suberin synthesis. Plant Physiol 151:1317–1328
Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci USA 109:10101–10106
Nawrath C (2002) The biopolymers cutin and suberin. Arabidopsis Book 1:e0021
Nawrath C, Schreiber L, Franke RB, Geldner N, Reina-Pinto JJ, Kunst L (2013) Apoplastic diffusion barriers in Arabidopsis. Arabidopsis Book 11:e0167
Pascal S, Bernard A, Sorel M, Pervent M, Vile D, Haslam RP, Napier JA, Lessire R, Domergue F, Joubès J (2013) The Arabidopsis cer26 mutant, like the cer2 mutant, is specifically affected in the very long chain fatty acid elongation process. Plant J 73:733–746
Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels LA (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702–704
Pinto PCRO, Sousa AF, Silvestre AJD, Neto CP, Gandini A, Eckerman C, Holmbom B (2009) Quercus suber and Betula pendula outer barks as renewable sources of oleochemicals: a comparative study. Ind Crops Prod 29:126–132
Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246
Ranathunge K, Schreiber L (2011) Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. J Exp Bot 62:1961–1974
Ranathunge K, Schreiber L, Franke R (2011) Suberin research in the genomics era—new interest for an old polymer. Plant Sci 180:399–413
Razeq FM, Kosma DK, Rowland O, Molina I (2014) Extracellular lipids of Camelina sativa: characterization of chloroform-extractable waxes from aerial and subterranean surfaces. Phytochemistry 106:188–196
Rowland O, Domergue F (2012) Plant fatty acyl reductases: enzymes generating fatty alcohols for protective layers with potential for industrial applications. Plant Sci 193–194:28–38
Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707
Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16:629–642
Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553
Schreiber L, Franke R, 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
Serra O, Soler M, Hohn C, Franke R, Schreiber L, Prat S, Molinas M, Figueras M (2009a) Silencing of StKCS6 in potato periderm leads to reduced chain lengths of suberin and wax compounds and increased peridermal transpiration. J Exp Bot 60:697–707
Serra O, Soler M, Hohn C, Sauveplane V, Pinot F, Franke R, Schreiber L, Prat S, Molinas M, Figueras M (2009b) 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
Serra O, Hohn C, Franke R, Prat S, Molinas M, Figueras M (2010) A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm. Plant J 62:277–290
Shiono K, Ando M, Nishiuchi S, Takahashi H, Watanabe K, Nakamura M, Matsuo Y, Yasuno N, Yamanouchi U, Fujimoto M, Takanashi H, Ranathunge K, Franke RB, Shitan N, Nishizawa NK, Takamure I, Yano M, Tsutsumi N, Schreiber L, Yazaki K, Nakazono M, Kato K (2014) RCN1/OsABCG5, an ATP-binding cassette (ABC) transporter, is required for hypodermal suberization of roots in rice (Oryza sativa). Plant J 80:40–51
Shockey JM, Fulda MS, Browse JA (2002) Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol 129:1710–1722
Silva S, Sabino M, Fernandes E, Correlo V, Boesel L, Reis R (2005) Cork: properties, capabilities and applications. Int Mater Rev 50:345–365
Soler M, Serra O, Molinas M, Huguet G, Fluch S, Figueras M (2007) A genomic approach to suberin biosynthesis and cork differentiation. Plant Physiol 144:419–431
Soliday CL, Kolattukudy PE, Davis RW (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
Stark RE, Sohn W, Pacchiano RA, Albashir M, Garbow JR (1994) Following suberization in potato wound periderm by histochemical and solid-state C-13 nuclear-magnetic-resonance methods. Plant Physiol 104:527–533
Thomas R, Fang X, Ranathunge K, Anderson TR, Peterson CA, Bernards MA (2007) Soybean root suberin: anatomical distribution, chemical composition, and relationship to partial resistance to Phytophthora sojae. Plant Physiol 144:299–311
Vishwanath SJ, Kosma DK, Pulsifer IP, Scandola S, Pascal S, Joubès J, Dittrich-Domergue F, Lessire R, Rowland O, Domergue F (2013) Suberin-associated fatty alcohols in Arabidopsis thaliana: distributions in roots and contributions to seed coat barrier properties. Plant Physiol 163:1118–1132
Yadav V, Molina I, Ranathunge K, Castillo IQ, Rothstein SJ, Reed JW (2014) ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell 26:3569–3588
Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, 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 USA 107:12040–12045
Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB (2012) A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol 160:638–652
Yeats TH, Laetitia BB, Martin Viart HMF, Isaacson T, He Y, Zhao L, Matas AJ, Buda GJ, Domozych SD, Clausen MH, Rose JKC (2012) The identification of cutin synthase: formation of the plant polyester cutin. Nature Chem Biol 8:609–611
Yeats TH, Huang W, Chatterjee S, Viart HM, Clausen MH, Stark RE, Rose JK (2014) Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J 77:667–675
Zeier J, Schreiber L (1998) Comparative investigation of primary and tertiary endodermal cell walls isolated from the roots of five monocotyledoneous species: chemical composition in relation to fine structure. Planta 206:349–361
Acknowledgments
We thank Nayana de Silva and Jessica White of Carleton University for valuable comments on the manuscript. SJV and OR were supported by the Natural Sciences and Engineering Research Council of Canada. CD was supported by a doctoral fellowship from the French Ministère de l’Enseignement Supérieur et de la Recherche.
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The authors declare that they have no conflicts of interest.
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Vishwanath, S.J., Delude, C., Domergue, F. et al. Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep 34, 573–586 (2015). https://doi.org/10.1007/s00299-014-1727-z
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DOI: https://doi.org/10.1007/s00299-014-1727-z