Log in

What can feruloyl esterases do for us?

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

The role of feruloyl esterases in plant wall development, in gut health, and in the breakdown of plant biomass for the production of bioactive phytochemicals and biofuel is covered in this review. These enzymes have potential roles in stomatal cell function and the phenolic substitutions and cross-linkages between plant cell wall components. As more plant genomes are sequenced, the role of ferulic acid and feruloyl esterases in planta may be better understood. In human and ruminal digestion, these enzymes are important to de-esterify dietary fibre, releasing hydroxycinnamates and derivatives which have been shown to have positive health effects, such as antioxidant, anti-inflammatory and anti-microbial activities. They are also involved in colonic fermentation where their extracellular and intracellular activities in the microbiota improve the breakdown of polysaccharides and increase microbial production of short chain fatty acids. Their specificity can also be employed to synthesize bioactive compounds for cosmetic and health applications. The enzymatic disassembly of cereal straws is greatly enhanced when feruloyl esterase activity is present, although the substrate specificity of the esterase appears to have some bearing on its optimal application. The involvement of feruloyl esterases in the improved enzymatic and microbial saccharification of cereal-derived material demonstrates a high importance for these enzymes in animal feed preparation and bioalcohol production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Brazil)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AnFaeA:

Type-A feruloyl esterase from Aspergillus niger

AnFaeB:

Type-B feruloyl esterase from Aspergillus niger

CA:

Caffeic acid

ChlA:

Chlorogenic acid

CLEA:

Cross-linked enzyme aggregate

diFA:

Diferulic acid

DPPH:

1,1-Diphenyl-2-picrylhydrazyl

FA:

Ferulic acid

FAE:

Feruloyl esterase

GH10:

Glycoside hydrolase family 10

GH11:

Glycoside hydrolase family 11

HCA:

Hydroxycinnamic acids

kDa:

One thousand Dalton units

LDL:

Low-density lipoprotein

MCA:

Methyl caffeate

MFA:

Methyl ferulate

MpCA:

Methyl p-coumarate

MSA:

Methyl sinapate

pCA:

p-Coumaric acid

SA:

Sinapic acid

StFaeC:

Type-C feruloyl esterase from Sporotrichum thermosporum

TsFaeC:

Type-C feruloyl esterase from Talaromyces stipitatus

WB:

Wheat bran

WS:

Wheat straw

References

  • Akin DE, Chesson A (1989) Lignification as the major factor limiting forage feeding value especially in warm conditions. Proc Int Grassl Congr 16:1753–1760

    Google Scholar 

  • Andersen A, Svendsen A et al (2002) Studies on ferulic acid esterase activity in fungal lipases and cutinases. Colloid Surf B Biointerfaces 26:47–55

    Article  CAS  Google Scholar 

  • Anderson WF, Akin DE (2008) Structural and chemical properties of grass lignocelluloses related to conversion for biofuels. J Ind Microbiol Biotechnol 35:355–366

    Article  CAS  PubMed  Google Scholar 

  • Andreasen MF, Kroon PA et al (2001a) Esterase activity able to hydrolyze dietary antioxidant hydroxycinnamates is distributed along the intestine of mammals. J Agric Food Chem 49:5679–5684

    Article  CAS  PubMed  Google Scholar 

  • Andreasen MF, Kroon PA et al (2001b) Intestinal release and uptake of phenolic antioxidant diferulic acids. Free Rad Biol Med 31:304–314

    Article  CAS  PubMed  Google Scholar 

  • Aurilia V, Parracino A, D’Auria S (2008) Microbial carbohydrase esterases in cold adapted environments. Gene 410:234–240

    Article  CAS  PubMed  Google Scholar 

  • Bathena J, Kulamarva A et al (2007) Microencapsulated bacterial cells can be used to produce the enzyme feruloyl esterase: preparation and in vitro analysis. Appl Microbiol Biotechnol 75:1023–1029

    Article  Google Scholar 

  • Bathena J, Kulamarva A et al (2008) Preparation and in vitro analysis of microencapsulated live Lactobacillus fermentum 11976 for augmentation of feruloyl esterase in the gastrointestinal tract. Biotechnol Appl Biochem 50:1–9

    Article  Google Scholar 

  • Beaugrand J, Chambat G et al (2004) Impact and efficiency of GH10 and GH11 thermostable endoxylanases on wheat bran and alkali-extractable arabinoxylans. Carbohydr Res 339:2529–2540

    Article  CAS  PubMed  Google Scholar 

  • Benoit I, Navarro D et al (2006) Feruloyl esterases as a tool for the release of phenolic compounds from agro-industrial by-products. Carbohydr Res 341:1820–1827

    Article  CAS  PubMed  Google Scholar 

  • Benoit I, Danchin EGJ et al (2008) Biotechnological applications and potential of fungal feruloyl esterases based on prevalence, classification and biochemical diversity. Biotechnol Lett 30:387–396

    Article  CAS  PubMed  Google Scholar 

  • Blum DL, Kataeva IA et al (2000) Feruloyl esterase activity of the Clostridium thermocellum cellulosome can be attributed to previously unknown domains of XynY and XynZ. J Bacteriol 182:1346–1351

    Article  CAS  PubMed  Google Scholar 

  • Buanafina MM, Langdon T et al (2006) Manipulating the phenolic acid content and digestibility of Italian ryegrass (Lolium multiflorum) by vacuolar-targeted expression of a fungal ferulic acid esterase. Appl Biochem Biotechnol 129–132:416–426

    PubMed  Google Scholar 

  • Buanafina MM, Langdon T et al (2008) Expression of a fungal ferulic acid esterase increases cell wall digestibility of tall fescue (Festuca arundinacea). Plant Biotechnol J 6:264–280

    Article  CAS  PubMed  Google Scholar 

  • Chigorimbo-Murefu NTL, Riva S, Burton SG (2009) Lipase-catalysed synthesis of esters of ferulic acid with natural compounds and evaluation of their antioxidant properties. J Mol Catal B Enzyme 56:277–282

    Article  CAS  Google Scholar 

  • Constabile A, Klinder A et al (2008) Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr 99:110–120

    Google Scholar 

  • Couteau D, McCartney AL et al (2001) Isolation and characterization of human colonic bacteria able to hydrolyze chlorogenic acid. J Appl Microbiol 90:873–881

    Article  CAS  PubMed  Google Scholar 

  • Crepin VF, Faulds CB, Connerton IF (2004) Functional classification of the microbial feruloyl esterases. Appl Microbiol Biotechnol 63:647–652

    Article  CAS  PubMed  Google Scholar 

  • de Vries RP, Michelsen B et al (1997) The faeA gene from Aspergillus niger and Aspergillus tubingensis encode ferulic acid esterases involved in degradation of complex cell wall polysaccharides. Appl Environ Microbiol 63:4638–4644

    PubMed  Google Scholar 

  • de Vries RP, van Kuyk PA et al (2002) The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds. Biochem J 363:377–386

    Article  PubMed  Google Scholar 

  • Donaghy JA, Bronnenmeier K et al (2000) Purification and characterization of an extracellular feruloyl esterase from the thermophilic anaerobe Clostridium stercorarium. J Appl Microbiol 88:458–466

    Article  CAS  PubMed  Google Scholar 

  • Encina A, Fry SC (2005) Oxidative coupling of a feruloyl-arabinoxylan trisaccharide (FAXX) in the walls of living maize cells requires endogenous hydrogen peroxide and is controlled by a low-Mr apoplastic inhibitor. Planta 223:77–89

    Article  CAS  PubMed  Google Scholar 

  • Faulds CB (2003) Feruloyl esterases: molecular tools to unravel cell structure. Recent Res Devel Appl Microbiol Biotechnol 1:245–275

    CAS  Google Scholar 

  • Faulds CB, Williamson G (1994) Purification and characterization of a ferulic acid esterase (FAE-III) from Aspergillus niger: specificity for the phenolic moiety and binding to microcrystalline cellulose. Microbiol 140:779–787

    Article  CAS  Google Scholar 

  • Faulds CB, Sancho AI, Bartolomé B (2002) Mono- and dimeric ferulic acid release from Brewer’s spent grain by fungal feruloyl esterases. Appl Microbiol Biotechnol 60:489–493

    Article  CAS  PubMed  Google Scholar 

  • Faulds CB, Zanichelli D et al (2003) Specificity of feruloyl esterases for water-extractable and water-unextractable feruloyl polysaccharides: influence of xylanase. J Cereal Sci 38:281–288

    Article  CAS  Google Scholar 

  • Faulds CB, Mandalari G et al (2006) Synergy between xylanases from glycoside hydrolase family 10 and family 11 and a feruloyl esterase in the release of phenolic acids from cereal arabinoxylan. Appl Microbiol Biotechnol 71:622–629

    Article  CAS  PubMed  Google Scholar 

  • Fazary AE, Ju YH (2007) Feruloyl esterases as biotechnological tools: current and future perspectives. Acta Biochim Biophys Sin 39:811–828

    Article  CAS  PubMed  Google Scholar 

  • Fazary AE, Ju YH (2008) The large-scale use of feruloyl esterases in industry. Biotechnol Mol Biol Rev 3:95–110

    Google Scholar 

  • Funk C, Braune A et al (2007) Moderate ferulate and diferulates levels do not impede maize cell wall degradation by human intestinal microbiota. J Agric Food Chem 55:2418–2423

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Conesa MT, Ostergaard P et al (2001) Hydrolysis of diethyl diferulates by a tannase from Aspergillus oryzae. Carbohydr Polym 44:319–324

    Article  CAS  Google Scholar 

  • Glei M, Hofmann T et al (2006) Both wheat (Triticum aestivum) bran arabinoxylans and gut flora-mediated fermentation products protect human colon cells from genotoxic activities of 4-hydroxynonenal and hydrogen peroxide. J Agric Food Chem 54:2088–2095

    Article  CAS  PubMed  Google Scholar 

  • Graf E (1992) Antioxidant potential of ferulic acid. Free Rad Biol Med 13:435–448

    Article  CAS  PubMed  Google Scholar 

  • Hopkins MJ, Englyst HN et al (2003) Degradation of cross-linked and non-cross-linked arabinoxylans by the intestinal microbiota in children. Appl Environ Microbiol 69:6354–6360

    Article  CAS  PubMed  Google Scholar 

  • Humberstone FJ, Briggs DE (2000) Extraction and assay of ferulic acid esterase from malted barley. J Inst Brew 106:21–29

    CAS  Google Scholar 

  • Huntley JF, Newlands GF et al (1985) Histochemical demonstration of chymotrypsin-like serine esterases in mucosal mast cells in four species including man. J Clin Pathol 38:375–384

    Article  CAS  PubMed  Google Scholar 

  • Jones L, Milne JL et al (2003) Cell wall arabinan is essential for guard cell function. Proc Nat Acad Sci (USA) 100:11783–11788

    Article  CAS  Google Scholar 

  • Jones L, Milne JL et al (2005) A conserved functional role of pectic polymers in stomatal guard cells from a range of plant species. Planta 221:255–264

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Nevins DJ (1985) Isolation and identification of O-(5-O-feruloyl-α-L-arabinofuranosyl-(1 → 3)-O-β-D-xylopyranosyl-(1 → 4)-D-xylopyranose as a component of Zea shoot cell-walls. Carbohydr Res 137:139–150

    Article  CAS  Google Scholar 

  • Kern SM, Bennett RN et al (2003) Characterization of metabolites of hydroxycinnamates in the in vitro model of human small intestinal epithelium Caco-2 cells. J Agric Food Chem 51:7884–7891

    Article  CAS  PubMed  Google Scholar 

  • Koseki T, Fushinobu S et al (2009) Occurence, properties, and applications of feruloyl esterases. Appl Microbiol Biotechol 84:803–810

    Article  CAS  Google Scholar 

  • Kosuga M, Kosuga T et al (1998) Topical and cosmetic preparations containing capsaicins, sinapines, or curcumines for secretion stimulation. Eur Pat Appl A2 9 pp CODEN: JKXXAF JP 10120558 A2 19989512

  • Kroon PA, Faulds CB, Williamson G (1996) Purification and characterisation of a novel esterase induced by growth of Aspergillus niger on sugar-beet pulp. Biotechnol Appl Biochem 23:255–262

    CAS  PubMed  Google Scholar 

  • Kroon PA, Faulds CB et al (1997) Release of covalently bound ferulic acid from fiber in the human colon. J Agric Food Chem 45:661–667

    Article  CAS  Google Scholar 

  • Krueger NA, Adesogan AT et al (2008) The potential to increase digestibility of tropical grasses with a fungal, ferulic acid esterase enzyme preparation. Anim Feed Sci Technol 145:95–108

    Article  CAS  Google Scholar 

  • Lafay S, Morand C et al (2006) Absorption and metabolism of caffeic acid and chlorogenic acid in the small intestine of rats. Br J Nutr 96:39–46

    Article  CAS  PubMed  Google Scholar 

  • Laszlo JA, Compton DL et al (2003) Packed-bed bioreactor synthesis of feruloylated monoacyl- and diacylglycerols: clean production of a “green” sunscreen. Green Chem 5:382–386

    Article  CAS  Google Scholar 

  • Laszlo JA, Compton DL, Li XL (2006) Feruloyl esterase hydrolysis and recovery of ferulic acid from jojoba meal. Ind Crops Prod 23:46–53

    Article  CAS  Google Scholar 

  • Levasseur A, Navarro D et al (2005) Construction of engineered bifunctional enzymes and their overproduction in Aspergillus niger for improved enzymatic tools to degrade agricultural by-products. Appl Environ Microbiol 71:8132–8140

    Article  CAS  PubMed  Google Scholar 

  • Levasseur A, Saloheimo M et al (2006) Production of a chimeric enzyme tool associating the Trichoderma reesei swollenin with the Aspergillus niger feruloyl esterase A for release of ferulic acid. Appl Microbiol Biotechnol 73:872–880

    Article  CAS  PubMed  Google Scholar 

  • Lupton JR (1999) Potential protective mechanisms of wheat bran fiber. Am J Med 106:S24–S27

    Article  Google Scholar 

  • Madhavi Latha G, Srinvas P, Muralikrishna G (2007) Purification and characterization of ferulic acid esterase from malted finger millet (Eleusine coracana, Indaf-15). J Agric Food Chem 55:9704–9712

    Article  PubMed  Google Scholar 

  • Mastihubová M, Mastihuba V et al (2006) Commercial enzyme preparations catalyse feruloylation of glycosides. J Mol Catal B Enzym 38:54–57

    Article  Google Scholar 

  • Mateos R, Goya L, Bravo L (2006) Uptake and metabolism of hydroxycinnamic acids (chlorogenic, caffeic, and ferulic acids) by HepG2 cells as a model of the human liver. J Agric Food Chem 54:8724–8732

    Article  CAS  PubMed  Google Scholar 

  • Matthew S, Abraham TE (2004) Ferulic acid: an antioxidant found naturally in plant cell walls and feruloyl esterases involved in its release and its applications. Crit Rev Biotechnol 24:59–83

    Article  Google Scholar 

  • McSweeney CS, Dulieu A et al (1999) Isolation and characterization of a Clostridium sp. with cinnamoyl esterase activity and unusual cell envelope ultrastructure. Arch Microbiol 172:139–149

    Article  CAS  PubMed  Google Scholar 

  • Moreau RA, Hicks KB (2004) The in vitro hydrolysis of phytosterol conjugates in food matrices by mammalian digestive enzymes. Lipids 39:769–776

    CAS  PubMed  Google Scholar 

  • Moussou P, Danaoux L et al (2004) Use of sinapic acid and/or its derivatives for skin protection. Eur Pat Appl 17 pp CODEN;EPXXDW EP 1437117 A1 20040714

  • Nsereko VL, Smiley BK et al (2008) Influence of inoculating forage with lactic acid bacterial strains that produce ferulate esterase on ensilage and ruminal degradation of fiber. Anim Feed Sci Technol 145:122–135

    Article  CAS  Google Scholar 

  • Otto RT, Scheib H et al (2000) Substrate specificity of lipase B from Candida antartica in the synthesis of arylaliphatic glycolipids. J Mol Catal B Enzym 8:201–211

    Article  CAS  Google Scholar 

  • Ou S, Li A, Yang A (2001) A study on synthesis of starch ferulate and its biological properties. Food Chem 74:91–95

    Article  CAS  Google Scholar 

  • Pathak AK, Pathak V et al (2002) Synthesis of an arabinofuranosyl disaccharide photoaffinity probe for arabinosyltransferase activity in Mycobacterium tuberculosis. Bioorg Med Chem Lett 12:2749–2752

    Article  CAS  PubMed  Google Scholar 

  • Pelloux J, Rustercucci C et al (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277

    Article  CAS  PubMed  Google Scholar 

  • Plumb GW, Garcia-Conesa MT et al (1999) Metabolism of chlorogenic acid by human plasma, liver, intestine and gut microflora. J Sci Food Agric 79:390–392

    Article  CAS  Google Scholar 

  • Prates JAM, Tarbouriech N et al (2001) The structure of the feruloyl esterase module of xylanase 10B from Clostridium thermocellum provides insights into substrate recognition. Structure 9:1183–1190

    Article  CAS  PubMed  Google Scholar 

  • Record E, Asther M et al (2003) Overproduction of the Aspergillus niger feruloyl esterase for pulp bleaching applications. Appl Microbiol Biotechnol 62:349–355

    Article  CAS  PubMed  Google Scholar 

  • Sancho AI, Faulds CB et al (1999) Characterisation of feruloyl esterase activity in barley. J Sci Food Sci 79:447–449

    Article  CAS  Google Scholar 

  • Sancho AI, Bartolomé B et al (2001) Release of ferulic acid from cereal residues by barley enzymatic extracts. J Cereal Sci 34:173–179

    Article  CAS  Google Scholar 

  • Schubot FD, Kataeva IA et al (2001) Structural basic for the substrate specificity of the feruloyl esterase domain of the cellulosomal xylanase Z from Clostridium thermocellum. Biochem 40:12524–12532

    Article  CAS  Google Scholar 

  • Selig MJ, Knoshaug EP et al (2008) Synergistic enhancement of cellobiohydrolase performance on pretreated corn stover by addition of xylanase and esterase activities. Biores Technol 99:4997–5005

    Article  CAS  Google Scholar 

  • Shin HD, McClendon S et al (2006) A complex enzymatic recovery of ferulic acid from corn residues with extracellular enzymes from Neosartorya spinosa NRRL185. Biotechnol Bioeng 95:1108–1115

    Article  CAS  PubMed  Google Scholar 

  • Sun A, Faulds CB, Bamforth C (2005) Barley contains two cationic acetylesterases and one anionic feruloyl esterase. Cereal Chem 82:621–625

    Article  CAS  Google Scholar 

  • Tabka MG, Herpoel-Gimbert I et al (2006) Enzymatic saccharification of wheat straw for bioethanol production by a combined cellulase xylanase and feruloyl esterase treatment. Enzyme Microb Technol 39:897–902

    Article  CAS  Google Scholar 

  • Tapin S, Sigoillot JC et al (2006) Feruloyl esterase utilization for simultaneous processing of nonwood plants into phenolic compounds and pulp fibers. J Agric Food Chem 54:3697–3703

    Article  CAS  PubMed  Google Scholar 

  • Topakas E, Stamatis H et al (2003) Purification and characterization of a Fusarium oxysporum feruloyl esterase (FoFae-I) catalysing the transesterification of phenolic acid esters. Enzyme Microb Technol 33:729–737

    Article  CAS  Google Scholar 

  • Topakas E, Vafiadi C, Christakopoulos P (2007) Microbial production, characterization and applications of feruloyl esterases. Process Biochem 42:497–509

    Article  CAS  Google Scholar 

  • Tsuchiyama M, Sakamoto T et al (2006) Esterification of ferulic acid with polyols using a ferulic acid esterase from Aspergillus niger. Biochim Biophys Acta 1760:1071–1079

    CAS  PubMed  Google Scholar 

  • Vafiadi C, Topakas E, Christakopoulos P (2006a) Regioselective esterase catalysed feruloylation of L-arabinose. Carbohydr Res 341:1992–1997

    Article  CAS  PubMed  Google Scholar 

  • Vafiadi C, Topakas E et al (2006b) The feruloyl esterase system of Talaromyces stipitatus: determining the hydrolytic and synthetic specificity of TsFaeC. J Biotechnol 125:210–221

    Article  CAS  PubMed  Google Scholar 

  • Vafiadi C, Topakas E et al (2007) Chemoenzymatic synthesis of feruloyl D-arabinose as a potential anti-mycobacterial agent. Biotechnol Lett 29:1771–1774

    Article  CAS  PubMed  Google Scholar 

  • Vafiadi C, Topakas E et al (2008) Enzymatic synthesis of butyl hydroxycinnamates and their inhibitory effects on LDL-oxidation. J Biotechnol 133:497–504

    CAS  PubMed  Google Scholar 

  • Vafiadi C, Topakas E et al (2009) Feruloyl esterase-catalyzed synthesis of glycerol sinapate using ionic liquids mixtures. J Biotechnol 139:124–129

    Article  CAS  PubMed  Google Scholar 

  • Vanbeneden N, Gils F et al (2007) Variability in the release of free and bound hydroxycinnamic acids from diverse malted barley (Hordeum vulgare L.) cultivars during wort production. J Agric Food Chem 55:11002–11010

    Article  CAS  PubMed  Google Scholar 

  • Vardakou M, Palop Nueno et al (2007) In vitro three-stage continuous fermentation of wheat arabinoxylan fractions and induction of hydrolase activity by the gut microflora. Int J Biol Macromol 41:584–589

    Article  CAS  PubMed  Google Scholar 

  • Walton NJ, Narbad A et al (2000) Novel approaches to the biosynthesis of vanillin. Curr Opin Biotechnol 11:490–496

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Geng X et al (2004) Purification and characterization of a feruloyl esterase from the intestinal bacterium Lactobacillus acidophilus. Appl Environ Microbiol 70:2367–2372

    Article  CAS  PubMed  Google Scholar 

  • Warner K, Laszlo JA (2005) Addition of ferulic acid, ethyl ferulate, and feruloylated monoacyl- and diacylglycerols to salad oils and frying oils. J Am Oil Chem Soc 82:647–652

    Article  CAS  Google Scholar 

  • Williamson G, Kroon PA, Faulds CB (1998) Hairy plant polysaccharides: a close shave with microbial esterases. Microbiol 144:2011–2023

    Article  CAS  Google Scholar 

  • Williamson G, Day AJ et al (2000) Human metabolic pathways of dietary flavonoids and cinnamates. Biochem Soc Trans 28:16–22

    CAS  PubMed  Google Scholar 

  • Wong DW (2006) Feruloyl esterase: a key enzyme in biomass degradation. Appl Biochem Biophys 133:87–112

    CAS  Google Scholar 

  • Yoshida-Shimokawa T, Yoshida S et al (2001) Enzymatic feruloylation of arabinoxylan-trisaccharide by feruloyl-CoA:arabinoxylan-trisaccharide O-hydroxylcinnamoyl transferase from Oryza sativa. Planta 212:470–474

    Article  CAS  PubMed  Google Scholar 

  • Yu P, McKinnon JJ et al (2003) Enzymic release of reducing sugars from oat hulls by cellulase, as influenced by Aspergillus ferulic acid esterase and Trichoderma xylanase. J Agric Food Chem 51:218–223

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The Biotechnology and Biological Sciences Research Council (BBSRC), UK, is kindly thanked for financial support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Craig B. Faulds.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Faulds, C.B. What can feruloyl esterases do for us?. Phytochem Rev 9, 121–132 (2010). https://doi.org/10.1007/s11101-009-9156-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11101-009-9156-2

Keywords

Navigation