Skip to main content

Advertisement

SpringerLink
Log in

Biotechnological potential of pectinolytic complexes of fungi

  • Review
  • Published:
Biotechnology Letters Aims and scope Submit manuscript

Abstract

Plant cell wall-degrading enzymes, such as cellulases, hemicellulases and pectinases, have been extensively studied because of their well documented biotechnological potential, mainly in the food industry. In particular, lytic enzymes from filamentous fungi have been the subject of a vast number of studies due both to their advantages as models for enzyme production and their characteristics. The demand for such enzymes is rapidly increasing, as are the efforts to improve their production and to implement their use in several industrial processes, with the goal of making them more efficient and environment-friendly. The present review focuses mainly on pectinolytic enzymes of filamentous fungi, which are responsible for degradation of pectin, one of the major components of the plant cell wall. Also discussed are the past and current strategies for the production of cell wall-degrading enzymes and their present applications in a number of biotechnological areas.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Acosta-Rodríguez I, Piñón-Escobedo C, Zavala-Páramo MG, López-Romero E, Cano-Camacho H (2005) Degradation of cellulose by the bean-pathogenic fungus Colletotrichum lindemuthianum. Production of extracellular cellulolytic enzymes by cellulose induction. Antonie van Leeuwenhoek 87:301–310

    Article  PubMed  Google Scholar 

  • Amorim HV, Amorim VL (1977) Coffee enzymes and coffee quality. In: Ori R, Angelo A (eds) Enzymes in food and beverage processing, vol 47. ACS Symposium Series, Washington, pp 27–56

    Chapter  Google Scholar 

  • Angelova M, Sheremetska P, Lekov M (1998) Enhanced polymethylgalacturonase production from Aspergillus niger 26 by calcium alginate immobilization. Proc Biochem 33:299–305

    Article  CAS  Google Scholar 

  • Aro N, Pakula T, Penttilä M (2005) Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 29:719–739

    Article  PubMed  CAS  Google Scholar 

  • Bajpai P (1999) Application of enzymes in the pulp and paper industry. Biotechnol Prog 15:147–157

    Article  PubMed  CAS  Google Scholar 

  • Barazarte H, Sangronis E, Unai E (2008) La cáscara de cacao (Theobroma cacao L): una posible fuente comercial de pectinas. Arch Latinoam Nutr 58:64–70

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Beldman G, Broek LAM, Schols HA, Leeuwen MJF, Laere KMJ, Voragen AGJ (1996) An exogalacturonase from Aspergillus aculeatus able to degrade xylogalacturonan. Biotechnol Lett 18:707–712

    Article  CAS  Google Scholar 

  • Benen JA, Visser J (2003) Polygalacturonases. In: Whitaker J, Voragen A, Wong D (eds) Handbook of food enzymology. Marcel Gekker Inc, New York, pp 857–866

    Google Scholar 

  • Benen JA, Kester HC, Parenicová L, Visser J (2000) Characterization of Aspergillus niger pectate lyase A. Biochemistry 39:15563–15569

    Article  PubMed  CAS  Google Scholar 

  • Bhat MK (2000) Cellulases and related enzymes in biotechnology. Biotechnol Adv 18:355–383

    Article  PubMed  CAS  Google Scholar 

  • Boccas F, Roussos S, Gutierrez M, Serrano L, Viniegra G (1994) Production of pectinase from coffee pulp in solid state fermentation system: selection of wild fungal isolate of high potency by a simple three-step screening technique. J Food Sci Technol 31:22–26

    CAS  Google Scholar 

  • Brady D, Jordaan J (2009) Advances in enzyme immobilization. Biotechnol Lett 31:1639–1650

    Article  PubMed  CAS  Google Scholar 

  • Cardoso PG, Ribeiro JB, Teixeira JA, Queiroz MV, Araújo EF (2007) Overexpression of the plg1 gene encoding pectin lyase in Penicillium griseoroseum. J Ind Microbiol Biotechnol 35:159–166

    Article  PubMed  Google Scholar 

  • Castilho LR, Medronho RA, Alves TLM (2000) Production and extraction of pectinases obtained by solid state fermentation of agroindustrial residues with Aspergillus niger. Bioresour Technol 71:45–50

    Article  CAS  Google Scholar 

  • Chen Z, Franco CF, Baptista RP, Cabral JMS, Coelho AV, Rodrigues CJ, Melo EP (2006) Purification and identification of cutinases from Colletotrichum kahawae and Colletotrichum gloeosporioides. Appl Microbiol Biotechnol 73:1306–1313

    Article  PubMed  Google Scholar 

  • Coenen G, Bakx E, Verhoef R, Schols H, Voragen A (2007) Identification of the connecting linkage between homo- or xylogalacturonan and rhamnogalacturonan type I. Carbohydr Polym 70:224–235

    Article  CAS  Google Scholar 

  • D′Addosio R, Páez G, Marín M, Mármol Z, Ferrer J (2005) Obtención y caracterización de pectina a partir de la cáscara de parchita (Pasiflora edulis F. flavicarpa Degener). Rev Fac Agron 22:240–249

    Google Scholar 

  • de Vries RP (2003) Regulation of Aspergillus genes encoding plant cell wall polysaccharide-degrading enzymes; relevance for industrial production. Appl Microbiol Biotechnol 61:10–20

    PubMed  Google Scholar 

  • de Vries RP, Visser J (2001) Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev 65:497–522

    Article  PubMed  Google Scholar 

  • de Vries RP, Flipphi MJ, Witteveen CF, Visser J (1994) Characterization of an Aspergillus nidulans l-arabitol dehydrogenase mutant. FEMS Microbiol Lett 123:83–90

    Article  PubMed  Google Scholar 

  • de Vries RP, Kester HC, Poulsen CH, Benen JA, Visser J (2000) Synergy between enzymes from Aspergillus involved in the degradation of plant cell wall polysaccharides. Carbohydr Res 327:401–410

    Article  PubMed  Google Scholar 

  • de Vries RP, Jansen J, Aguilar G, Parenicova L, Joosten V, Wulfert F, Benen JA, Visser J (2002) Expression profiling of pectinolytic genes from Aspergillus niger. FEBS Lett 530:41–47

    Article  PubMed  Google Scholar 

  • de Vries RP, van Grieken C, van Kuyk PA, Wösten HA (2005) The value of genome sequences in the rapid identification of novel genes encoding specific plant cell wall degrading enzymes. Curr Genomics 6:157–187

    Article  Google Scholar 

  • Delattre C, Michaud P, Vijayalakshmi MA (2008) New monolithic enzymatic micro-reactor for the fast production and purification of oligogalacturonides. J Chromatogr B 861:203–208

    Article  CAS  Google Scholar 

  • Diano N, Grimaldi T, Bianco M, Rossi S, Gabrovska K, Yordanova G, Godjevargova T, Grano V, Nicolucci C, Mita L, Bencivenga U, Canciglia P, Mita DG (2008) Apple juice clarification by immobilized pectolytic enzymes in packed or fluidized bed reactors. J Agric Food Chem 56:11471–11477

    Article  PubMed  CAS  Google Scholar 

  • Faulds CB, De Vries RP, Kroon PA, Visser J, Williamson G (1997) Influence of ferulic acid on the production of feruloyl esterases by Aspergillus niger. FEMS Microbiol Lett 157:239–244

    Article  PubMed  CAS  Google Scholar 

  • Freixo MR, Karmali A, Arteiro JM (2008) Production and chromatographic behaviour of polygalacturonase from Pleurotus ostreatus on immobilized metal chelates. Proc Biochem 43:531–539

    Article  CAS  Google Scholar 

  • Guetsky R, Kobiler I, Wang X, Perlman N, Gollop N, Avila-Quezada G, Hadar I, Prusky D (2005) Metabolism of the flavonoid epicatechin by laccase of Colletotrichum gloeosporioides and its effect on pathogenicity on avocado fruits. Phytopathology 95:1341–1348

    Article  PubMed  CAS  Google Scholar 

  • Hadj-Taieb N, Ayadi M, Trigui S, Bouabdallah F, Gargouri A (2002) Hyperproduction of pectinase activities by a fully constitutive mutant (CT1) of Penicillium occitanis. Enzyme Microb Technol 30:662–666

    Article  CAS  Google Scholar 

  • Hang YD, Woodams EE (1994) Production of fungal polygalacturonase from apple pomace. Lebenson Wiss Technol 27:194–196

    Article  CAS  Google Scholar 

  • Hernández-Silva L, Piñon-Escobedo C, Cano-Camacho H, Zavala-Páramo M, Acosta-Rodríguez I, López-Romero E (2007) Comparison of fungal growth and production of extracellular pectin lyase activity by pathogenic and non-pathogenic races of Colletotrichum lindemuthianum cultivated under different conditions. Physiol Mol Plant Pathol 70:88–95

    Article  Google Scholar 

  • Herron SR, Benen JA, Scavetta RD, Visser J, Jurnak F (2000) Structure and function of pectic enzymes: virulence factors of plant pathogens. Proc Natl Acad Sci USA 97:8762–8769

    Article  PubMed  CAS  Google Scholar 

  • Hoondal G, Tiwari R, Tewari R, Dahiya N, Beg Q (2002) Microbial alkaline pectinases and their industrial applications: a review. Appl Microbiol Biotechnol 59:409–418

    Article  PubMed  CAS  Google Scholar 

  • Jayani RS, Saxena S, Gupta R (2005) Microbial pectinolytic enzymes: a review. Process Biochem 40:2931–2944

    Article  CAS  Google Scholar 

  • Jeoh T, Michener W, Himmel ME, Decker SR, Adney WS (2008) Implications of cellobiohydrolase glycosylation for use in biomass conversion. Biotechnol Biofuels 1:1–12

    Article  Google Scholar 

  • Kashyap DR, Vohra PK, Chopra S, Tewari R (2001) Applications of pectinases in the commercial sector: a review. Bioresour Technol 77:215–227

    Article  PubMed  CAS  Google Scholar 

  • Kitamoto N, Yoshino-Yasuda S, Ohmiya K, Tsukagoshi N (2001a) Sequence analysis and overexpression of a pectin lyase gene (pel1) from Aspergillus oryzae KBN616. Biosci Biotechnol Biochem 65:209–212

    Article  PubMed  CAS  Google Scholar 

  • Kitamoto N, Yoshino-Yasuda S, Ohmiya K, Tsukagoshi N (2001b) A second pectin lyase gene (pel2) from Aspergillus oryzae KBN616: its sequence analysis and overexpression, and characterization of the gene products. J Biosci Bioeng 91:378–381

    Article  PubMed  CAS  Google Scholar 

  • Koubala BB, Mbome LI, Kansci G, Tchouanguep MF, Crepeau MJ, Thibault JF, Ralet MC (2008) Physicochemical properties of pectins from ambarella peels (Spondias cytherea) obtained using different extraction conditions. Food Chem 106:1202–1207

    Article  CAS  Google Scholar 

  • Kourkoutas Y, Bekatorou A, Banat IM, Marchant R, Koutinas AA (2004) Immobilization technologies and support materials suitable in alcohol beverages production: a review. Food Microbiol 21:377–397

    Article  CAS  Google Scholar 

  • Krause DR, Christopher J, Wood J, Maclean DJ (1991) Glucoamylase (exo-1, 4-α-d-glucan glucanohydrolase, EC 3.2.1.3) is the major starch-degrading enzyme secreted by the phytopathogenic fungus Colletotrichum gloeosporioides. J Gen Microbiol 137:2463–2468

    CAS  Google Scholar 

  • Kuroda K, Ueda M (2010) Cell surface engineering of yeast for applications in white biotechnology. Biotechnol Lett 33(1):1–9

    Article  PubMed  Google Scholar 

  • MacCabe AP, Orejas M, Tamayo EN, Villanueva A, Ramon D (2002) Improving extracellular production of food-use enzymes from Aspergillus nidulans. J Biotechnol 96:43–54

    Article  PubMed  CAS  Google Scholar 

  • Mamma D, Kourtoglou E, Christakopoulos P (2008) Fungal multienzyme production on industrial by-products of the citrus-processing industry. Bioresour Technol 99:2373–2383

    Article  PubMed  CAS  Google Scholar 

  • Mantovani CF, Geimba MP, Brandelli A (2005) Enzymatic clarification of fruit juices by fungal pectin lyase. Food Biotechnol 19:173–181

    Article  CAS  Google Scholar 

  • Martens-Uzunova ES, Schaap PJ (2009) Assessment of the pectin degrading enzyme network of Aspergillus niger by functional genomics. Fungal Genet Biol 46:S170–S179

    Article  PubMed  CAS  Google Scholar 

  • Martens-Uzunova ES, Zandleven JS, Benen JA, Awad H, Kools HJ, Beldman G, Voragen AG, Van Den Berg JA, Schaap PJ (2006) A new group of exo-acting family 28 glycoside hydrolases of Aspergillus niger that are involved in pectin degradation. Biochem J 400:43

    Article  PubMed  CAS  Google Scholar 

  • Martin N, Souza S, Silva R, Gomes E (2004) Pectinase production by fungal strains in solid-state fermentation using agro-industrial bioproduct. Braz Arch Biol Technol 47:813–819

    Article  CAS  Google Scholar 

  • Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto A, Chang K (1992) Extraction and physicochemical characterization of pectin from sunflower head residues. J Food Sci 57:1439–1443

    Article  CAS  Google Scholar 

  • Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277

    Article  PubMed  CAS  Google Scholar 

  • Neustroev KN, Krylov AS, Firsov LM, Abroskina OL, Khorlin AY (1991) Isolation and properties of β-mannosidase from Aspergillus awamori. Biokhimiya 56:1406–1412

    CAS  Google Scholar 

  • Nevalainen KMH, Te’o VSJ, Bergquist PL (2005) Heterologous protein expression in filamentous fungi. Trends Biotechnol 23:468–474

    Article  PubMed  CAS  Google Scholar 

  • Nighojkar S, Phanse Y, Sinha D, Nighojkar A, Kumar A (2006) Production of polygalacturonase by immobilized cells of Aspergillus niger using orange peel as inducer. Process Biochem 41:1136–1140

    Article  CAS  Google Scholar 

  • Pagán J, Ibarz A, Llorca M, Pagán A, Barbosa-Cánovas G (2001) Extraction and characterization of pectin from stored peach pomace. Food Res Int 34:605–612

    Article  Google Scholar 

  • Pařenicová L, Benen JA, Kester HC, Visser J (2000) pgaA and pgaB encode two constitutively expressed endopolygalacturonases of Aspergillus niger. Biochem J 345:637–644

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ralet MC, Crépeau MJ, Buchholt HC, Thibault JF (2003) Polyelectrolyte behaviour and calcium binding properties of sugar beet pectins differing in their degrees of methylation and acetylation. Biochem Eng J 16:191–201

    Article  CAS  Google Scholar 

  • Ramos AM, Gally M, Garcia MC, Levin L (2010) Pectinolytic enzyme production by Colletotrichum truncatum, causal agent of soybean anthracnose. Rev Iberoam Micol doi:10.1016/j.riam.2010.06.002

  • Singh P (1968) Amylase and polyphenol oxidase production by germinating conidia of Colletotrichum falcatum Went. Cell Mol Life Sci 24:117–118

    Article  CAS  Google Scholar 

  • Solís S, Loeza J, Segura G, Tello J, Reyes N, Lappe P, Guitérrez L, Ríos F, Huitrún C (2009) Hydrolysis of orange peel by a pectin lyase-overproducing hybrid obtained by protoplast fusion between mutant pectinolytic Aspergillus flavipes and Aspergillus niveus CH-Y-1043. Enzyme Microb Technol 44:123–128

    Article  Google Scholar 

  • Spagna G, Pifferi PG, Gilioli E (1995) Immobilization of a pectinlyase from Aspergillus niger for application in food technology. Enzyme Microb Technol 17:729–738

    Article  CAS  Google Scholar 

  • Spagnuolo M, Crecchio C, Pizzigallo MDR, Ruggiero P (1997) Synergistic effects of cellulolytic and pectinolytic enzymes in degrading sugar beet pulp. Bioresour Technol 60:215–222

    Article  CAS  Google Scholar 

  • Tanabe H, Kobayashi Y, Akamatsu I (1986) Pretreatment of pectic wastewater from orange canning by soft-rot Erwinia corotovora. J Ferment Technol 64:265–268

    Article  CAS  Google Scholar 

  • Templeton MD, Sharrock KR, Bowen JK, Crowhurst RN, Rikkerink EH (1994) The pectin lyase-encoding gene (pnl) family from Glomerella cingulata: characterization of pnlA and its expression in yeast. Gene 142:141–146

    Article  PubMed  CAS  Google Scholar 

  • Vaillant F, Millan A, Millan P, Dornier M, Decloux M, Reynes M (2000) Co-immobilized pectin lyase and endocellulase on chitin and nylon supports. Process Biochem 35:989–996

    Article  CAS  Google Scholar 

  • Van der Veen P, Flipphi MJ, Voragen AG, Visser J (1993) Induction of extracellular arabinases on monomeric substrates in Aspergillus niger. Arch Microbiol 159:66–71

    Article  PubMed  Google Scholar 

  • Van der Vlugt-Bergmans CJB, Meeuwsen PJA, Voragen AGJ, Van Ooyen AJJ (2000) Endo-xylogalacturonan hydrolase, a novel pectinolytic enzyme. Appl Environ Microbiol 66:36–41

    Article  PubMed  Google Scholar 

  • Viniegra-González G, Favela-Torres E, Aguilar CN, Rómero-Gomez SJ, Díaz-Godínez G, Augur C (2003) Advantages of fungal enzyme production in solid state over liquid fermentation systems. Biochem Eng J 13:157–167

    Article  Google Scholar 

  • Voragen AGJ, Beldman G, Schols H (2001) Chemistry and enzymology of pectins. In: McCleary B, Prosky L (eds) Advanced dietary fibre technology. Blackwell Science, Oxford, pp 379–397

    Google Scholar 

  • Wei Y, Shih J, Li J, Goodwin PH (2002) Two pectin lyase genes, pnl-1 and pnl-2, from Colletotrichum gloeosporioides f. sp. malvae differ in a cellulose-binding domain and in their expression during infection of Malva pusilla. Microbiology 148:2149–2157

    PubMed  CAS  Google Scholar 

  • Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  PubMed  CAS  Google Scholar 

  • Willats WG, Knox JP, Mikkelsen JD (2006) Pectin: new insights into an old polymer are starting to gel. Trends Food Sci Tech 17:97–104

    Article  CAS  Google Scholar 

  • Wu MC, Jiang CM, Huang PH, Wu MY, Wang YT (2007) Separation and utilization of pectin lyase from commercial pectic enzyme via highly methoxylated cross-linked alcohol-insoluble solid chromatography for wine methanol reduction. J Agric Food Chem 55:1557–1562

    Article  PubMed  CAS  Google Scholar 

  • Yapo BM, Robert C, Etienne I, Wathelet B, Paquot M (2007) Effect of extraction conditions on the yield, purity and surface properties of sugar beet pulp pectin extracts. Food Chem 100:1356–1364

    Article  CAS  Google Scholar 

  • Yoon SH, Kim SK, Kim JF (2010) Secretory production of recombinant proteins in Escherichia coli. Recent Pat Biotechnol 4:23–29

    Article  PubMed  CAS  Google Scholar 

  • Zhao QX, Yuan S, Zhang YL (2007) Expression of pectin lyase 1 from Aspergillus oryzae in Escherichia coli. Sheng Wu Gong Cheng Xue Bao 23:873–877

    PubMed  CAS  Google Scholar 

  • Zheng Z, Shetty K (2000) Solid state production of polygalacturonase by Lentinus edodes using fruit processing wastes. Process Biochem 35:825–830

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centro Multidisciplinario de Estudios en Biotecnología, Universidad Michoacana de San Nicolás de Hidalgo, Apartado Postal No. 53, Administración Chapultepec, 262, Morelia, Mich, México

    Alicia Lara-Márquez, María G. Zavala-Páramo & Horacio Cano Camacho

  2. División de Ciencias Naturales y Exactas, Departamento de Biología, Universidad de Guanajuato, Apartado Postal No. 187, 36000, Guanajuato, Gto, México

    Everardo López-Romero

Authors
  1. Alicia Lara-Márquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María G. Zavala-Páramo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Everardo López-Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Horacio Cano Camacho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Horacio Cano Camacho.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lara-Márquez, A., Zavala-Páramo, M.G., López-Romero, E. et al. Biotechnological potential of pectinolytic complexes of fungi. Biotechnol Lett 33, 859–868 (2011). https://doi.org/10.1007/s10529-011-0520-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10529-011-0520-0

Keywords

Search

Navigation