Monitoring the cell wall characteristics of degraded beech wood by white-rot fungi: Anatomical, chemical, and photochemical study
Keywords:
Carbohydrate degradation, cell wall decomposition, FT-IR, Oriental beech wood, simultaneous white-rot, wood chemistry, wood decayAbstract
Meticulous chemical analysis of decaying xylem and linking it to corresponding anatomical modification at the cellular level can improve our understanding of the decay process. The aim of this study was to monitor the histological, chemical, photochemical, and progression of wood degradation by two white-rot fungi at different intervals. Oriental beech wood (Fagus orientalis) blocks were exposed to Pleurotus ostreatus and Trametes versicolor to investigate the degradation capabilities of these two fungi. Light microscopy was used to study the decay patterns in wood. Decayed wood samples were also analyzed to determine lignin, cellulose and sugar contents and also evaluated at two week intervals by FT-IR spectroscopy to study chemical alterations. According to chemical analyses lignin is the most degraded polymer followed by cellulose and hemicelluloses for both white rot fungi. However, both test fungi tended to consume lignin more than cellulose. FT-IR spectra changes for lignin and carbohydrates in beech wood supported chemical alteration and indicated that both fungi decay wood in a simultaneous pattern.
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References
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Baldrian, P; 2008. Enzymes of saprotrophic basidiomycetes. In: Boddy, L., Frankland, J.C; Van West, P. (Eds.), Ecology of Saprotrophic Basidiomycetes. Academic Press, Elsevier, London: pp. 19-41.
Bari, E. 2014. Potential of biological degradation of oriental beech wood by the white-rot fungus Pleurotus ostreatus and the effects on mechanical and chemical properties there of and its comparison with standard the white-rot fungus Trametes versicolor. Dissertation, Sari Agriculture and Natural Resources University, Sari, Iran.
Bari, E.; Nazarnezhad N, Kazemi SM, Tajick Ghanbary MA, Mohebby B, Schmidt O Clausen CA. 2015a. Comparison of degradation capabilities of the white rot fungi Pleurotus ostreatus and Trametes versicolor. Int. Biodeterior. Biodegr 104: 231–237.
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Bari, E.; Schmidt, O.; Oladi, R. 2015c. A histological investigation of Oriental beech wood decayed by Pleurotus ostreatus and Trametes versicolor. For. Pathol. 45: 349–357.
Bari, E.; Taghiyari, H.R.; Mohebby, B.; Clausen, C.A.; Schmidt, O.; Vaseghi, M.J. 2015d. Mechanical properties and chemical composition of beech wood exposed for 30 and 120 days to white-rot fungi. Holzforschung 69: 587–593.
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Bari, E; Karim, M.; Oladi, R.; Tajick Ghanbary, MA.; Ghodskhah Daryaei, M.; Schmidt, O.; Benz, J.P.; Emaminasab, M. 2017. The white-rot fungus Pleurotus ostreatus causes simultaneous decay in Oak trees in vivo. For Pathol DOI: 10.1111/efp.12338.
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Blanchette, R.A. 1995. Degradation of the lignocellulose complex in wood. Can. J. Bot. 73[Suppl 1], S999–S1010.
Bouslimi, B.; Koubaa, A.; Bergeron, Y. 2014. Effects of biodegradation by brown-rot decay on selected wood properties in eastern white cedar (Thuja occidentalis L.). Int. Biodeterior. Biodegrad: 87, 87-98.
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Carrillo, F.; Colom, X.; Sunõl, J.J.; Saurina, J. 2004. Structural FTIR analysis and thermal characterisation of lyocell and viscose-type fibres. Eur Polym J 40: 2229-2234.
Colom, X.; Carrillo, F.; Nogues, F.; Garriga, O. 2003. Structural analysis of photodegraded wood by means of FTIR spectroscopy. Polym Degrad Stabil 80: 543-549.
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Fackler, K.; Stevanic, J.S.; Ters, T.; Hinterstoisser, B.; Schwanninger, M.; Salmen, L. 2011. FT-IR imaging microscopy to localise and characterize simultaneous and selective white-rot decay within spruce wood cells. Holzforschung 65: 411-420.
Gärtner, H.; Schweingruber, F.H., 2013. Microscopic preparation techniques for plant stem analysis. Kessel, Remagen.
Hale, MDC.; Eaton, RA. 1985a. Oscillatory growth of fungal hyphae in wood cell walls. Trans. Br. Mycol. Soc. 84: 277-288.
Hale, MDC.; Eaton, RA. 1985b. The ultrastructure of soft-rot fungi. II. Cavity forming hyphae in wood cell walls. Mycologia 77: 594-605.
Harrington, K.J., Higgins, H.G., Michell, A.J., 1964. Infrared spectra of Eucalypus regnans F. Muell. and Pinus radiata D.Don. Holzforschung 18: 108–113.
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Hatakka A., Hammel K.E., 2010. Fungal Biodegradation of Lignocelluloses. In: HOFRICHTER M (Ed) The Mycota. 2nd ed. Springer, Berlin, Heidelberg, New York, pp: 319–340.
Hervé, V., Mothe, F., Freyburger, C., Gelhaye, E., Frey-Klett, P. 2014. Density mapping of decaying wood using X-ray computed tomography. Int. Biodeterior. Biodegrad 86: 358-363.
Hinterstoisser, B.; Salmen, L. 2000. Application of dynamic 2D FTIR to cellulose. Vib Spectros 22: 111–118.
Karim, M.; Ghodskhah Daryaei, M.; Torkaman, J.; Oladi, R.; Tajick Ghanbary, M.A.; Bari, E. 2016. In vivo investigation of chemical alteration in Oak wood decayed by Pleurotus ostreatus. Int Biodeterior Biodegrad 108: 127-132.
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Kim, J.S.; Gao, J.; Daniel, G. 2015. Cytochemical and immunocytochemical characterization of wood decayed by the white rot fungus Pycnoporus sanguineus I. preferential lignin degradation prior to hemicelluloses in Norway spruce wood. Int Biodeterior Biodegrad 105: 30-40.
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Kondo, T. 1997. The assignment of IR absorption bands due to free hydroxyl groups in cellulose. Cellulose 4: 281-292.
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Kubicek, C.P. 2013. Fungi and lignocellulosic biomass. John Wiley & Sons, Inc, Chichester.
Liers, C.; Ullrich, R.; Steffen, K,T.; Hatakka, A.; Hofrichter, M. 2006. Mineralization of 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Appl. Microbiol. Biotechnol 69: 573–579.
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Mann, J.; Marrinan, H.J. 1956. The reaction between cellulose and heavy water. Part 3.-A quantitative study by infra-red spectroscopy. Trans Faraday Soc 52:492-497.
Martinez, A.T; Camarero, S.; Gutiérrez, A.; Bochini, P.; Galleti, G.C .2001. Studies on wheat lignin degradation by Pleurotus species using analytical pyrolysis. Journal of Analytical and Applied Pyrolysis 58–59: 401–411.
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Mohebby, B. 2005. Attenuated total reflection infrared spectroscopy of white-rot decayed beech wood. Int. Biodeterior. Biodegrad 55, 247–251.
Nagadesi, P.; Arya, A.; Albert, S. 2013. Delignification pattern of wood decay by white rot fungi in teak (Tectona grandis L. f.). J Indian Acad Wood Sci 10: 1-8.
O’Sullivan ,A.C. 1997. Cellulose: the structure slowly unravels. Cellulose 4: 173–207.
Ouis, D. 2000. Detection of decay in logs through measuring the damping of bending vibrations by means of a room acoustical technique. Wood Sci Technol 34: 221–236.
Pandey, K.K; Pitman, A.J .2003. FTIR studies of the changes in wood following decay by brown-rot and white-rot fungi. Int Biodeterior Biodegr 52: 151–160.
Pandey, K.K.; Theagarajan, K.S. 1997. Analysis of wood surfaces by diffuse reflectance (DRIFT) and photoacoustic (PAS) Fourier transform infrared spectroscopic techniques. Holz alas Roh- und Werkstoff 55: 383–390.
Popescu, C.M.; Popescu, M.C.; Singurel, G.; Vastile, C.; Argyropoulos, D.; Willfor, S. 2007. Spectral characterization of eucalyptus wood. Appl. Spectr 61: 1168-1177.
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Schmidt, O.; Bahmani, M.; Koch, G.; Potsch, T.; Brandt, K. 2016. Study of the fungal decay of oil palm wood using TEM and UV techniques. Int. Biodeterior. Biodegrad 111: 37-44.
Schmidt, O.; Gaiser, O.; Dujesiefken, D. 2012. Molecular identification of decay fungi in the wood of urban trees. Eur J Forest Res 131: 885–891.
Schubert, M.; Volkmer, T.; Lehringer, C.; Schwarze, F.W.M.R. 2011. Resistance of bioincised wood treated with wood preservatives to blue-stain and wood-decay fungi. Int Biodeterior Biodegrad 65: 108-115.
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Schwanninger, M.; Rodrigues, J.C.; Pereira, H.; Hinterstoisser, B. 2004. Effects of short-time vibratory ball milling on the shape of FT-IR spectra of wood and cellulose. Vib Spectros 36: 23–40.
Schwarze, F.W.M.R.; Engels, J.; Matthek, C. 2004. Fungal strategies of wood decay in trees. 2nd ed. Springer, Berlin, Heidelberg, New York.
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Sugiyama, J.; Persson, J.; Chanzy, H. 1991. Combined infrared and electron diffraction study of the polymorphism of native celluloses. Macromolecules 24: 2461–2466.
Sweet, M.; Winandy, J.E. 1999. Influence of degree of polymerization of cellulose and hemicellulose on strength loss in fire-retardant-treated southern pine. Holzforschung 53: 311–317.
TAPPI standard. 1998. Standard methods for acid-insoluble lignin in wood and pulp, T 222. om-98.
TAPPI standard. 1992. Standard methods for Carbohydrate composition of extractive-free wood and wood pulp by gas-liquid chromatography. Standard T249 cm–85.
TAPPI standard. 1997. Cellulose in wood. Standard T17 wd–97.
Timell, T.E. 1967. Recent progress in the chemistry of wood hemicelluloses. Wood Sci Technol 1: 45–70.
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Anagnost, S.E. 1998. Light microscopic diagnosis of wood decay. IAWA J 19: 141–167.
Argyropoulos, D.S; Menachem, S.B. 1997. Lignin. Adv. Biochem. Eng. Biotechnol 57: 127–158.
Baldrian, P; 2008. Enzymes of saprotrophic basidiomycetes. In: Boddy, L., Frankland, J.C; Van West, P. (Eds.), Ecology of Saprotrophic Basidiomycetes. Academic Press, Elsevier, London: pp. 19-41.
Bari, E. 2014. Potential of biological degradation of oriental beech wood by the white-rot fungus Pleurotus ostreatus and the effects on mechanical and chemical properties there of and its comparison with standard the white-rot fungus Trametes versicolor. Dissertation, Sari Agriculture and Natural Resources University, Sari, Iran.
Bari, E.; Nazarnezhad N, Kazemi SM, Tajick Ghanbary MA, Mohebby B, Schmidt O Clausen CA. 2015a. Comparison of degradation capabilities of the white rot fungi Pleurotus ostreatus and Trametes versicolor. Int. Biodeterior. Biodegr 104: 231–237.
Bari, E.; Oladi, R.; Schmidt, O.; Clausen, C.A.; Ohno, K.; Nicholas, D.D.; Ghodskhah Daryaei, M.; Karim, M. 2015b. Influence of xylem ray integrity and degree of polymerization on bending strength of beech wood decayed by Pleurotus ostreatus and Trametes versicolor. Int. Biodeterior. Biodegr 104: 299–306.
Bari, E.; Schmidt, O.; Oladi, R. 2015c. A histological investigation of Oriental beech wood decayed by Pleurotus ostreatus and Trametes versicolor. For. Pathol. 45: 349–357.
Bari, E.; Taghiyari, H.R.; Mohebby, B.; Clausen, C.A.; Schmidt, O.; Vaseghi, M.J. 2015d. Mechanical properties and chemical composition of beech wood exposed for 30 and 120 days to white-rot fungi. Holzforschung 69: 587–593.
Bari, E; Taghiyari, H.R.; Naji, H.R; Schmidt, O.; Ohno, M.K.; Clausen, C.A.; Bakar, E.S. 2016: Assessing the destructive behavior of two white-rot fungi on beech wood. Int. Biodeterior. Biodegr 114: 129-140.
Bari, E; Karim, M.; Oladi, R.; Tajick Ghanbary, MA.; Ghodskhah Daryaei, M.; Schmidt, O.; Benz, J.P.; Emaminasab, M. 2017. The white-rot fungus Pleurotus ostreatus causes simultaneous decay in Oak trees in vivo. For Pathol DOI: 10.1111/efp.12338.
Bellamy, L.J. 1975. The Infrared Spectra of Complex Molecules. Chapman and Hall/London: 299p
Blanchette, R.A. 1995. Degradation of the lignocellulose complex in wood. Can. J. Bot. 73[Suppl 1], S999–S1010.
Bouslimi, B.; Koubaa, A.; Bergeron, Y. 2014. Effects of biodegradation by brown-rot decay on selected wood properties in eastern white cedar (Thuja occidentalis L.). Int. Biodeterior. Biodegrad: 87, 87-98.
Bravery, A.F. 1978. Screening techniques for potential wood preservative Chemicals. IRG/WP 2113.
Carrillo, F.; Colom, X.; Sunõl, J.J.; Saurina, J. 2004. Structural FTIR analysis and thermal characterisation of lyocell and viscose-type fibres. Eur Polym J 40: 2229-2234.
Colom, X.; Carrillo, F.; Nogues, F.; Garriga, O. 2003. Structural analysis of photodegraded wood by means of FTIR spectroscopy. Polym Degrad Stabil 80: 543-549.
Cowling, E.B. 1961. Comparative biochemistry of the decay of sweetgum sapwood by white-rot and brown-rot fungi. Technical Bulletin–1258. USDA Forest Service, Washington, DC.
Curling, S.F.; Clausen, C.A.; Winandy, J.E. 2002. Relationships between mechanical properties, weight loss, and chemical composition of wood during incipient brown-rot decay. Forest Product Journal 52: 34–39.
Davis, M.W. 1998. A rapid modified method for compositional carbohydrate analysis of lignocellulosics by high pH anion-exchange chromatography with pulsed amperometric detection (HPAEC/PAD). J Wood Chem Technol18(2): 235-252.
Ding, S.Y.; Himmel, M.E. 2008. Anatomy and ultrastructure of maize cell walls: an example of energy plants. In: Himmel, M.E., (Ed.), Biomass recalcitrance. Deconstruction of the plant cell wall for bioenergy. Blackwell, London, pp: 38–60.
Eaton, RA., Hale MDC. 1993. Wood: decay, pests and protection. Chapman and Hall/ London.
EN 113. 1997. Wood Preservatives-determination of the Toxic Values against Wood Destroying Basidiomycetes Cultured on Agar Medium.
Eriksson, K.E.L.; Blanchette, R.A.; Ander, P. 1990. Microbial and enzymatic degradation of wood and wood components. Springer, Berlin.
Fackler, K.; Stevanic, J.S.; Ters, T.; Hinterstoisser, B.; Schwanninger, M.; Salmen, L. 2011. FT-IR imaging microscopy to localise and characterize simultaneous and selective white-rot decay within spruce wood cells. Holzforschung 65: 411-420.
Gärtner, H.; Schweingruber, F.H., 2013. Microscopic preparation techniques for plant stem analysis. Kessel, Remagen.
Hale, MDC.; Eaton, RA. 1985a. Oscillatory growth of fungal hyphae in wood cell walls. Trans. Br. Mycol. Soc. 84: 277-288.
Hale, MDC.; Eaton, RA. 1985b. The ultrastructure of soft-rot fungi. II. Cavity forming hyphae in wood cell walls. Mycologia 77: 594-605.
Harrington, K.J., Higgins, H.G., Michell, A.J., 1964. Infrared spectra of Eucalypus regnans F. Muell. and Pinus radiata D.Don. Holzforschung 18: 108–113.
Hartig, R., 1878. Die Zersetzungserscheinungen des Holzes der Nadelholzbaume und der Eiche in forstlicher, botanischer und chemischer Richtung. Springer, New York.
Hatakka A., Hammel K.E., 2010. Fungal Biodegradation of Lignocelluloses. In: HOFRICHTER M (Ed) The Mycota. 2nd ed. Springer, Berlin, Heidelberg, New York, pp: 319–340.
Hervé, V., Mothe, F., Freyburger, C., Gelhaye, E., Frey-Klett, P. 2014. Density mapping of decaying wood using X-ray computed tomography. Int. Biodeterior. Biodegrad 86: 358-363.
Hinterstoisser, B.; Salmen, L. 2000. Application of dynamic 2D FTIR to cellulose. Vib Spectros 22: 111–118.
Karim, M.; Ghodskhah Daryaei, M.; Torkaman, J.; Oladi, R.; Tajick Ghanbary, M.A.; Bari, E. 2016. In vivo investigation of chemical alteration in Oak wood decayed by Pleurotus ostreatus. Int Biodeterior Biodegrad 108: 127-132.
Kartal, N.S; Terzi, E.; Yılmaz, H.; Goodell, B. 2015. Bioremediation and decay of wood treated with ACQ, micronized ACQ, nano-CuO and CCA wood preservatives. Int Biodeterior Biodegrad 99: 95-101.
Kirk, T.K.; Koning, J.W.; Burgess, R.R.; Akhtar, M.; Blanchette, R.A.; Cameron, D.C.; Cullen, D.; Kersten, P.J.; Lightfoot, E.N.; Myers, G.C.; Sachs, I.; Sykes, M.; Beth Wall, M. 1993. Biopulping. A glimpse of the future? USDA Forest Serv. Res. Paper FPL-RP-523.
Kim, J.S.; Gao, J.; Daniel, G. 2015. Cytochemical and immunocytochemical characterization of wood decayed by the white rot fungus Pycnoporus sanguineus I. preferential lignin degradation prior to hemicelluloses in Norway spruce wood. Int Biodeterior Biodegrad 105: 30-40.
Klemm, D.; Schmauder, H.P.; Heinze, T. 2004. Cellulose. In: Steinbüchel, A. (Ed.), Biopolymers Volume 6, Polysaccharides II: Polysaccharides from Eukaryotes Münster, Germany: Wiley-VCH.
Kondo, T. 1997. The assignment of IR absorption bands due to free hydroxyl groups in cellulose. Cellulose 4: 281-292.
Koshijima, T.; Watanabe T. 2003. Association between lignin and carbohydrates in wood and other plant tissues. Springer, Berlin Heidelberg, New York.
Kubicek, C.P. 2013. Fungi and lignocellulosic biomass. John Wiley & Sons, Inc, Chichester.
Liers, C.; Ullrich, R.; Steffen, K,T.; Hatakka, A.; Hofrichter, M. 2006. Mineralization of 14C-labelled synthetic lignin and extracellular enzyme activities of the wood-colonizing ascomycetes Xylaria hypoxylon and Xylaria polymorpha. Appl. Microbiol. Biotechnol 69: 573–579.
Liese, W. 1970. Ultrastructural aspects of woody tissue disintegration. Ann Rev Phytopath 8: 231–258.
Mann, J.; Marrinan, H.J. 1956. The reaction between cellulose and heavy water. Part 3.-A quantitative study by infra-red spectroscopy. Trans Faraday Soc 52:492-497.
Martinez, A.T; Camarero, S.; Gutiérrez, A.; Bochini, P.; Galleti, G.C .2001. Studies on wheat lignin degradation by Pleurotus species using analytical pyrolysis. Journal of Analytical and Applied Pyrolysis 58–59: 401–411.
Martínez, A.T.; Speranza, M.; Ruiz-Dueñas, F.J.; Ferreira, P.; Camarero, S.; Guillén, F.; Martínez, M.J.; Gutiérrez, A.; delRío, J.C.2005. Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Intern Microbiol 8: 195–204.
Mohebby, B. 2005. Attenuated total reflection infrared spectroscopy of white-rot decayed beech wood. Int Biodeterior Biodegr 55: 247–251.
Mohebby, B. 2005. Attenuated total reflection infrared spectroscopy of white-rot decayed beech wood. Int. Biodeterior. Biodegrad 55, 247–251.
Nagadesi, P.; Arya, A.; Albert, S. 2013. Delignification pattern of wood decay by white rot fungi in teak (Tectona grandis L. f.). J Indian Acad Wood Sci 10: 1-8.
O’Sullivan ,A.C. 1997. Cellulose: the structure slowly unravels. Cellulose 4: 173–207.
Ouis, D. 2000. Detection of decay in logs through measuring the damping of bending vibrations by means of a room acoustical technique. Wood Sci Technol 34: 221–236.
Pandey, K.K; Pitman, A.J .2003. FTIR studies of the changes in wood following decay by brown-rot and white-rot fungi. Int Biodeterior Biodegr 52: 151–160.
Pandey, K.K.; Theagarajan, K.S. 1997. Analysis of wood surfaces by diffuse reflectance (DRIFT) and photoacoustic (PAS) Fourier transform infrared spectroscopic techniques. Holz alas Roh- und Werkstoff 55: 383–390.
Popescu, C.M.; Popescu, M.C.; Singurel, G.; Vastile, C.; Argyropoulos, D.; Willfor, S. 2007. Spectral characterization of eucalyptus wood. Appl. Spectr 61: 1168-1177.
Rayner, A.D.M.; Boddy, L. 1988. Fungal decomposition of wood: its biology and ecology. Wiley, Chichester.
Schmidt, O. 2006. Wood and Tree Fungi: Biology, Damage, Protection, and Use. Springer, Berlin, Heidelberg.
Schmidt, O.; Bahmani, M.; Koch, G.; Potsch, T.; Brandt, K. 2016. Study of the fungal decay of oil palm wood using TEM and UV techniques. Int. Biodeterior. Biodegrad 111: 37-44.
Schmidt, O.; Gaiser, O.; Dujesiefken, D. 2012. Molecular identification of decay fungi in the wood of urban trees. Eur J Forest Res 131: 885–891.
Schubert, M.; Volkmer, T.; Lehringer, C.; Schwarze, F.W.M.R. 2011. Resistance of bioincised wood treated with wood preservatives to blue-stain and wood-decay fungi. Int Biodeterior Biodegrad 65: 108-115.
Schultz, T.P.; Glasser, W.G. 1986. Quantitative structural analysis of lignin by diffuse reflectance Fourier transform spectrometry. Holzforschung 40: 37–44.
Schwanninger, M.; Rodrigues, J.C.; Pereira, H.; Hinterstoisser, B. 2004. Effects of short-time vibratory ball milling on the shape of FT-IR spectra of wood and cellulose. Vib Spectros 36: 23–40.
Schwarze, F.W.M.R.; Engels, J.; Matthek, C. 2004. Fungal strategies of wood decay in trees. 2nd ed. Springer, Berlin, Heidelberg, New York.
Schwarze, F.W.M.R. 2007. Wood decay under the microscope. Fun Biol Rev 21: 133–170.
Sjöström, E. 1993. Wood Chemistry, Fundamentals and Applications. Academic, San Diego.
Stokland, J.N.; Siitonen, J.; Jonsson, B.G. 2012. Biodiversity in dead wood. Cambridge University Press, New York.
Sugiyama, J.; Persson, J.; Chanzy, H. 1991. Combined infrared and electron diffraction study of the polymorphism of native celluloses. Macromolecules 24: 2461–2466.
Sweet, M.; Winandy, J.E. 1999. Influence of degree of polymerization of cellulose and hemicellulose on strength loss in fire-retardant-treated southern pine. Holzforschung 53: 311–317.
TAPPI standard. 1998. Standard methods for acid-insoluble lignin in wood and pulp, T 222. om-98.
TAPPI standard. 1992. Standard methods for Carbohydrate composition of extractive-free wood and wood pulp by gas-liquid chromatography. Standard T249 cm–85.
TAPPI standard. 1997. Cellulose in wood. Standard T17 wd–97.
Timell, T.E. 1967. Recent progress in the chemistry of wood hemicelluloses. Wood Sci Technol 1: 45–70.
Wälchli, O. 1970. Influence of the content of organic matter of soil on the degradation of wood by soft rot fungi. The International Research Group on Wood Preservation. IRG/WP 27.
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2018-01-01
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Bari, E., Mohebby, B., Reza Naji, H., Oladi, R., Yilgor, N., Nazarnezhad, N., M. Ohno, K., & D. Nicholas, D. (2018). Monitoring the cell wall characteristics of degraded beech wood by white-rot fungi: Anatomical, chemical, and photochemical study. Maderas-Cienc Tecnol, 20(1), 35–56. Retrieved from https://revistas.ubiobio.cl/index.php/MCT/article/view/3008
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