Professional Documents
Culture Documents
1991 Blanchette Annual Review of Phytopathology 29 1 Delignification by Wood-Decay Fungi
1991 Blanchette Annual Review of Phytopathology 29 1 Delignification by Wood-Decay Fungi
REVIEWS Further
Quick links to online content
DELIGNIFICATION BY
WOOD-DECAY FUNGI
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
Robert A. Blanchette
by University of Edinburgh on 05/31/12. For personal use only.
INTRODUCTION
Wood decay fungi are unique because of their capacity to decompose lignified
cell walls. A few species are of special interest because they can selectively
remove lignin from wood without extensive cellulose degradation. Lignin is a
complex, heterogeneous phenylpropanoid structural polymer that occurs
throughout the cell wall (71, 112). Spatially, lignin is intimately interspersed
with hemicelluloses forming a matrix that surrounds cellulose microfibrils
(67, 75), and provides a formidable physical and chemical barrier to biodeg
radative systems. Although most saprophytic fungi produce some degradative
enzymes, such as cellulases, xylanases, mannanases and others, these en
zymes do not permeate and degrade effectively woody substrates unless lignin
is unbound, modified, or removed.
Investigations of decomposition processes in forest ecosystems have usual
ly considered lignin to be the most recalcitrant component and the last
degraded (l0, 88). The decomposition pathway for decay by some fungi in
the Basidiomycotina, such as those that cause brown rots, involves the
degradation of all wood carbohydrates, including crystalline cellulose. A
residual lignin matrix, consisting of chemically modified lignin, is left to be
gradually converted to humic substances by long-term processes involving
other microbes (38, 41, 106). However, this is not always the sequence of
events. Fungi in the Basidiomycotina that cause white rots of wood may
simultaneously degrade lignin along with all cell wall carbohydrates, or lignin
381
0066-4286/9 110901-0381$02:00
382 BLANCHETTE
Table 1 Percent weight, lignin, and sugar residues in wood polysaccharides lost in Betula
papyrifera after 1 2 weeks of decay by white-rot fungi"
% loss in
Fungus Weight Lignin b GlucoseC Xylosed
Dichomitus squalens 44 71 44 43
Ganoderma colossum 35 46 19 45
Heterobasidion annosum 24 55 4 26
Perenniporia medulla-panis 31 73 0 32
Phanerochaete chrysosporium
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
BKM-F- 1 767 39 73 15 55
Fp 1 02 1 69 55 60 55 66
HHB - 1 I741 46 51 48 58
ME- I O 33 41 24 34
by University of Edinburgh on 05/31/12. For personal use only.
Phellinus pini 17 54 5 13
Phlebia tremellosa 34 75 4 39
Trametes versicolor 65 64 65 68
'Sound Betula contains 20% lignin, 47% glucose, and 24% xylose.
bKlason lignin determination using 72% sulfuric acid.
cGlucose residue represents hydrolized cellulose from wood.
"Xylose residue represents hydrolized xylan from wood.
PATTERNS OF DELIGNIFICATION
All white-rot fungi can cause lignin degradation but some can selectively
remove lignin leaving large concentrations of cellulose. These areas of cellu
lose appear as bright, white zones in the heartwood of living trccs or in
sapwood and heartwood of downed timber (Figure 2). A well-known fungus,
Phellinus pini, causes extensive decay in living conifers throughout the
world. The decay consists of spindle-shaped pockets of white, delignified
wood. It is not surprising that this type of decay, with its striking appearance
of white pockets scattered throughout the dark-colored heartwood, was one of
the first investigated (56), and continued to receive considerable attention (9,
11, 13, 38, 65, 85-87). Many of the most serious decay-causing fungi result
in selective delignification of wood (e. g. Ganoderma lucidum, Heterobasid
ion annosum, Inonotus tomentosus, Inonotus dryadeus, Phellinus nigroiimi
tatus, Phellinus weirii) (5, 16, 3S).
The fossil record also shows that wood with a white-pocket rot, containing
spindle-shaped zones of delignified wood, occurred as early as the Triassic in
Araucarioxylon (117; Figure 2). These samples represent some of the oldest
known examples of decay, and demonstrate that little change has occurred in
decay patterns over millions of years (11S). Since these early gymnosperms
most likely had high lignin contents and large concentrations of extractives, it
is not surprising to find the decay fungi present were those with the capacity to
cause extensive lignin degradation.
384 BLANCHETTE
forests for pasture, gradually decayed, and during the winter months of
subsequent years, farmers split these logs open giving livestock access to the
huge concentrations of digestible fiber. This procedure is still practiced today
by University of Edinburgh on 05/31/12. For personal use only.
Anatomical Considerations
dies ( 13). The pockets of delignified wood are often first associated with
latewood regions of annual rings, and elongate within an individual growth
ring. In contrast, Ganoderma tsugae preferentially degrades the earlywood
cells, but not latewood cells (14). In hardwood species, such as Quercus, the
latewood fibers and rays form borders between pockets of delignification
caused by Inonotus dryophilus (94). Phellinus nigrolimitatus produces large
pockets of delignified wood that may form across several annual rings, and
decay is not restricted to latewood or earlywood zones. Pockets of delignifica
tion also form in tropical species, such as those caused by Phellinus kawaka
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
mii in Acacia koa. where no annual rings are formed in the tree (23).
Although the reason for the formation of localized pockets of delignified
wood remains unknown, it should be possible to obtain a better understanding
by University of Edinburgh on 05/31/12. For personal use only.
& Kraepelin (37) concluded that the extremely low nitrogen content of the
wood was the primary cause for delignification. Several other ecological
factors, including relatively low temperatures (8 to 13°C during the entire
year) and high humidity also appeared to favor delignification. Nutrient
nitrogen has been found to play a crucial role in wood decay (32, 84, 90).
Low levels of nitrogen have been shown to stimulate lignin degradation by
several different white-rot fungi, whereas high nitrogen concentrations stimu
late polysaccharide degradation (45,78,108). Ligninolytic activity of some
white-rot fungi, however, is not affected by nitrogen concentrations (81,
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
125).
Oxygen concentrations also affect lignin degradation. In general, most
investigations have shown that the greatest ligninolytic activity in shake flask
by University of Edinburgh on 05/31/12. For personal use only.
guaiacyl ratio of all the native woods tested. Indeed, Nothofagus dombeyi has
one of the highest syringyl lignin contents reported for any wood (6). In vitro
decay studies,using a species of Ganoderma isolated from delignified wood
of palo podrido and native woods of southern Chile,confirmed field observa
tions that selective delignification occurred in wood of Nothofagus dombeyi,
whereas a simultaneous rot was always found in wood of Laurelia phillipiana
(R. A. Blanchette & E. Agosin, unpublished results).
The lignin of angiosperms contains varying ratios of syringyJ (S) to
guaiacyl (G) phenylpropane monomer units. Nothofagus dombeyi has a S/G
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
ratio of 2.73, whereas the ratio for Laurelia phillipiana is 0.35 (6; a correction
factor of 2.3 has been used to compare the thioacidolysis determination to the
nitrobenzene assay for S/G ratios). The ratio for Acer saccharum and Tilia
by University of Edinburgh on 05/31/12. For personal use only.
lignin-degrading capacity than the original wild type (64). Several recent
studies have examined the genetic factors influencing lignin peroxidase activ
ity (see section on Ligninolytic Systems; 102, 104, 105). Using 53 single
basidiospore-derived strains of Phanerochaete chrysosporium, lignin per
oxidase activity was determined for each monokaryotic isolate and compared
to the activity of the parent dikaryon (105). The variation in lignin peroxidase
activity varied with many of the haploid progeny exhibiting superior
ligninolytic activity to that of the parent. In a study using 20 monokaryotic
isolates of Dichomitus squalens, a similar experimental procedure was used,
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
and cellulolytic activity varied greatly. Several isolates had low cellulolytic
activity while others displayed high ligninolytic activity. It appears possible
that significant improvements in ligninolytic activity could be achieved for
industrial purposes by selection and cross-breeding of haploid strains.
Lignin is distributed throughout the wood cell wall layers, but the greatest
concentrations are in the compound middle lamella and cell comer regions
(Figure 4). To visualize lignin with electron microscopy, KMn04 is often
used as a fixative and lignin stain to identify the relative distribution of lignin
in wood (12, 24). The most lignified layer, the middle lamella, has the
greatest electron density. Other methods used to precisely determine the
ultrastructural localization of lignin have confirmed the distribution patterns
previously determined by KMn04 staining,and have been used to quantify
lignin concentrations in different types of cells as well as within various cell
wall layers (38, 99, 1 1 1, 123a).
Decay fungi colonize wood via the anatomical paths of least resistance,and
quickly move into areas containing easily assimilated nutrients. Ray pa
renchyma cells are frequently the first to be colonized (31, 124). Movement
through pit apertures or direct penetration of cell walls by bore holes allows
the fungus to proliferate throughout the wood. With relatively few hyphae
within individual xylary cells (i. e. one or two per cell) lignin degradation
begins. Lignin degradation by hyphae in cell lumina causes a diffuse reduc
tion in KMn04 electron density within the secondary wall layers immediately
adjacent to the fungus (Figure 4). Gradually, the entire secondary wall
becomes less electron dense. The process of lignin removal occurs from the
cell lumen toward the middle lamella (Figure 4). Once lignin is removed from
the SI and S2 layers of the secondary walls, the middle lamella between cells
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
by University of Edinburgh on 05/31/12. For personal use only.
Figure 1 Drawing by Robert Hartig (1878) showing two forms of white rot in wood of Pinus
sylvestris decayed by Heterobasidion annosum. On the left, incipient to advanced stages of
selective delignification is shown. Lignin (stippled ateas) is progressively removed from tracheid
cell walls, resulting in cells void of middle lamellae. Once lignin was removed, cellulolytic
activity gradually degraded the delignified secondary wall. On the right a simultaneous decay of
all cell wall components is presented. This form of white rot resulted in cell wall erosion of
secondary walls followed by portions of the middle lamellae. The last ateas to be degraded are the
lignified middle lamellae. This drawing represents the first observations showing selective
de lignification in wood , and demonstrates that white rot fungi can cause different forms of
degradation.
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
by University of Edinburgh on 05/31/12. For personal use only.
Figure 2 White-pocket rot in living trees, with spindle-shaped areas of delignified wood
separated by nondecayed wood. A Drawing of a split open section of a conifer showing
white-pocket rot within the heartwood. B The white-pockets consist of delignified cells where
lignin has been completely removed leaving the white, cellulose-rich tracheids remaining. Areas
of apparently unaltered wood occur between the pockets. C Transverse section and light
microscopy micrograph of a white pocket in a deciduous wood (Betula papyrijera) inoculated
with Phellinus pini. Delignified cells (arrows indicate edge of the white pocket) lack middle
lamella and are detached from adjacent cells. The hyphae (one or two per cell) can be seen within
the deJignified cells as well as in nondecayed cells between pockets. D Fossilized Araucarioxylon
wood, a silicified gymnosperm genus from the Triassic age, found in the Fremouw Peak locality,
Antarctica. The fossil wood contains a white-pocket rot with spindle-shaped pockets of de
lignified wood. Bar = 1 cm in A and D, 50/-Lm in C. (A reproduced by courtesy of Alex Shigo,
US Forest Service, D reproduced by courtesy of T.N. Taylor, Ohio State University).
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
by University of Edinburgh on 05/31/12. For personal use only.
Figure 3 A mottled-rot caused by Ganoderma tsugae showing two different fonns of white rot,
selective delignification and simultaneous decay of all cell wall components, in Tsuga
canadensis. A Mottled appearance of the wood results from a combination of delignified cells (dl)
and simultaneous decayed cells (sd). Within the simultaneously decayed zones, large voids were
fonned that were filled with white fungal mycelia (m). In delignified areas, manganese dioxide
deposits were common, appearing as large black zones (arrows). B and C Wood from the white,
delignified zones contained tracheids that lacked middle lamellae and cells easily detached from
adjacent cells. D and E Wood from simultaneously decayed areas had cells with erosion troughs
and holes evident within the cell walls. In some areas, large voids fonned and were filled with
fungal mycelia (14).
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
by University of Edinburgh on 05/31/12. For personal use only.
Figure 4 Transmission electron micrographs showing the progressive stages of selective de
lignification in cell walls of Nothofagus dombeyi by Ganoderma sp. Wood was fixed with
KMn04 to stain lignin within cell walls. A 50und wood showing fiber (F) and vessel (V) w it h
electron-dense cell wall layer s . The secondary wall layers (5" 52. and 53) and middle lamella
(ml) are evident. The middle lamella between cells and in cell corners (CC) appear the most
electron dense. B Incipient stages of delignification showing an electron lucid zone within the 52
layer of the secondary wall. There is a progressive loss of electron density from the lumen toward
the middle lamella (arrows). The area where no stain is apparent represents delignified regions of
the cell wall. C A more advanced stage shows a cell where secondary wall layers have been
delignified and the middle lamella between cells has been degraded (arrows). Other cells show
loss of lignin from the S2 layer of the secondary walls but delignification had not reached the S I
layer or middle lamella. D Advanced stage of delignified wood with lignin removed from the
secondary wall layers and middle lamellae completely degraded. Bar = 2 /Lm (from (6)).
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
by University of Edinburgh on 05/31/12. For personal use only.
wood and in wood decayed by fungi ( 18, 20). In wood cells delignified by
fungi, colloidal gold coupled to endo-l, 4-I3-glucanase II (EG-II) or l,4-I3-D
glue an cellobiohydrolase I (CBHI) labeled intensely residual cell walls in a
pattern similar to that of sound wood, indicating crystalline and amorphous
cellulose were still present in large concentrations. Examination of cell walls
labeled with endo-l, 4-I3-xylanase, however, showed that substantial amounts
of xylan had been removed. In another investigation, gold-labeled lignin
peroxidase was used to locate lignin within the cell walls of sound and
delignified wood ( 19). In delignified cells, no gold labeling was apparent,
except for some in the residual cell comer regions that had maintained a high
lignin content. Fluorescence microscopy also has been useful in monitoring
the lignin distribution in wood since lignified cell walls fluoresce in UV light
of certain wavelengths (9, 47). In a study of Quercus wood decayed by
Lentinula edodes, the Shiitake fungus, delignification was apparent in cells
that did not fluoresce (126). In that study, a similar pattern of lignin removal
was found as described above. Secondary cell wall layers were progressively
delignified from cell lumina toward the middle lamella, followed by degrada
tion of middle lamella between cells, and finally attack of the cell comer
regions. Between delignified zones in the wood, a simultaneous type of white
rot was evident. Lentinula edodes, therefore, appears to be a white-rot fungus
exhibiting considerable diversity in delignification capacity among different
strains, since previous studies have indicated that this fungus causes only a
nonselective attack on the cell wall (R. A. Blanchette, unpublished data;
122).
In addition to differences in delignification observed in various regions of
the xylem (latewood vs earlywood), there appears to be a great deal of
variability in the types of cells that are delignified by different white-rot fungi.
Some fungal species delignify all the different types of cells that occur in
angiosperms, including vessels, fibers, and ray parenchyma cells (Figure 5).
However, delignification may not occur in vessels of some woods, such as
390 BLANCHETTE
Acacia koa, where sound vessels occur among completely delignified fibers
(23). In decay of Quercus species by Inonotus dryophilus, the latewood fibers
remain free of degradation while earlywood fibers are delignified (94). Fibers
delignified by Ganoderma zonatum may not be uniformly affected, and
irregular zones of lignin may remain in parts of the secondary wall (5). In
conifers, it is common to find delignified tracheids among totally degraded
ray parenchyma cells (Figure 5). In palm wood, delignification is apparent in
the vessel elements but is not observed in other cells (4). Additional studies of
delignification processes should provide insight into the factors that allow
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
LIGNINOLYTIC SYSTEMS
would be able to diffuse into wood, and recent studies suggest that Mn III
under certain conditions is capable of ligninolytic activity (46). Other low
molecular weight compounds, such as the modified porphyrins, also diffuse
into wood and degrade lignin. Since LiP is a heme protein containing pro
toporphyrin IX, various researchers have used synthetic metalloporphyrins to
degrade lignin model compounds as well as lignin in wood. Low molecular
weight porphyrins appear to mimic the activities of lignin peroxidase and
cause delignification in a manner similar to selective delignification by white
rot fungi (34, 101, 115). Some porphryins readily diffuse into the wood and
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
reach the same levels of wood cell wall delignification that usually requires 2
to 3 months of laboratory degradation by white-rot fungi.
It may not be absolutely essential for initial delignification agents to be low
molecular weight compounds. Some enzymes, such as the hemicellulases, are
produced early in the decay process, and are associated with lignin degrada
tion ( 17, 38). Hemicellulases may gradually degrade hemicelluloses in the
wall immediately adjacent to the lumen and progressively move into the
secondary wall. As some of the hemicelluloses are degraded, channels of
sufficient size should open, allowing access to LiP and MnP. Immunocyto
chemical investigations using gold-labeled LiP-antisera and sections of white
rotted wood have shown that LiP does occur in areas of the cell wall
undergoing delignification (20,35,36). In partially delignified wood decayed
by Phellinus pini or Phanerochaete chrysosporium, LiP was localized within
the wall at the edge of electron-dense regions that still contained lignin. The
ultrastructural localization of xylanase in decayed wood from Betula also was
within the cell wall, and apparently in advance of zones showing lignin
removal (20). Purified preparations of both LiP and MnP have been infiltrated
into white-rotted wood followed by immunogold labeling and were found
within cell walls that had a loose, open fibrillar structure (36). No diffusion
occurred in nondecayed cell walls.
Many other enzymes (including polyphenol oxidases, laccases, H20z
producing enzymes and quinone-reducing enzymes) are also thought to be
important for lignin degradation. (For recent reviews that provide detailed
coverage of the enzymes involved in lignin degradation see 30, 38, 60, 72,
73, 75, 1 19.) Also of interest are the factors that regulate both enzyme
production and activity. Manganese, which can be found in exceedingly large
concentrations in delignified wood ( 15; Figure 3), appears to regulate LiP and
MnP production (27). In low concentrations of MnII, extracellular LiP pre
dominates, whereas in the presence of higher concentrations of Mn II, MnP is
dominant.
392 BLANCHETTE
The surge of research activities in this area will continue, and we can
expect to see important new developments that utilize ligninolytic fungi for
many commercial purposes. Applications in tum should spur investigations
that will provide needed basic information on enzyme mechanisms involved
in microbial degradation of living trees and forest products.
CONCLUDING REMARKS
White-rot fungi may cause a simultaneous type of attack that degrades all
wood cell wall components or preferential degradation of lignin. Selective
delignification may occur throughout the decayed wood (e. g. palo podrido,
palo blanco), in small localized pockets (e. g. decay by Phellinus pini) or in a
mottled-rot where delignified cells are surrounded by simultaneously decay
ing wood (e. g. decay by Ganoderma tsugae, Heterobasidion annosum).
Fungi that delignify wood include some of our most serious root and butt rot
fungi (e. g. Ganoderma lucidum, Heterobasidion annosum, Inonotus tomen
tosus, Phellinus weirii, Rigidoporus lignosus, Phellinus noxius) and trunk rot
fungi (e. g. Ganoderma applanatum, Inonotus dryophilus, Phellinus pini).
Information on basic biological processes, such as degradative mechanisms,
survival strategies, and ecological relationships is lacking, but is needed to
ascertain potential disease-control measures. Some of this information may
become available from investigations that are specifically designed for using
selective delignifying fungi for industrial applications.
The biotechnical potential of fungi that delignify wood is enormous. One
use currently being tested includes the pretreatment of wood chips with fungi
that selectively remove lignin for pulp and paper production. Pretreated chips
with selected strains of Phanerochaete chrysosporium, Ceriporiopsis sub
vermispora, and other fungi improved paper strength properties while requir
ing up to 68% less energy than standard mechanical pulping procedures (82,
83, 91). Another aspect of white-rot fungi that may be of significant use is
DELIGNIFICATION BY FUNGI 393
their ability to "bleach" wood to a white color. The effluents produced during
chemical bleaching of kraft pulping are major contributors to water pollution,
and new methods of bleaching wood pulp with fungi or their enzymes may
provide a viable substitute for some of the chemicals now used (30a, 37a, 39,
121). Delignification processes also may be used to modify wood or agri
cultural byproducts to increase their nutritional value for ruminant animal
feed. The digestibility of straw, bagasse, and wood can be dramatically
increased when treated with various white-rot fungi, and have shown no
problems of palatability or toxicity (7, 30, 77, lO7, lO9). Of major signifi
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
cance are the recent investigations showing that fungi with high ligninolytic
activity are able to degrade environmental pollutants, such as PCB, DDT,
dioxins, industrial dyes, and chlorinated phenols (28-30, 33, 38, 39, 42, 53).
by University of Edinburgh on 05/31/12. For personal use only.
The use of these fungi as bioremedial treatments of toxic wastes has im
mediate application. For example, Phanerochaete chrysoporium BKM-F-
1767 is currently being used in large scale ficld tests to detoxify soils (K.
Kirk, personal communication).
We can expect to see additional uses for fungi that de1ignify wood as our
knowledge of these organisms increases. One major benefit from these in
vestigations will be the increased comprehension of white-rot degradation
mechanisms that will undoubtedly improve our understanding of pathological
relationships among decay fungi and living trees.
ACKNOWLEDGMENTS
This article is contribution No. 18,588 of the Minnesota Agricultural Experi
ment Station. The author thanks Andre Abad, Kory Cease, Marge Eerdmans
and Lewis Otjen for their contributions to research on selective delignification
of wood reported here, and to Drs. Kent Kirk, Roberta Farrell, Gary Leath
am, and Jim Adaskaveg for their critical reviews of this manuscript. The work
of the author has been supported by NSF Grant INT-8900153, Repligen
Sandoz Research Corp. , and the Biopulping Consortium. The consortium
consists of the University of Wisconsin Biotechnology Center, USDA Forest
Products Laboratory, Madison, WI, and 20 member companies involved in
pulp and paper production and associated fields.
Literature Cited
8. Ander, P., Eriksson, K-E. 1 977. Selec of lignin peroxidase and xylanase by im
tive degradation of wood components by munocytochemical labeling in wood de
white-rot fungi. Physiol. Plant. 4 1 :239- cayed by Basidiomycetes. Appl. En
48 viron. Microbiol. 55: 1 457-65
9. Aufess, H. von, Pechmann, H. von, 21. Blanchette, R. A., Burnes, T. A.,
Graessle, H. 1 968. Fluoreszenzmikrosk Leatham, G. F. , Effland, M. J. 1 988.
poischc Beobachtungcn an pilzbefal Selection of white rot fungi for biopulp
lenem Holz. Holz Roh Werkst. 261 :50- ing. Biomass 1 5:93- 1 0 1
61 22. Blanchette, R . A . Nilsson, T. , Daniel,
1 0 . Barbour, M . G., Burk, J . H . , Pitts, W. G., Abad, A. 1 990. Biological degrada
D. 1 987. Terrestrial Plant Ecology. tion of wood. In Archaeological Wood:
Menlo Park: Benjamin/Cummings. 634 Properties, Chemistry and Preservation,
pp. ed. R. M. Rowell, R. J. Barbour, pp.
II. Bjorkman, E., Samuelson, 0., Ring 1 4 1-74. Adv. Chern. SeT. 225, Am.
strom, E., Bergelk, T., Maim, E. 1 949. Chern. Soc. Washington DC
Decay injuries in spruce forests and their 23. Blanchette, R. A., Obst, 1. R., Hedges,
importance for the production of chemi J. I., Weliky, K. 1 988. Resistance of
cal paper pulp and rayon pulp. K. Skog hardwood vessels to degradation by
shogskolan Skr. NO. 4. Stockholm white rot basidiomycetes. Can. J. Bot.
1 2. Bland, D. E., Foster, R. c., Logan, A. 66:1841-47
F. 1 97 1 . The mechanism of permanga 24. Blanchette, R. A., Otjen, L., Carlson,
nate and osimum tetroxide fixation and M. C. 1 987. Lignin distribution in cell
the distribution of lignin in the cell wall walls of birch wood decayed by white
of Pinus radiata. Holzforschung rot Basidiomycetes. Phytopathology 77:
25:1 37-42 684--90
1 3. Blanchette, R. A. 1 980. Wood decom 25. Boddy, L. 1 983. Microclimate and
position by Phellinus (Fames) pini: A moisture dynamics of wood decompos
scanning electron microscopy study. ing in terrestrial ecosystems. Soil BioI.
Can. J. Bot. 58 : 1 496-503 Biochem. 1 5: 1 49-57
1 4. Blanchette, R. A. 1 984. Selective de 26. Boddy, L. 1 986. Water and decomposi
lignification of eastern hemlock by tion processes in terrestrial ecosystems.
Ganoderma tsugae. Phytopathology 64: In Water, Fungi and Plallts, ed. P. G.
1 53-60 Ayres, L. Boddy, pp. 375-98. Cam
1 5. Blanchette, R. A. 1 984. Manganese ac bridge: Cambridge Univ. Press
cumulation in wood decayed by white 27. Bonnarme, P., Jefferies, T. W. 1 990.
rot fungi. Phytopathology 74:725-30 Mn(II) regulation of lignin peroxidases
1 6. Blanchette, R. A. 1 984. Screening wood and manganese-dependent peroxidases
decayed by white rot fungi for preferen from lignin-degrading white rot fungi.
tial lignin degradation. Appl. Environ. Appl. Environ. Microbiol. 56: 2 1 0- 1 7
Microbiol. 48:647-53 2 8 . Bumpus, J . A . , Aust, S . D . 1 986. Bio
1 7. Blanchette, R. A., Abad, A. R. 1 988. degradation of environmental pollutants
Ultrastructural localization of hemicellu by the white rot fungus Phanerochaete
lose in birch wood (Betula papyrifera) chrysosporium: involvement of the lig
decayed by brown and white rot fungi. nin degrading system. BioEssays 6:
HolzIorschung 42:393-98 1 66-70
DELIGNIFICATION BY FUNGI 395
Pulp and Paper Manufacture, Applica degrade lignin. Appl. Microbiol. Bio
tions and Fundamental Investigations, technol. 2 1 :320-27
ed. T. K. Kirk, H-M. Chong. pp. 429- 65 . Jurasek, L. 1 964. Changes in the micro
38. Boston: Butterworth-Heinemann structure at the destruction of wood by
52. Gonzalez, A . , Grinbergs, J. , Griva, E . wood destroying fungi. Drev. Vysk. 3:
1986. Biological transformation o f wood 1 27-44
into feed for cattle - "Palo podrido". Zbl. 66. Kawase, K . 1 962. Chemical compo
Mikrobiol. 14 1 : 1 8 1-86 nents of wood decayed under natural
53. Hammel, K. E. 1989. Organopollutant conditions and their properties. Hok
degradation by ligninolytic fungi. En kaido Diagaku Sapporo 1. Fac. Agr.
zyme Microb. Technol. 1 1 :776-77 52: 1 86-245
54. Hammel , K. E . , Tien, M . , Kalyanara 67. Kerr, J. , Goring, D. A. I. 1 975. The
man, B . , Kirk, T. K. 1 985. Mechanisms ultrastructural arrangement of the wood
of oxidative C - C cleavage of a lignin cell wall. Cellul. Chem. Techno/. 9:
Annu. Rev. Phytopathol. 1991.29:381-403. Downloaded from www.annualreviews.org
cheinungen des Holzes der Nadelholz generates cation radicals from methoxy
baume und der Eiche in forstlicher. benzenes. 1. Bioi. Chem. 260:2609-
botanischer und chemischer Richtung. 12
Berlin/New York: Springer. 1 5 1 pp. 69. Kim, Y . S . , Park, B . D . , Lee, J. K .
56. Hartig, R. 1 894. Text-book of the Dis 1988. Micromorphological features of
eases of Trees. Trans!. W. Somerville, oak wood cultivated with Shiitake mush
H. M .Ward. London: Macmillan. 331 room, Lentinus edodes (Berk) Sing. Ko
pp. rean Wood Sci. Technol. 16:38-47
57. Hartig, T. 1833. Abhandlung uber die 70. Kimura, Y . , Asada, Y . , Kuwahara, M .
Verwandlung der polycotyledonischen 1990. Screening o f basidiomycetes for
Pflanzenzelle in Pilz und Schwamm lignin peroxidase genes using a DNA
gebilde und der daraus hervorgehenden probe. Appl . Microbiol. Biotechnol. 32:
sogenannten Faulniss des Holzes. Ber 436-42
lin. 46 pp. 7 1 . Kirk, T. K. 1 97 1 . Effect of microorgan
58. Hedges, J. I . , B lanchette, R. A . , isms on lignin. Annu. Rev. Phytopathol.
Weliky, K . , Devol, A. H . 1 988. Effects 9 : 1 85-210
of fungal delignification on the CuO 72. Kirk, T. K. 1987. Lignin-degrading en
oxidation products of lignin: A con zymes. Phil. Trans. R. Soc. Lond.
trolled laboratory study. Geochim. Cos 321 :461-74
mochim. Acta 52:27 1 7-26 73. Kirk, T . K . 1988. Biochemistry of lig
59. Highley, T. L . , Bar-Lev, S. S . , Kirk, T . nin degradation by Phanerochaete
K . , Larsen, M . J. 1 983. Influence of chrysosporium. In Biochemistry and Ge
02and CO2 on wood dccay by heartrot netics of Cellulose Degradation, cd. J.
and saprot fungi . Phytopathology 73: P. Aubert, P. Beguin, J. Millet. pp.
630-33 3 1 5-32. London: Academic
60. Higuchi, T. 1990. Lignin biochemistry: 74. Kirk, T. K . , Cowling , E. B . 1 984.
biosynthesis and biodegradation. Wood Biological decomposition of wood. In
Sci. Technol. 24:23-63 The Chemistry of Solid Wood. ed. R. M .
6 1 . Hutterman, A . , Cwielong, P. 1 99 1 . Rowell. pp. 455-87. Adv. Chern. Ser.
Biochemistry of lignin degradation as 207. Am. Chern. Soc . , Washington DC
a base for control of Hcterobasidion 75. Kirk, T. K . , Farrell, R . L . 1 987. En
annosum inside the living tree. See Ref. zymatic "combustion": The microbial
1 10a degradation of lignin. Annu. Rev. Mi
62. Huynh, V-B . , Crawford, R. L. 1985. crobiol. 4 1 :465-505
Novel extracellular enzymes (ligninases) 76. Kirk, T. K . , Jeffries, T. W . , Leatham,
of Phanerochaete chrysosporium. G. F. 1983. Biotechnology: Applica
FEMS Microbiol. Lett. 28:119-23 tions and implications for the pulp and
63. Jensen, K . F. 1 969. Oxygen and carbon paper industry. Tappi. 1. 66(5):45-5 1
concentrations in sound and decaying 77. Kirk, T. K . , Moore , W. E. 1972. Re
red oak trees . For. Sci. 1 5:246-5 1 moving lignin from wood with white-rot
64. Johnsrud, S. C . , Eriksson , K-E. 1985. fungi and digestibility of resulting wood.
Cross-breeding of selected and mutated Wood Fiber 4:72-79
homokaryotic strains of Phanerochaete 78. Kirk, T. K . , Schultz, E . , Connors, W .
chrysosporium K-3 : New cellulase de J. , Lorenz, L . F. , Zeikus, J . G . 1 978.
ficient strains with increased ability to Influence of culture parameters on lignin
DELIGNIFICATION BY FUNGI 397
Fungal Decomposition of Wood. Its Bi Tansley Rev. No. 12. New Phytol. 1 08:
ology and Ecology. New York: Wiley. 3-25
587 pp. 1 1 9. Tien, M. 1987. Properties of ligninase
1 07. Reade, A. E. , McQueen, R. E. 1983. from Phanerochaete chrysosporium and
Investigation of white rot fungi for the their possible applications. CRC Crit.
by University of Edinburgh on 05/31/12. For personal use only.