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Medio ambiente y desarrollo sustentable
Artículo arbitrado
Review of agricultural and medicinal
applications of basidiomycete
mushrooms
Revisión sobre las aplicaciones de las setas en
agricultura y medicina
LORETO ROBLES-HERNÁNDEZ1, 2, ANA CECILIA-GONZÁLEZ- FRANCO1, JUAN MANUEL SOTO- PARRA1 AND
FEDERICO MONTES-DOMÍNGUEZ1
Aceptado: Septiembre 09, 2008
Recibido: Abril 18, 2008
Abstract
Resumen
Basidiomycetes are characterized in part because they produce
their basidiospores on a basidium and many but not all have
clamp connections that no other group of fungi has.
Basidiomycetes are divided into four classes, Gasteromycetes,
Ustilaginomycetes, Urediniomycetes and Hymenomycetes. The
class Hymenomycetes is characterized by the formation of
basidia in a hymenium. Members of this class form visible
macroscopic basidiocarps of different shapes, such as
mushrooms, puffballs, shelf fungi, jelly fungi, and bird’s nest
fungi. Mushrooms have many unique properties that have played
major roles in human history, religion, and culture. Of all the
fungi, these organisms are the most visible and the most colorful.
The purpose of this work was to review the potential of
basidiomycete mushrooms as producers of metabolites with
agricultural and medicinal applications. Medicinal mushrooms
offer an advantage in that their active ingredients are safe for
humans.
Many compounds, such as b-D-glucans,
heteropolysaccharides, glycoproteins, lectines, and terpenoids
inhibit tumor cell lines and did not show negative effects on
treated patients. The antimicrobial properties of certain
basidiomycetes provide human and plant disease control that is
generally safe and effective.
Several species of
basidiomycetes mushrooms have demonstrated antibacterial
activity against human pathogens; others have shown antifungal
activity against both human and plant pathogens, while others
have inhibited fitopathogenic nematodes. In conclusion,
basidiomycetes offer a unique set of compounds with potential
to address agricultural and medicinal challenges.
Los basidiomycetos se caracterizan en parte por producir
sus basidiosporas sobre un basidio y por tener fíbulas que
otros grupos de hongos no tienen. Los basidiomicetos se
dividen en cuatro clases: Gasteromycetos, Ustilaginomycetos,
Urediniomycetos e Hymenomycetos. Los Hymenomycetos
forma sus basidios en un himenio y sus basidiocarpos
macroscópicos son de formas variadas, tales como las setas,
los bejines, los hongos de repisa, etc. Las setas tienen
propiedades únicas que han influenciado de manera importante
la historia del ser humano, religión y cultura. De todos los
hongos, las setas son las más visibles y llamativos. El propósito
de este trabajo fue revisar el potencial de las setas como
productoras de metabolitos con aplicaciones en agricultura y
medicina. Los ingredientes activos de estos hongos tienen la
ventaja de ser seguros para el ser humano. Los b-D-glucanos,
heteropolisacáridos, glicoproteínas, lectinas y terpenoides
inhibieron células cancerígenas y no presentaron efectos
negativos en los pacientes tratados. Las propiedades
antimicrobianas de algunos basidiomicetos usados para el
control de enfermedades de animales y de plantas
generalmente también fueron seguras y efectivas. Varias
especies de setas han mostrado actividad antibacteriana contra
patógenos de humanos, otras han presentado actividad
antifúngica contra patógenos tanto de humanos como de
plantas, mientras que otras especies han inhibido nematodos
fitopatógenos. En conclusión, los basidiomicetos ofrecen
compuestos únicos con potencial para resolver problemas en
agricultura y medicina.
Keywords: Antibacterial, antifungal and helminticidal activities,
medicinal applications, polisaccharides, lectines
Palabras clave: Actividades antibacterianas, antifúngicas y
helminticidas, aplicaciones medicinales, polisacáridos, lectinas
__________________________________
1
Facultad de Ciencias Agrotecnológicas, Universidad Autónoma de Chihuahua, Ciudad Universitaria S/N Campus 1, Chihuahua, Chih.,
31310, México.Phone and Fax: (614) 439-1844
2
Dirección electronica del autor de correspondencia: [email protected]
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Introduction
B
asidiomycetes are characterized in part because they produce their sexual spores
(basidiospores) on a cell called basidium usually in fours. Many but not all have clamp
connections. No other group of fungi has these structures. The basidium is the cell in
which karyogamy (nuclear fusion) and meiosis occur, and on which usually four haploid
basidiospores are formed on the tips of sterigmata, which are little prong like projections that
originate from the basidium. Millions of these spores are packed together in the hymenium,
which covers the exposed or enclosed surfaces of the sporocarp, which are quite variable in
form.
These are then discharged a short
distance into the space between the gills,
tubes, or teeth, of the sporocarp.
Subsequently they fall out of the cap to be
carried away on air currents (Alexopolous, et
al., 1996).
The phylum Basidiomycota is divided into
four
classes:
Gasteromycetes,
Hymenomycetes, Ustilaginomycetes, and
Urediniomycetes.
In the class
Gasteromycetes (stomach fungi) the basidia
are formed inside the fruiting body, which
typically are one-celled. The fruiting bodies
of this group remain closed during spore
formation and maturation. The class
Hymenomycetes is characterized by the
formation of basidia in a hymenium.
Members of this class typically form visible
macroscopic basidiocarps of different
shapes, such as mushrooms, puffballs, shelf
fungi, jelly fungi, and bird’s nest fungi. The
classes Ustilaginomycetes (smut fungi and
allied taxa) and Urediniomycetes (rust fungi
and allied taxa) comprise mostly plant
parasitic taxa, and most members in both
classes form teliospores, thick-walled resting
spores, in which karyogamy occurs and from
which basidia are formed (Alexopolous et al.,
1996).
Mushrooms have many unique properties
that have played major roles in human history,
religion, and culture. These highly adaptive
96
organisms mainly feed on dead and
occasionally living matter. Of all the fungi,
these organisms are the most visible and
the most colorful. Most of us recognize the
value of mushrooms as food and certainly,
some species as delicacies.
The medicinal properties of
basidiomycete mushrooms are frequently
described in ancient cultures and a few have
been developed into pharmacological
applications today. In Asian cultures, the
holocarp of several genera are eaten,
included as a garnish, or boiled as teas and
applied as therapies for a variety of human
ailments ranging from the common cold to
cure for certain forms of cancers.
A major development in agricultural
chemistry was derived from the pine cone
fungus, Strobilurus tenacellus. Strobilurin
fungicides have become a valuable tool for
managing plant diseases. These strobilurins
are site-specific (inhibition of mitochondrial
respiration) and translaminar (systemic)
compounds that provide control of
Oomycota, Ascomycota, Basidiomycota,
and Deuteromycota fungi.
The nematode-destroying fungi have
diverse morphological and physiological
adaptations to the environment. Some are
parasitic by means of constricting rings,
injectable spores, and/or adhesive peg cells.
Some secrete attachments to trap and
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penetrate the nematode, or by secreting
toxins to inactivate the prey nematodes.
Potent antibiotics may be secreted by the
colonizing hyphae to protect the food source
from other microorganisms (Barron, 1977).
The bactericidal activity has also been
reported. When 317 strains, representing
204 species and 17 orders of
basidiomycete mushrooms were screened
for antimicrobial activity on human
pathogens, over 45 % of the tested strains
were positive for antibacterial activity (Suay
et al., 2000). The highest activity occurred
among members of the Ganodermatales,
Poriales, Agaricales, and Stereales. Eight
species of the family Ganodermataceae
strongly inhibited Bacillus subtilis; Fomes
fomentarius inhibited growth of
Pseudomonas aeruginosa, Serratia
marcescens, Staphylococcus. aureus, B.
subtilis, and Mycobacterium smegmatis. In
this review, we focus on the potential of
basidiomycete mushrooms as producers of
metabolites with medicinal and agricultural
applications.
Medicinal Applications
Anti-cancer substances of mushroom
origin
Cancer accounts for over 6 million
deaths each year worldwide (Jang et al.,
1997). Prostate cancer only accounts for
33 % of all newly diagnosed malignancies
among men in the United States (Crawford,
2003). Cancer chemopreventive agents
include nonsteroidal anti-inflamatory drugs
(NSAIDs), such as indomethacin, aspirin,
piroxicam, and sulindac. All of these
synthetic products inhibit cyclooxygenase
(COX) functions. This inhibitory activity is
extremely important to cancer
chemoprevention because COX catalyzes
the conversion of arachidonic acid to
proinflamatory substances such as
prostaglandins (PGs) that stimulate cell
growth and suppress the immune response.
COX can also activate carcinogens to
damage genetic material (Jang et al., 1997).
There are at least two kinds of COX
enzymes, COX-1 and COX-2. COX-1
makes PGs to protect the stomach and
kidney from damage; while COX-2 induced
by inflammatory stimuli, such as cytokine,
produces PGs that promote the pain and
inflammation (Vane and Botting, 1998) and
induction to tumor formation (Vane, 2000).
In searching for new cancer treatments
over the past several years, many species
of basidiomycete mushrooms have been
investigated for their anti-cancer properties
(Yang and Jong, 1989). Lucas, (1957) first
demonstrated the anti-cancer activity of
mushrooms. He used extracts of fruiting
bodies of Boletus edulis and other
mushrooms in tests against implanted
Sarcoma 180 line in mice. The anti-cancer
calvacin, a conjugated protein containing
one or more carbohydrate residues was
extracted from the giant puffball Calvatia
gigantea and tested against many
experimental tumors, such as Sarcoma 180,
mammary adenocarcinoma 755, leukemia
L-1210, and HeLa cell lines presenting
significant growth inhibition on those types
of cancer (Lucas, 1957). Many other anticancer compounds of mushroom origin,
including
b-D-glucans,
heteropolysaccharides, glycoproteins,
lectines, and terpenoids have been
investigated. The primary sources of these
compounds are discussed below.
b-D-Glucans
b-D-Glucans are homopolysaccharides
that contain only glucose monomeric units
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(Donald and Judith, 1995; Garrett and
Grishman, 1999). -D-glucans with anti-cancer
activity have been identified from several
species of mushrooms belonging to the
orders Auriculariales, Tremellales, and
Polyporales; families Gasteromycetaidea,
and Agaricomycetaidea through screening
against Sarcoma 180 in mice (Mizuno,
1995). Lentinan, and other glucans isolated
from the shiitake mushroom Lentinus
edodes, have shown anti-cancer activities.
Lentinan showed prominent anti-cancer
activity against implanted Sarcoma 180 and
other synergic and autochthonous tumors
Figure 1. Representation of the (A) Primary structure of (1à3)-b-D-Glucan and (B) b-(1à3) linkage of the
tertiary structure of curdlan. Adapted from Iain and Brown, (1995).
(Wasser, 2002), while a-glucan, administered
at a dose of 20 mg/kg of body weight to
BALB/C mice having implanted solid
Sarcoma 180 was effective with an inhibition
rate of 42% (Zhang and Cheung, 2002).
b-D-glucans sometimes are referred as
biological response modifiers (BRMs)
because they activate the host immune
system. They bind to lymphocyte surfaces or
serum specific proteins, which activate
macrophage, T-helper, NK, and other cellular
effectors. All of the above increase the
production of antibodies as well as
interleukins (IL-1, IL-2) and interferon IFNg
(Mizuno, 1995). The main component of these
substances is (1à3)-b-D-glucan (Wasser and
Weis, 1999) arranged in a triple helical tertiary
configuration as illustrated in Figure 1. This
configuration is known to be important for the
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immune-stimulating activity. For example,
when lentinan and schizophyllan were
denatured to their primary structure with
dimethyl sulfoxide, urea, or sodium
hydroxide, significant reduction in tumor
inhibition was observed. These findings
confirmed the correlation between anticancer activity and the triple helix structure
(Wasser, 2002).
Mushroom b-D-Glucans preventing
oncogenesis, showed direct anti-cancer
activity against various allogeneic and
syngenic tumors, and tumor metastasis
(Wasser, 2002). Significant reductions in
size of the tumors were observed in mice
treated with lentinan. Lymphocytes
extracted from AKR mice treated with
lentinan for 7 days were inoculated into the
nude mice.
This was followed by
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of agricultural and medicinal applications of basidiomycete mushrooms
implantation of human colon-carcinoma cell
lines into these mice. The nude mice
treated with lymphocytes extracted from the
AKR mice, developed much smaller tumors
than those non-treated with the same
lymphocytes (Ng and Yap, 2002).
Heteropolysaccharides
Heteropolysaccharides consist of
monosaccharides linked together by
glycosidic
bonds.
They
are
heteropolysaccharides because they
contain more than one type of monomeric
unit, such as D-glucose, D-fructose, Dgalactose, L-galactose, D-mannose, Larabinose, and D-xylose (Garrett and
Grishman, 1999; Voet and Voet, 1995).
Anti-cancer heteropolysaccharides
containing chains of xylose, mannose,
galactose, and uronic acid have been
isolated from several species of
basidiomycete mushrooms (Wasser and
Weis, 1999). For example, EA501, isolated
from golden needle Flammulina velutipes
consisted of D-glucose 42.3%, D-galactose
17.3%, D-mannose 12.2%, D- xylose 6.7%,
and L-arabinose 14.7% (Ikekawa et al.,
1982).
Several
other
heteropolysaccharides have been identified
from the chinese mushroom ‘huangmo.’ F10
(a mixture of galactose-containing
heteroglycan and b-D-glucan), FA-1 and FA2 (containing b-D-glucan with galactose,
hetero-glycan and protein), FII-2 (consisting
of b-D-glucan), FIII-1-b and FIII-2-b
[containing (1à6) b-D-glucosyl branched
(1à3) b-D-glucan] reduced cancer activity in
mice implanted with Sarcoma 180 (Ma et
al., 1991).
Other heteropolysaccharides isolated
from culture fluids of Agaricus blazei
containing glucomannan with a chain of bD-glucopyranosyl-3-0-b-glucopyranosyl
residues as a side chain also reduced
cancer activity in mice implanted with
Sarcoma 180 cells (Mizuno et al., 1999).
Another anti-cancer water-soluble
heteropolysaccharide, S-3-B (1à6)-branched
(1à3)-b-glucan was isolated from the fruiting
bodies Cryptoporus volvatus. Enzymatic
analysis using exo-(1à3)-b-D-glucosidase
and methylation analysis indicated that this
heteropolysaccharide has a main chain
composed
of
b-(1à3)-linked
Dglucopyranosyl residues and b-(1à6)-linked
D-glucopyranosyl residues attached as side
chains approximately every fourth sugar
residue of the main chain.
This
polysaccharide showed anti-cancer activity
when tested against Sarcoma 180 implanted
in mice (Kitamura et al., 1994). In a recent
study, a new heteropolysaccharide,
Ganopoly®, extracted from Ganoderma
lucidum, increased production of antibodies
and concentrations of interleukin-2,
interleukin-6 and interferon IFNg, and reduced
levels of tumor-necrosis factor (TNF-a) in
most patients (Gao et al., 2003).
Glycoproteins
Glycoproteins, are proteins covalently
attached to carbohydrates such as glucose,
galactose, lactose, fucose, sialic acid, Nacetylglucosamine, N-acetylgalactosamine,
etc. (Donald and Judith, 1995). Several
glycoproteins produced by basidiomycetes
have been studied for their anti-cancer
activity. For instance, KS-2 extracted from
mycelia of Lentinus edodes containing a amannan product linked to a peptide
composed of serine, threonine, alanine, and
other amino acid residues inhibited growth
of both Sarcoma 180 and Ehrlich tumors (Fujii
et al., 1978). FIo-A, a water-soluble
glycoprotein, isolated from the mycelia of
Ganoderma tsugae showed anti-cancer
activity on Sarcoma 180 implanted in mice.
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FIo-A consisted of 9.3 % protein, heteroglyco-chain of mannose and xylose (Zhang
et al., 1994). FIo (water-soluble glycoprotein)
and FIII-1 and FIII-2 (water-insoluble
glycoproteins) extracted from the oyster
mushroom Pleurotus citrinopileatus
presented a very strong anti-cancer activity
against Sarcoma 180 implanted in mice. The
FIo glycoprotein consisted of protein,
mannose, glucose, arabinose, and
galactose. Both the water-insoluble, FIII-1
and FIII-2, showed protein-containing b-Dglucans (Zhang et al., 1994). Similar anticancer glycoproteins were identified from
fruiting bodies of Tricholoma giganteum. FIa glycoprotein (water-soluble) was
composed of a mixture of a-D-glucan and
xyloglucomannan. FA-1 contained 1 % of
protein, FII-1, contained 7.8 % protein, and
FIII-2-a, b, and c, consisted of xylose,
galactose, and protein. Both water-soluble
and water-insoluble glycoproteins showed
strong anti-cancer activity against Sarcoma
180 implanted in mice (Mizuno et al., 1995).
Lectins
Lectins are glycoproteins that bind
carbohydrates with high specificity. They
agglutinate red blood cells or precipitate
polysaccharides. They identify vital cells,
such as erythrocytes, and bind complex
carbohydrates and proteins. (Donald and
Judith, 1995). It has been reported that some
species of basidiomycetes, including
Agaricus sp., Polyporus sp., Agrocybe sp.
produce lectins that are useful to study
polysaccharides and glycoproteins, as well
as enzymatic modifications and cellular
membranes. Because of their characteristic
sequences, lectins can be used to diagnose
cancer cells, or as specific binding moieties
for targeted cancer therapy. For example,
N-acetylgalactosamine, a specific lectin
100
isolated from Grifola frondosa, agglutinated
all types of erythrocytes equally (Griffin, 1994;
Wasser and Weis, 1999). Agaricus
bisporus agglutinin (ABA) reacted with
monosaccharides and possessed a potent
anti-cancer effect on malignant colon
epithelial cells (Wu et al., 2003). A lectin,
AAL, isolated from the edible mushroom
Agrocybe aegerita, showed strong growth
inhibition of human tumor cell lines, such as
HeLa, SW480, SGC-7901, MGC80-3,
BGC-823, HL-60, and mouse Sarcoma 180
(Zhao et al., 2003). Another lectin isolated
from the mushroom Polyporus adusta
showed antiproliferative activity against
tumor cell lines and mitogenic activity of
splenocytes. A large range of other
carbohydrates
inhibited
the
hemagglutinating activity of this lectin. NaOH
or HCl and high temperature also affected
its activity. However, divalent metallic
chlorides tested at 1.25-10 μM, such as
CaCl2, MgCl2, ZnCl2, MnCl2 and AlCl3 favored
its activity and FeCl3 at 10 μM increased the
activity of this lectin by 100% (Wang et al.,
2003).
Terpenoids
Terpenoids are the combination of two
or more molecules of 2-methyl-2, 3butadiene, also known as isoprene (a fivecarbon unit that is abbreviated C5).
Terpenoids are subdivided according to the
number of carbon atoms. For example, a
monoterpenoid (C10) consists of two
subunits of isoprene, a sesquiterpene (C15)
consists of three isoprene units, and so on
(Garrett and Grishman, 1999). Many
terpenoids isolated from Polyporales and
Ganodermatales mushrooms have anticancer properties. There have been
reported about 100 different types of
terpenoids obtained from fruiting bodies of
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furanoganoderic acids (Figure 2), lucidinic
acids, ganolucidinic acids, lucidic acids
Ganoderma lucidum and G. applanatum.
For
instance,
ganoderic
acids,
Figure 2. Representation of the chemical structures of three different terpenoids isolated from
Ganoderma lucidum. Adapted from Wasser and Weis, (1999).
Furanoganoderic acid
Ganoderic acid A
Ganoderic acid G
(Figure 3) and other triterpenoid components,
including methyl lucidenate P, methyl
ganoderic acid O, trideacetyl ganoderic acid
T have been investigated (Iwatsuki et al.,
2003; Wasser and Weis, 1999).
Omphalotus
olearius
and
Lampteromyces japonicus produce a
cytotoxic tricyclic sesquiterpene, illudin
S=lampterol, which has strong anti-cancer
properties and inhibits cancer cell growth by
a unique mechanism. Activated by
glutathione, it is then bound to DNA. This
prevents DNA replication and leads to cell
death (Wasser and Weis, 1999). Three
different triterpene aldehydes, including
lucialdehydes A, B, and C, were isolated
from fruiting bodies of G. lucidum. Their
structures were determined and their
cytotoxicity tested against Lewis lung
carcinoma, T47D, Sarcoma 180, and Meth-
Figure 3. Representation of the chemical structures of different terpenoids extracted from Ganoderma
lucidum. LA, Lucidinic acid; GLA, Ganolucidic acid; L, Lucidic acid ; GA, Ganoderic acid. Adapted from
Iwatsuki et al., (2003).
LA-A: R1β-CH, R2=H
LA-D1: R1=R2=O
GA-B: R1=β-OH, R2=O
GA-C2: R1=β-OH, R2=α-OH
GA-K: R2=O, R2=α-OH
GLA-D
GA-A: R1=β-OH, R2=α-OH
GA-C1: R1=β-OH, R2=O
GA-J: R1=O, R2=α-OH
LA-B: R1=R5=O4=R2=R3=H2, R4=β-OH
LA-C: R1=R4=β-OH, R2=R3=H, R5=O
LA-E1: R1=R5=O, R2=R3=H, R4=α-OH
LA-G: R1=O, R2=OH, R3=R4=H, R5=α-OH
LA-H: R1=β-OH, R2=R4=H, R3=OH, R5=O
GLA-C
LA-I
GA-D
L-B
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A tumor cell lines. Of these three lucialdehyde
terpenoids, lucialdehyde C showed the highest
cytotoxicity in all the tumor cell lines tested
(Gao et al., 2002).
Agricultural Aplications
Antibacterial Activity
When 317 strains, representing 204
species and 17 orders of basidiomycete
mushrooms were screened for antimicrobial
activity on human pathogens, over 45 % of the
tested strains were positive for antibacterial
activity (Suay et al., 2000). The highest activity
occurred among members of the
Ganodermatales, Poriales, Agaricales, and
Stereales. Eight species of the family
Ganodermatacea, including three strains of
Ganoderma lucidum, three of G. pfeifferi, and
two of G. resinaceum strongly inhibited
Bacillus subtilis. Members of the family
Coriolacea, for instance Laetiporus
sulphureus showed bactericidal activity
against
Serratia
marcescens,
Staphylococcus aureus, and Bacillus subtilis
(Suay et al., 2000). Ganoderma applanatum
inhibited Gram-positive bacteria such as
Bacillus cereus and Staphylococcus aureus
were less inhibitory against Gram-negative
bacteria, including Escherichia coli and
Pseudomonas aeruginosa (Smania et al.,
2001). The woody tinder fungus, Fomes
fomentarius inhibited growth of P. aeruginosa,
Serratia marcescens, S. aureus, B. subtilis,
and Mycobacterium smegmatis, a relative of
the pathogenic Mycobacterium tuberculosis.
Other reports have shown that Ganoderma
lucidum has antibacterial activity against
Staphylococci, Streptococci, and Bacillus
pneumoniae and against Gram-positive
bacteria (Brian, 1951). Lentinan from shiitake
mushroom Lentinus edodes inhibited
Mycobacterium tuberculosis and Listeria
102
monocytogenes (Chihara, 1992). Three
antibacterial substances extracted with
chloroform, ethyl acetate, or water from
fruiting bodies of L. edodes are active
against Streptococcus sp., Actinomyces
sp., Lactobacillus sp., Prevotella sp., and
Porphyromonas sp. Other bacteria, such
as Enterococcus sp., Staphylococcus sp.,
Escherichia sp., and Bacillus sp. were
relatively resistant to these substances. It
was suggested that these active compounds
might be similar to lenthionine, disulphide
derivative and lentinan types, respectively
(Hirasawa et al., 1999). Crude culture fluids
of L. edodes presented antibacterial activity
against Streptococcus pyogenes,
Staphylococcus aureus, and Bacillus
megaterium (Hatvani, 2001). Coprinol is
isolated from culture fluids of Coprinus sp.
with antibacterial activity against many multidrug resistant Gram-positive bacteria invitro (Johansson et al., 2001). The fungicide
strobilurin, F 500 enhances resistance of
tobacco to the wild fire pathogen
Pseudomonas syringae pv. tabaci. The
mechanism of action of strobilurin F 500 is
by inducing cellular responses to the
pathogen attack. It induces production of
endogenous salicylic acid and
pathogenesis-related proteins that usually
are used as molecular markers for disease
resistance (Herms et al., 2002).
Antifungal Activity
In addition to their antibacterial potential,
some basidiomycete mushrooms have
antifungal activity. For instance, the oyster
mushroom Pleurotus ostreatus inhibits the
growth of Aspergillus niger the causal agent
of aspergillosis, a lung disease that
seriously threatens people with
compromised
immune
systems
(Gerasimenya et al., 2002). A member of
the Poriales, Gloephyllum sepiarium,
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LORETO ROBLES-HERNÁNDEZ, ANA CECILIA-GONZÁLEZ- FRANCO, JUAN MANUEL SOTO-PARRA AND FEDERICO MONTES-DOMÍNGUEZ: Review
of agricultural and medicinal applications of basidiomycete mushrooms
inhibited growth of Sacharomyces
cerevisiae and Aspergillus fumigatus (Suay
et al., 2000). A novel ribosome-inactivating
protein, hypsin, isolated from fruiting bodies
of the edible mushroom Hypsizigus
marmoreus, inhibited the mycelial growth of
several fungal species, such as
Mycosphaerella
arachidicola,
Physalospora
piricola,
Fusarium
oxysporum, and Botrytis cinerea with an IC50
of 2.7, 2.5, 14.2, and 0.06 mM, respectively
(Lam and Ng, 2001b). Another ribosomeinactivating protein, lyophyllin, isolated from
fruiting bodies of the mushroom Lyophyllum
shimeji showed antifungal activity against P.
piricola and M. arachidicola with an IC50 of
70 mM (Lam and Ng, 2001a). The 10-oxotrans-8-decenoic acid (ODA) and 1-octen3-ol produced by Agaricus bisporus and
other species of mushrooms during the
enzymatic breakdown of linoleic acid
(Champavier et al., 2000; Okull et al., 2003)
inhibited the mycelial growth of Penicillium
expansum, the common food spoilage
organism, at concentrations of 1.25 mM and
at pH 3.5 (Okull et al., 2003). Lentin, a new
antifungal protein of 27.5 MW extracted from
fruiting bodies of Lentinus edodes inhibits
P. piricola, Botrytis cinerea, and M.
arachidicola (Ngai and Ng, 2003). Three
different triterpenes, applanoxidic acids A,
C, and F, isolated from Ganoderma annulare
inhibit mycelial growth of Microsporum
cannis and Trichophyton mentagrophytes
at concentrations of 500 to 1000 mg/ml
(Smania et al., 2003). Some isolates of G.
applanatum were highly antagonistic against
to the rhizomorph of Armillaria luteobubalina
(Perch, 1990).
Strobilurins is another class of fungicidal
compounds extracted from mycelia of the
mushroom Strobilurus tenacellus.
Strobilurins A and B were highly active by
inhibiting respiration of yeast and other
filamentous fungi (Anke and Oberwinkler,
1977). The biological activity of strobilurins
involve ubihydroquinone cytochrome C
reductase, which plays a crucial role in
respiration (Gatti and Tzagoloff, 1990). Its
activity, however, depends of the presence
of
(E)-b-methoxyacrylate
moiety
(Fredenhagen et al.,1990). The antifungal
(E)-b-methoxyacrylates of strobilurin C and
outdemansin B from cultures of Xerula
longipes inhibit many phytopathogenic fungi.
Like the strobilurins A and B, they also inhibit
fungal respiration (Anke et al., 1983).
Strobilurin E is another antifungal compound
of the (E)-b-methoxyacrylate class extracted
from mycelial cultures of Crepidotus
fulvotomentosus. In addition to inhibiting
fungal respiration, it can induce cell
deformations (Weber et al., 1990).
Strobilurins D and F are other strobilurins,
extracted from mycelial cultures of the
basidiomycete Cyphellopsis anomala that
have cytostatic and antifungal antibiotics of
the (E)-b-methoxyacrylate class. These
strobilurins inhibit many fungi, and like
strobilurins A and B, they also are potent
inhibitors of respiration (Weber et al., 1990).
Strobilurin M isolated from the mushroom
Mycena sp. also showed antifungal and
cytostatic activities (Deferner et al., 1998).
Other strobilurins F, G, and H extracted from
culture fluids of Bolinea lutea Sacc. inhibit
Aspergillus fumigatus, Botrytis cinerea,
Microsporum cannis and Sporotrichum
schenckii. These compounds reduce fungal
respiration; however, they might be different
from the analogs previously described
(Fredenhagen et al., 1990).
Helminthicidal Activity
There are abundant nutrients and a large
variety of life forms in soil. There are groups
of microorganism for relationships and
associations that includes predation or
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LORETO ROBLES-HERNÁNDEZ, ANA CECILIA-GONZÁLEZ- FRANCO, JUAN MANUEL SOTO-PARRA AND FEDERICO MONTES-DOMÍNGUEZ: Review
of agricultural and medicinal applications of basidiomycete mushrooms
parasitism. The relationship between fungi
and nematodes is especially interesting to
scientists. Nematode destroying fungi are
those that trap and feed on nematodes by
predation and parasitism. Fungal species that
trap or consume nematodes mainly belong to
Zygomycetes, Basidiomycetes and
Hyphomycetes found in agricultural soil and
in decaying organic debris (Barron, 1977).
Fresenius in 1852 (cited in Barron, 1977)
observed a fungus that produced scattered
conidiophores and clusters of large two-celled
conidia. He named this fungus Arthrobotrys
oligospora. Later, Woronin (1870) [cited in
Barron, 1977] observed that aerial hyphae of
Arthrobotrys curved and fused with
themselves to form nets of hyphae. Finally,
Zopf (1888) [cited in Barron, 1977] proved that
these hyphal nets trapped motile nematodes
and penetrated them. The fast growing hyphae
consumed and killed the nematodes.
Approximately fifty years later, Drechsler
(1933) [cited in Barron, 1977] showed that
adhesive fungal nets were responsible for
holding the captured nematodes.
The
nematode-destroying
basidiomycetes, the Nematoctonus, were first
described by Drechsler (1941) [cited in
Barron, 1977] as he discovered that two
species possessed clamp connections but
lacked sexual states. To date, a total of nine
species have been described having this
Nematoctonus predatory and endoparasitic
ability. Predaceous species capture
nematodes by means of adhesive knobs on
prostrate hyphae. Endoparasitic species
have adhesive knobs on the spores, which
attach directly to the cuticle of the nematode
(Barron, 1977). The adhesive device is a
secretory cell with an hourglass shape. The
cells bind the so tightly that they completely
immobilize nematodes (Barron, 1977; Thorn
and Barron, 1984).
Some species of Nematoctonus produce
104
small basidiocarps in-vitro similar to the
Agaricales of the hymenial basidiomycetes.
The basidiospores produced are
discharged and germinate in the presence
of nematodes and form adhesive knobs
(Barron, 1977; Thorn and Barron, 1984).
Hohenbuehelia, a gilled fungus in the
Pleurotiaceae
(Agaricales,
Hymenomycetes), is teleomorphic. At least
10 species of gilled fungi belonging to the
genera Hohenbuehelia, Pleurotus, and
Resupinatus can attack nematodes by
adhesion or through the production of toxins
(Thorn and Barron, 1984).
Some species of Nematoctonus, such
as Nematoctonus haptocladus and N.
concurrens produce nematotoxins. As
nematodes touch the adhesive spores of
these species, they became immobile and
die before being penetrated. Nematode
death occurs within 24 hours after
attachment. This immobilization prevents
host from escaping. When the female
nematodes are attacked, the nematotoxin
prevents eggs to hatch (Barron, 1977).
Concluding Remarks
Basidiomycetes is a highly evolved
group of fungi. These fungi convert organic
carbon to inorganic carbon in the carbon
cycle. Edible species of basidiomycetes are
well known. The commercial mushrooms
Agaricus bisporus, shiitakii mushroom
(Lentinus edodes) and oyster mushroom
(Pleurotus spp.) are the most common.
However, many wild mushrooms, such as
Fistulina hepatica, Sparassis crispa,
Albatrellus sp., Grifola frondosa, the bear’s
head (Hericium erinaceum), and chicken of
the woods (Laetiporus sulphureus) are also
edible. Medicinal mushrooms offer an
advantage in that their active ingredients are
safe for humans. Many compounds, such
as b-D-glucans, heteropolysaccharides,
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LORETO ROBLES-HERNÁNDEZ, ANA CECILIA-GONZÁLEZ- FRANCO, JUAN MANUEL SOTO-PARRA AND FEDERICO MONTES-DOMÍNGUEZ: Review
of agricultural and medicinal applications of basidiomycete mushrooms
glycoproteins, lectines, and terpenoids
inhibit tumor cell lines. The antimicrobial
properties by certain basidiomycetes
provide human and plant disease control that
is generally safe and effective. Several
species of basidiomycetes inhibit both
Gram-positive and Gram-negative human
pathogenic bacteria. Other basidiomycetes
have demonstrated antifungal activity
against both human and plant pathogens
and the Nematoctonus, are active against
several plant pathogenic nematodes.
Basidiomycetes offer a unique set of
compounds with potential to address
agricultural and medicinal challenges.
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Este artículo es citado así:
Robles-Hernández Loreto, Ana Cecilia-González- Franco, Juan Manuel Soto-Parra and Federico MontesDomínguez.R. 2008. Review of agricultural and medicinal applications of basidiomycete mushrooms. TECNOCIENCIA
Chihuahua 2(2): 95-107.
Resúmenes curriculares de autor y coautores
LORETO ROBLES-HERNÁNDEZ. Es profesor de la Facultad de Ciencias Agrotecnológicas de la Universidad Autónoma de Chihuahua.
Obtuvo su Doctorado en la Universidad de Idaho, USA, su Maestría y Licenciatura en la Universidad Autónoma de Chihuahua.
Actualmente conduce su investigación sobre enfermedades bacterianas, enfermedades virales, control biológico y diagnóstico
de enfermedades de plantas. El Dr. Robles imparte los cursos de Fitopatología, Microbiología, Control Biológico y Fisiología de
Poscosecha. Es asesor de estudiantes de posgrado y forma parte de comité de asesores del posgrado. Actualmente es
responsable del área de diagnóstico de enfermedades y fisiología de poscosecha en el laboratorio de Microbiología Aplicada,
Fitopatología y Fisiología de Poscosecha de la Facultad de Ciencias Agrotecnológicas-UACH.
106
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LORETO ROBLES-HERNÁNDEZ, ANA CECILIA-GONZÁLEZ- FRANCO, JUAN MANUEL SOTO-PARRA AND FEDERICO MONTES-DOMÍNGUEZ: Review
of agricultural and medicinal applications of basidiomycete mushrooms
ANA CECILIA GONZÁLEZ-FRANCO. Es profesor de la Facultad de Ciencias Agrotecnológicas de la Universidad Autónoma de Chihuahua.
Obtuvo su Doctorado en la Universidad de Idaho, USA, su Maestría y Licenciatura en la Universidad Autónoma de Chihuahua.
Actualmente conduce su investigación sobre enfermedades fúngicas, enfermedades virales y control biológico. Imparte las
cátedras de Interacción microorganismo planta, Bioquímica, Química y Biotecnología. Asesora estudiantes de posgrado y forma
parte del comité de asesores de posgrado. Es miembro del Sistema Nacional de Investigadores. Actualmente es responsable del
área de microbiología aplicada y biología molecular en el laboratorio de Microbiología Aplicada, Fitopatología y Fisiología de
Poscosecha de la Facultad de Ciencias Agrotecnológicas-UACH.
JUAN MANUEL SOTO-PARRA. Es profesor de la Facultad de Ciencias Agrotecnológicas de la Universidad Autónoma de Chihuahua. Obtuvo
su Maestría en 1992 y su licenciatura en 1981 en la misma institución. Ocupó el cargo de director en la Facultad de Ciencias
Agrotecnológicas-UACH del 2000 al 2004; sus áreas de especialización son Fisiología y Nutrición Vegetal, con énfasis en la
Fisiología de la Producción en los cultivos del manzano y nogal pecanero. Actualmente se encuentra realizando sus estudios de
doctorado en el área de Recursos Naturales de la facultad de Zootecnia –UACH.
FEDERICO MONTES-DOMÍNGUEZ. Es profesor de la Facultad de Ciencias Agrotecnológicas de la Universidad Autónoma de Chihuahua.
Obtuvo su Maestría en 1998 y su licenciatura en 1989 en la misma institución; realiza investigación en las áreas de Fisiología y
Nutrición Vegetal, con énfasis en la Fisiología de la Producción en los cultivos del manzano y nogal pecanero. Actualmente ocupa
el cargo de Responsable Técnico en la Unidad Experimental «la Semilla» de la Universidad Autónoma de Chihuahua.
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