Journal of Ethnopharmacology 74 (2001) 89 96

www.elsevier.com/locate/jethpharm

Short Communication

Screening antifungal activities of selected medicinal plants

Emma Nelly Quiroga, Antonio Rodolfo Sampietro 1,
Marta Amelia Vattuone *,2
Catedra de Fitoqumica, Instituto de Estudios Vegetales Dr. Antonio R. Sampietro, Facultad de Bioqumica, Qumica y Farmacia,
Uni6ersidad Nacional de Tucuman, Ayacucho 471, 4000 San Miguel de Tucuman, Argentina
Received 19 November 1999; received in revised form 26 August 2000; accepted 22 September 2000

Abstract
Plants synthesise a vast array of secondary metabolites that are gaining importance for their biotechnological
applications. The antifungal activity of the ethanolic extracts of ten Argentinean plants used in native medicine is
reported. Antifungal assays included radial growth inhibition, disk and well diffusion assays and growth inhibition by
broth dilution tests. The chosen test fungi were yeasts, microfungi and wood-rot causing Basidiomycetes. Extracts of
Larrea di6aricata, Zuccagnia punctata and Larrea cuneifolia displayed remarkable activity in the assays against the
majority of the test fungi. In addition to the former plants, Prosopanche americana also inhibited yeast growth.
2001 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Fungi; Antifungal activities; Bioassays

1. Introduction
Fungi occur ubiquitously and are well adapted
to use a wide range of substrates as their carbon,
nitrogen and energy source. The growth of many
fungi is especially difficult to control because of
their ability to metabolize many substances.
* Corresponding author. Tel.: + 54-381-4247752, ext. 260;
fax: + 54-381-4248025.
E-mail address: sampietro@tucbbs.com.ar (M.A. Vattuone).
1
Deceased.
2
Researcher from the Consejo Nacional de Investigaciones
Cientficas y Tecnicas, Buenos Aires, Argentina.

These organisms can cause serious diseases in

plants, animals, and humans. Many Basidiomycetes such as Ganoderma applanatum,
Lenzites elegans, Pycnoporus sanguineus and
Schizophyllum commune were associated with
white-rot of living trees and on logs, dead twigs
and slumps (Harsh and Bisht, 1997). They can
degrade wood, leading to economic losses in
forestry. Therefore, it is important to find products or methods to protect living trees and timber
from decay (Blanchette, 1994).
Antifungal secondary metabolites isolated from
the heartwood of plants (Reyes Chilpa et al.,
1987) have been considered to contribute to tree

0378-8741/01/$ - see front matter 2001 Elsevier Science Ireland Ltd. All rights reserved.
PII: S 0 3 7 8 - 8 7 4 1 ( 0 0 ) 0 0 3 5 0 - 0

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E.N. Quiroga et al. / Journal of Ethnopharmacology 74 (2001) 8996

resistance against wood destroying fungi. For this

reason, it is of growing interest to detect antifungal active compounds to control the development
of these wood-destroying fungi.
Plants produce a great deal of secondary
metabolites, many of them with antifungal activity. Well-known examples of these compounds
include flavonoids, phenols and phenolic glycosides, unsaturated lactones, sulphur compounds, saponins, cyanogenic glycosides and
glucosinolates (Gomez Garibay et al., 1990; Bennett and Wallsgrove, 1994; Grayer and Harborne,
1994; Osbourne, 1996).
We present results from a screening for antifungal higher plant extracts obtained from selected
plants of the Northwest of Argentina. The chosen
plants are all used in traditional medicine.

2. Materials and methods

Penicillium notatum Westling, Trichoderma spp.

and Aspergillus niger Thom and Church. These
fungi were supplied by Instituto Nacional de Tecnologa Agraria, Tucuman, Argentina.
The yeast strains used in this study were Saccharomyces carlsbergensis Hansen (IEV 002) and
Rhodotorula spp (IEV 001). They were obtained
from Laboratorio de Micologa, Instituto de Microbiologa, UNT, Argentina.

2.3. Preparation of ethanolic extracts

Ten grams of ground air-dried plant material
were shaken in 100 ml EtOH 96 at 40C for 48 h
(40 cycles/min). The insoluble material was
filtered by filter paper (Whatman No. 4) and
evaporated to dryness under reduced pressure at
40C. The extract was weighed and dissolved in
EtOH 96 at 0.100 and 0.035 g ml 1 final concentration for antifungal tests against yeasts and
mycelial fungi.

2.1. Plant material

2.4. Fungal cultures
Some plants were purchased from the market
and others were collected in different sites of the
Northwest of Argentina. Plants were identified by
Dr A.R. Sampietro at the chair in Phytochemistry
of the Universidad Nacional de Tucuman (UNT),
Argentina (Toursarkissian, 1980). Voucher specimens were deposited in the Herbarium of the
Instituto de Estudios Vegetales (IEV), Facultad
de Bioqumica, Qumica y Farmacia, UNT (Tucuman, Argentina).
The used parts were leaves, stems, flowers,
roots, tree barks and, in some cases, the whole
plant.

2.2. Microorganisms
The following wood-destroying fungi were
used: L. elegans Spreng ex Fr. (IEV 012), G.
applanatum (pers, ex Walls) Pat. (IEV 017), P.
sanguineus (L. Ex Fr.) Murr. (IEV 006), and S.
commune Fr. (IEV 009). These strains were obtained from the Botanical Institute Miguel Lillo,
Tucuman, Argentina, and were originally isolated
from local decaying wood. Other phytopatogenic
fungi used were Fusarium oxysporum Schlecht,

Filamentous fungi were inoculated in 250 ml

Erlenmeyer flasks with 50 ml growth medium:
malt extract broth (15 g malt extract and 5 g
peptone in 1 l distilled water). Then, it was incubated at 30C until a strong mycelial growth was
obtained (810 days). Yeasts were grown in the
same medium and were incubated at 30C for
2448 h. Fungal cultures were maintained on
malt extract broth plus 15 g Bacto agar l 1 (1.5%
malt extract, 0.5% peptone and 1.5% Bacto agar).

2.5. Test for antifungal acti6ity

The in vitro biological activity of alcoholic
plant extracts was assessed on basis of hyphal
radial growth rate of filamentous fungi, and
growth rate of yeasts in the presence and absence
of the plant extract. Different volumes of each
alcoholic extract (0.035 g ml 1) from 0.2 to 0.4
ml were poured into assay flasks containing 16 ml
hot sterilised growth medium (malt agar 1.5%)
and the final volume was adjusted to 17 ml with
EtOH. After it was thoroughly mixed with a
vortex, aliquots of 5 ml treated medium were

E.N. Quiroga et al. / Journal of Ethnopharmacology 74 (2001) 8996

poured into Petri dishes (60 15 mm). Control

plates were treated with EtOH only. The plates
were left to stand overnight after pouring in a
sterile hood to remove the solvent completely. The
assay was performed by placing a 3-mm diameter
plug of growing mycelia onto the centre of a Petri
dish containing the alcoholic extract in the
medium. This plug was taken from an 8- to 10-day
culture.
The fungal strains P. notatum, Trichoderma spp.
and A. niger, cultured at 30C for 7 10 days,
easily produced spores. A spore suspension was
prepared in 0.9% NaCl solution at a known inoculum density (2.5 104 ml 1 fungal spores). Ten
microliter aliquots of this suspension were placed
onto the centre of the Petri dish as already described. These suspensions were prepared immediately before the test was carried out. Plates were
incubated aerobically at 30C in a humidity environment to prevent the growth medium from
drying out. Three replicates were run simultaneously. The radial growth of mycelia (colony
diameter (mm)) in all plates was measured 5 days
after inoculation. Each datum point is the mean of
at least four measurements of a growing colony.
The percentage of growth inhibition was calculated from mean values as (Reyes Chilpa et al.,
1997):

91

plus 2% Bacto agar cooled at 45C. This was then

poured into 9.1 cm diameter Petri dishes, and
maintained for 1 h at room temperature. Small
wells were cut in the agar plate using a cork borer
(5 mm). A fixed volume of different alcoholic
extract concentration and a carrier solvent control
were loaded in the wells. The dishes were then
inverted and preincubated at 4C for 2 h to allow
uniform diffusion into the agar. After preincubation, the plates were inverted and incubated aerobically at 30C for 48 h. The diameter of the
inhibition zone around each well was recorded in
four different directions.

2.6.2. Paper disk diffusion assays

Agar plates were poured in the same mode as
already described. Sterile paper disks (Whatman
No. 4 paper, 5 mm diameter) were impregnated
with 10 ml different vegetal alcoholic extract dilutions of known concentrations. The disks were
allowed to dry and then six disks were spaced on
the agar surface of each Petri dish. A disk negative
control (10 ml ethanol) was included. The diameter
of the inhibition zone around the disks was measured after 48 h at 30C. The values were the
average (mm) of four measurements per disk,
taken at four different directions in order to mistake minimisation. The experiment involved the
use of at least three plates for each test.

% Inhibition=
mycelial growth in control mycelial growth in extract plant
100
mycelial growth in control

2.6. Test for biological acti6ity against yeasts

In these assays, two agar diffusion techniques (
Camm et al., 1975; Cole, 1994; Torres et al., 1998)
and broth dilution tests were employed.
The yeast cultures were prepared by inoculating
the microorganism to be tested in a 250 ml Erlenmeyer flask containing 50 ml malt-broth medium,
followed by incubation at 30C for 24 48 h or
until the turbidity matched the Mac Farland tube
No. 1.

2.6.1. Agar well diffusion assays

An aliquot of 50 ml inoculum preparation was
added to 20 ml melted extract malt-broth medium

2.6.3. Dilution test

This test was used for minimal inhibitory concentration (MIC) determination. A 96-well plastic
microplate was used. Each well contained malt
extract broth (15 g malt extract and 5 g peptone in
1 l distilled water), plus a fixed volume of serially
diluted plant extracts. Each well was inoculated
with a 10 ml aliquot of the yeast inoculum prepared according to Section 2 in a final volume of
0.15 ml. The controls contained malt extract broth
plus plant extract. Incubations were performed at
30C for 24 h. Yeast growth was quantified by
A550 nm using an automatic microplate reader
Model 550 (Bio-Rad Laboratories, Richmond,
CA).
MIC was defined as the lowest concentration of
plant extract to which no yeast growth was observed after incubation at 30C for 24 h.

E.N. Quiroga et al. / Journal of Ethnopharmacology 74 (2001) 8996

92

3. Results and discussion

The antifungal activity of crude ethanolic extracts of ten medicinal plants used in the traditional medicine of the Northwest of Argentina
was tested. Ethnobotanical data are shown in
Table 1. As this table shows, the antifungal
screening was performed in the whole plant when
the selected plant was herbaceous or a woody
shrub. When it was a tree, only defined parts were
chosen.
The plant antifungal activity was assayed
against eight filamentous fungi and two yeasts.
The growth inhibitory activities of the alcoholic
extracts of the different Argentine plants against
filamentous fungi are summarized in Table 2. The
data indicate that alcoholic extracts of Zuccagnia
punctata and Larrea di6aricata have considerable
in vitro activity against all filamentous fungi
tested. Extracts of Larrea cuneifolia have no activity only against F. oxysporum. The Schkuhria
pinnata extract did not inhibit the growth of all
the filamentous fungi assayed.

Some members of the Aspergillus and Fusarium

genera are well known to produce aflatoxins.
These secondary metabolites are potent carcinogens, hepatotoxins, teratogens and inmunosuppresive compounds (Ciegler, 1975). F. oxysporum
produces phytotoxic fusaric acid and lycomarasmin (Ueno et al., 1977). A. niger produces potent
mycotoxins on foodstuffs and is the most prevalent fungus affecting corn (Marassas, 1991). These
fungi represent threats not only to the health of
crops, but also to animals and humans ingesting
contaminated feeds and foods.
The alcoholic extract from L. di6aricata effectively reduced the growth of P. notatum in maltagar medium. Samples of 2, 3 and 4 mg dry
extract/plate (0.4, 0.6 and 0.8 mg ml 1 dry matter
in culture medium) produce 47, 68 and 89% of
inhibition, respectively (Fig. 1).
Extract from Z. punctata inhibited mycelial
growth of G. applanatum and L. elegans (Fig. 2).
The aqueous and alcoholic extracts from Phytolacca dioica and Zinnia peru6iana showed antimicrobial activity against Gram-positive and

Table 1
Ethnobotanical data of the studied plants
Family

Botanical name

Common name

Used parts

Popular uses

Zygophyllaceae

Larrea di6aricata Cav

Jarilla, jarilla hembra

Whole plant

Zygohyllaceae

Larrea cuneifolia Cav

Jarilla, jarilla macho

Whole plant

Equisetaceae
Compositae

Cola de caballo
Canchalahua

Whole plant
Whole plant

Compositae
Leguminosae

Equisetum giganteum L.
Schkuhria pinnata Lam O.
Kuntzi
Zinnia peru6iana L
Zuccagnia punctata Cav

Whole plant
Whole plant

Leguminosae

Acacia ca6en (Mol) Molina

Chinita del campo

Jarilla pispito, jarilla de la
Puna, pus-pus
Churqui, tusca, espinillo

Vulnerary, antirheumatic,
emmenagoge,
antiinflamatory
Vulnerary, antrheumatic,
emmenagoge,
antiinflamatory
Diuretic, astringent
Antibiotic, vulnerary,
phototoxic
Vulnerary, phototoxic
Vulnerary

Phytolaccaceae

Phytolacca dioica L o
Pircunia dioica (L) Moq.
Prosopanche americana (R.
Br) Baillon o P.burmeisteri
De Bary
Schinus molle L.

Hydnoraceae

Anacardiaceae

Ombu
Guaycuru santiagueno, flor
de tierra
Molle, pimienta del diablo,
aguaribay

Leaf, stem, bark Antiseptic, vulnerary,

of a tree
cicatrizant
Whole plant
Vulnerary, antifeverish,
vermifugy
Flowers, roots
Vulnerary, hemostatic,
expectorant
Whole plant

Antiinflamatory,
emmenagoge, vulnerary

E.N. Quiroga et al. / Journal of Ethnopharmacology 74 (2001) 8996

93

Table 2
Radial growth inhibition of alcoholic extracts against filamentous fungia
Fungib

Alcoholic extractsc
1

++

++

++

+++

++

++

+++

++

++

++

++

++

++

++

+++

++

++

++

++

++

++

+++

10

+
+
+
+
a
The extract concentration (dry matter) in the culture medium was 0.8 mg ml1 in all cases. The inhibition was reported as ()
B10% growth inhibition, ( 9 ) between 10 and 20%, (+) between 20 and 40%, (++) between 40 and 80%, and (+++) 80%.
(n= 12.)
b
A, Lenzites elegans; B, Schizophyllum commune; C, Pycnoporus sanguineus; D, Ganoderma applanatum; E, Fusarium oxysporum;
F, Penicillium notatum; G, Aspergillus niger; H, Trichoderma spp.
c
1, Larrea di6aricata Cav.; 2, Larrea cuneifolia Cav.; 3, Schkuhria pinnata (Lam) O. Kuntzi; 4, Zinnia peru6iana (L), L.; 5,
Equisetum giganteum L.; 6, Zuccagnia punctata Cav.; 7, Acacia ca6en (Mol) Molina; 8, Phytolacca dioica L.; 9, Prosopanche
americana (R.Br) Baillon; 10, Schinus molle L.

gram-negative microorganisms (Amani et al.,

1998). Otherwise, alcoholic extracts of P. dioica
and Z. peru6iana did not show significant antifungal activity against the eight filamentous fungi
tested at the highest dose used.
L. elegans, P. sanguineus and F. oxysporum were
average sensitive in vitro to alcoholic extracts of
flowers and roots of Prosopanche americana. A
peptide designed Pa-AMP was isolated and
purified from seeds of P. americana. This peptide
showed inhibitory activity for pathogenic fungi
and Gram-positive and negative bacteria (Minami
et al., 1998).
It was found that the extract from Schinus
molle inhibits the growth of F. oxysporum, P.
notatum, A. niger and Trichoderma spp. Triterpe-

nes and sesquiterpenolactones isolated from

leaves and fruits of S. molle showed antifungal
activity when they were tested against Candida
albicans, Trichophyton mentagraphytes and A.
niger. Also Aspergillus alternata, Aspergillus
fla6us, Mycrosporum griseum, P. cyclopium and P.
italicum showed growth inhibition in vitro by
their leaf essential oils (Ross et al., 1980; Dishit et
al., 1986).
The responses of the two assayed yeasts (S.
carlsbergensis and Rhodotorula spp.) are shown in
Table 3. It was found that extracts of L. di6aricata, L. cuneifolia, Z. punctata and P. americana
reduced the growth of both yeasts. Fig. 3 shows
growth inhibition of S. carlsbergensis by various
amounts of L. di6aricata extract. Similar results

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E.N. Quiroga et al. / Journal of Ethnopharmacology 74 (2001) 8996

Table 3
Paper disk diffusion of plant alcoholic extracts on yeast
growtha
Plant alcoholic extracts Yeast strains

Fig. 1. Growth inhibition of Penicillium notatum by alcoholic

extract of Larrea di6aricata. C, Control; 2, 3 and 4 mg dry
matter/plate.

were obtained with the agar well diffusion assays

(not shown).
Table 4 shows the MICs observed for the effect
of different plant extracts on yeasts. L. cuneifolia
exhibited a better inhibition activity against S.
carlsbergensis than L. di6aricata and P. americana.

Fig. 2. Antifungal activity of Zuccagnia punctata extract

against the wood destroying fungi Ganoderma applanatum and
Lenzites elegans. C, Control; 2; 3 and 4 mg dry matter/plate.

L. di6aricata Cav.
L. cuneifolia Cav.
S. pinnata Lam O.
Kuntzi
Z. peru6iana (L), L.
E. giganteum L.
Z. punctata Cav.
A. ca6en (Mol.)
Molina
P. dioica L.
P. americana (R.Br)
Baillon
S. molle L.

S.
carlsbergensis

Rhodotorula spp.

++
++

+++
++

++

++

++

++

a
The growth inhibition of the two yeasts was determined by
paper disk diffusion assays, using 0.2 mg dry matter/disk. The
inhibition is reported as: () without inhibition, (+) dr =1.0
mm, (++) dr =1.01.5 mm, and (+++) dr =1.52.0 mm,
where dr is diameter of the inhibition zone. (n =12.)

Otherwise, L. di6aricata and L. cuneifolia showed

the highest inhibition of Rhodotorula spp. growth.
The MICs of L. cuneifolia against S. carlsbergensis and Rhodotorula spp. were 100 and 133 mg
ml 1, respectively, while the MIC of an accepted
antifungal compound isolated and purified from

Fig. 3. Disk diffusion assay. Effect of growing amounts of

Larrea di6aricata extract on Saccharomyces carlsbergensis
growth. Control and 25, 33, 50, 100 and 200 mg dry matter/
disk in the clockwise sense.

E.N. Quiroga et al. / Journal of Ethnopharmacology 74 (2001) 8996

Table 4
MICs of different plant extracts against yeastsa
Plant extracts

Yeasts
S. carlsbergensis
(mg ml1)

Larrea di6aricata Cav.

Larrea cuneifolia Cav.
Zuccagnia punctata
Cav.
Prosopanche
americana (R.Br)
Baillon

Rhodotorula
spp. (mg ml1)

200
100
400

100
133
200

200

266

MICs were determined by dilution tests as indicated in

Section 2. Data were taken from the inhibition produced by
plant extracts (20500 mg dry extract ml1 were used). (n= 8;
S.D. =0.010.09).

Anemarrhena asphodeloides against Saccaromyces

cere6isiae was 200 mg ml 1 (Iida et al., 1999).
Although studies on growth inhibition of fungi
by isolated plant compounds suggest a role in plant
defense, such in vitro tests may not always give an
accurate indication of the significance of these
compounds in restricting fungal growth in the
plant (Mansfield, 1983). As plants are sessile organisms, they are confined to the place where they
grow. They are capable of sensing the presence of
potential phytopatogens (fungi, bacteria and
viruses) and mounting defense mechanisms. Plants
can produce antifungal compounds to protect
themselves from biotic attack that could be essential for fungi infection resistance (Wojtaszek,
1997). The understanding of the inhibitory mechanism would provide better directions toward the
development of efficient production and application of technologies associated with biofungicide
plant materials.
This is the first report showing the antifungal
activities of different Argentine plants. Further
studies, including the isolation and structure function relationships of the antifungal natural products are now in progress.
Acknowledgements
The authors are grateful to the Catedra de
Micologa, Instituto de Microbiologa, Facultad de

95

Bioqumica, Qumica y Farmacia de la Universidad Nacional de Tucuman (UNT) and to the

Instituto Nacional de Tecnologa Agropecuaria
(INTA), Tucuman, Argentina for the generous gift
of fungus cultures. This work was supported by
grants from the Secretara de Ciencia y Tecnica
from the UNT, Tucuman, Argentina.

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