CETvol87
DOI: 10.3303/CET2187087
Paper Received: 16 September 2020; Revised: 6 February 2021; Accepted: 10 May 2021
Please cite this article as: Julcapoma Polo K.J., Mendoza Campos H.L., Castaneda Olivera C., Jave Nakayo J.L., Valverde Flores J.W., 2021,
Biofungicide for the Control of Botrytis Cinerea and Fusarium Oxysporum: a Laboratory Study, Chemical Engineering Transactions, 87,
517- 522 DOI:10.3303/CET2187087
CHEMICAL ENGINEERING TRANSACTIONS
VOL. 87, 2021
A publication of
The Italian Association
of Chemical Engineering
Online at www.cetjournal.it
Guest Editors: Laura Piazza, Mauro Moresi, Francesco Donsì
Copyright © 2021, AIDIC Servizi S.r.l.
ISBN 978-88-95608-85-3; ISSN 2283-9216
Biofungicide for the Control of Botrytis Cinerea and Fusarium
Oxysporum: a Laboratory Study
Karla J. Julcapoma Polo, Heyssy L. Mendoza Campos, Carlos A. Castañeda
Olivera*, Jorge L. Jave Nakayo, Jhonny W. Valverde Flores
Universidad César Vallejo, Campus Los Olivos, Lima, Peru
caralcaso@gmail.com
The use of fungicides based on plant extracts for the inhibition of phytopathogens has become a sustainable
alternative for the environment. In this sense, research has developed biofungicides based on extracts of
Allium cepa (A. cepa), Allium sativum (A. sativum), Zingiber officinale (Z. officinale) and Domestic Residual Oil
(DRO) for the inhibition of Botrytis cinerea (B. cinerea) and Fusarium oxysporum (F. oxysporum). The
inhibition of the two phytopathogenic fungi was evaluated in vitro, measuring the growth of mycelium of the
fungi inoculated in the potato dextrose agar (PDA) culture medium, subjected to four treatments with three
different doses (10, 15 and 20 %). The treatment that totally inhibited the mycelial growth of B. cinerea and F.
oxysporum was the biofungicide composed by Z. officinale and domestic residual oil with a dose of 15 %.
Finally, it is concluded that the use of the biofungicide is favorable for the control of fungi and could be used as
an environmentally friendly alternative.
1. Introduction
Solanum lycopersicum (S. lycopersicum) (tomato) is one of the most cultivated and used vegetables for food
processing due to the main nutritional contributions it has (high content of vitamins and minerals) (Iglesias et
al., 2017). During the cultivation period of S. lycopersicum, favorable climatic and agronomic conditions arise
for the propagation of phytopathologies, among which are "gray rot" and "vascular withering" caused by the
fungi B. cinerea and F. oxysporum (Boiteux et al., 2019; Terrones, 2015). To date, many of these diseases are
attacked using chemical fungicides whose residues negatively alter the environment and human health
(Borucka and Celiński, 2019; Ferreira et al., 2018; Oliveira, 2018). In order to implement sustainable
agriculture, some researchers have evaluated the use of extracts from various plants in the control of
phytopathogenic pests. In S. lycopersicum L. crops, the extract of Junglannes spp. and Carya sp. inhibits the
fungus F. oxysporum allowing the adequate development of the plant (Jasso de Rodríguez et al., 2019). On
the other hand, the extracts of Trichilia heudelotii, Nesogordonia papaverifera, Celtis mildbraedii, Cola
gigantea and Triplochiton scleroxylon are effective in inhibiting F. oxysporum (Kamelé, 2019).
There are unconventional plants such as Sesamun indicum, whose extract is used to inhibit B. cinerea and F.
oxysporum by presenting fungal and/or fungistatic characteristics (Fernández and Laurentin, 2016), or the
ethanolic extract of Azadirachta indica (neem) which is used to inhibit B. cinerea (Gholamnezhad, 2019).
Among the fungi that afflict S. lycopersicum L. (tomato) crops are B. cinerea and F. oxysporum. B. cinerea is
an aggressive, versatile phytopathogenic fungus and is primarily responsible for the disease known as gray
mold or strawberry rot. B. cinerea reproduction occurs in senescent and/or dead tissues of ornamental plants,
fruits and vegetables and in high humidity environments (Abbey et al., 2019; Šernaitė et al., 2020). F.
oxysporum is a fungus with high antioxidant activity that lives in the soil and is the phytopathogen that causes
vascular withering and the phytopathogenic disease called Fusariosis (Ramírez et al., 2020).
Plant extracts have several secondary metabolites that make possible the mycelial inhibition of any fungus.
These metabolites vary by species, for example, A. cepa extracts have secondary metabolites such as
flavonols which are sulfur-rich compounds that prevent the proliferation of phytopathogenic microorganisms
(Miralha Franco et al., 2018). A. sativum extracts have various biologically active components. These
components usually contain sulfur compounds such as allicin, ajoene, allylmethyltrisulfide, diallyltrisulfide,
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diallyldisulfide, saponins, flavonoids, among other compounds that inhibit the growth of fungi and bacteria (De
Falco et al., 2018; Fufa, 2019; Liaqat et al., 2019). On the other hand, the extracts of Z. officinale are
composed mainly of oxygenated monoterpenes such as citral, ethyl ether verbenil, geranic acid, artemiseole,
among other compounds that allow the inhibition of various fungi and phytopathogenic bacteria (Hussein and
Joo, 2018).
Currently, the development of phytopathogenic pests is a constant problem in the agricultural industry. This
productive activity uses 85 % of the pesticides produced worldwide, and their excessive use causes severe
damage to the soil composition and the taxonomy of plants and fruits. These damages are caused by the
different chemical compounds present in the pesticides, which disperse rapidly in biotic (fauna and flora) and
abiotic (air, soil and water) environments, altering their balance and presenting themselves as a threat to
human health (del Puerto Rodríguez et al., 2014). Likewise, in the report "Soil contamination: a hidden reality",
it is expressed that the global consumption of fertilizers reached 200 million tons in 2018; being Chile and the
United States the consumer countries of 50% of the total (Rodríguez Eugenio et al., 2019).
The elaboration of biofungicides is a promising alternative to conventional fungicides. Therefore, the objective
of this research was to evaluate the fungicidal activity of four biofungicides obtained from A. cepa, A. sativum,
Z. officinale and domestic residual oil on B. cinerea and F. oxysporum.
2. Methodology
2.1 Identification and isolation of fungi
The fungi (B. cinerea and F. oxysporum) were isolated from leaves, fruits and stems of S. lycopersicum crops
in the Kantu nursery, located in Lurin, Lima, Peru. Petri dishes with Potato Dextrose Agar were used for
identification and isolation.
2.2 Obtaining the biofungicide
Obtaining the biofungicide followed the manual "Antiamoebic and phytochemical screening of some
Congolese medicinal plants" (Tona et al., 1998). For this, 3 Kg of each plant (A. cepa, A. sativum and Z.
officinale) were disinfected with sodium hypochlorite and abundant distilled water, then dried and cut into small
pieces and then liquefied separately. Each liquefied paste was deposited in glass containers adding 800 mL of
90 % ethanol, and then stored at 5 ºC. After 48 hours of refrigeration, the macerated products were filtered,
stored in bottles and kept in an environment away from sunlight and at 20°C until they were used in the
experimental tests (Figueroa Gualteros et al., 2019).
2.3 Characterization of the fungi
For the process of characterization of the fungi, B. cinerea and F. oxysporum cultures were submitted to a
microscope, model Olimpus, with 400 X and 100 X magnification, and later images of the structures of each
one of the phytopathogens were captured.
2.4 In vitro antifungal activity test
For the test of the antifungal activity the potato dextrose agar (PDA) culture medium was mixed with the
biofungicides inside an Erlenmeyer of 250 mL. The different extracts were diluted in the culture medium in
three different doses (Table 1).
Table 1: Dosage of treatments´
N° Treatments Dose (%)
1 Biofungicide 1 (BIO1) 10 15 20
2 Biofungicide 2 (BIO2) 10 15 20
3 Biofungicide 3 (BIO3) 10 15 20
4 Biofungicide 4 (BIO4) 10 15 20
BIO1: A. cepa + DRO
BIO2: A. sativum + DRO
BIO3: Z. officinale + DRO
BIO4: A. cepa + A. sativum + Z. officinale + DRO
Subsequently, the diluted medium was distributed in Petri dishes according to the doses of the different
treatments shown in Table 1, and incubated at a temperature of 25°C. After three days of incubation, the
diameter of the mycelial growth (mm) of each fungus was measured using a digital vernier. Measurement was
performed at three-day intervals during the twelve-day incubation, and all measurements obtained were
518
inserted into a data collection format for further processing to determine the percentage of mycelial growth
inhibition (Iglesias et al., 2017). The percentage mycelial growth inhibition was calculated according to
equation 1 (Luksiene et al., 2020).
From the equation, %ICM is the percentage of Mycelial Growth Inhibition, CTT the mycelial growth in the
control treatment and CTE the mycelial growth in the evaluated treatment.
3. Result and discussion
3.1 Characterization of B. cinerea and F. oxysporum
Figure 1 show the microscopic structure of the fungi B. cinerea and F. oxysporum, respectively.
Figure 1: Imagen microscópica: a) B. cinerea y b) F. oxysporum
Macroscopically, B. cinerea develops cottony colonies of variable pigmentation, from greyish white to greyish
brown. In Figure 1-a, it was observed microscopically that the mycelium is constituted by partitioned,
cylindrical hyphae (Latorre, 2004). On the other hand, F. oxysporum develops cottony colonies with white and
violet pigmentation. In Figure 1-b, it was observed microscopically that the mycelium is constituted by
Microconidia that have hyalines in ellipsoidal to cylindrical form that can be straight or curved (Latorre, 2004).
3.2 Mycelial inhibition of B. cinerea
The percentages of B. cinerea inhibition are shown in Table 2. The biofungicide based on Z. officinale extract
and DRO, achieved the total inhibition of the B. cinerea fungus at concentrations of 15 and 20 %. On the
contrary, the less effective biofungicide was the one elaborated with A. sativum extract and DRO. The total
inhibition carried out by the biofungicide based on Z. officinale and DRO was favorable due to the bioactive
compounds of the extract such as gingerol, oxygenated monoterpenes, citral, etc (De Falco et al., 2018).
Table 2: Inhibition of mycelial growth of B. cinerea from the beginning of treatment (day 3) to the end of
treatment (day 12)
D3, D6, D9 y D12: day 3, day 6, day 9 y day 12, respectively
𝐼𝐼𝐼𝐼𝐼𝐼 =
𝐼𝐼𝐶𝐶𝐶𝐶 − 𝐼𝐼𝐶𝐶𝐶𝐶
𝐼𝐼𝐶𝐶𝐶𝐶
× 100%
(1)
Treatments
Mycelial inhibition (%)
10% dose 15% dose 20% dose
D3 D6 D9 D12 D3 D6 D9 D12 D3 D6 D9 D12
BIO1 98.57 72.68 47.66 46.28 99.59 93.39 86.86 82.82 100 100 100 100
BIO2 92.78 59.47 45.45 38.57 98.83 80.86 73.08 57.03 100 96.84 90.74 87.90
BIO3 100 81.87 64.89 57.72 100 100 100 100 100 100 100 100
BIO4 93.84 77.94 60.07 48.34 100 100 80.25 71.09 100 100 100 100
519
From Table 2, with the 10% dose, the treatment that achieved the highest percentage of inhibition (57.72 %)
of B. cinerea in the last day of incubation was the BIO3 (Z. officinale extract and DRO) since it presents
secondary compounds that prevent the spread of B. cinerea fungus (Ferreira et al., 2018). On the other hand,
with the 15% dose, the biofungicide that totally (100 %) inhibited the fungus was also the BIO3. This inhibition
was carried out from the third day of incubation until the last day of experimentation as a result of citral,
verbenyl ethyl ether, geranic acid, among other compounds belonging to the species of Z. officinale that totally
inactivate the growth of phytopathogens (Hussein and Joo, 2018). In other works, the crude extract of Z.
officinale managed to inhibit B. cinerea by 17.5% at a dose of 0.5% (Hussein and Joo, 2018). The difference
in the percentages of inhibition could be associated to the incubation temperature of the plates submitted
during the experimental development, since the extract of Z. officinale presents synergistic properties (Sacchi
Sneha, 2016) that allow them to inhibit the mycelial growth of B. cinerea at low temperatures of 21 to 25°C
(Ramírez et al., 2020).
In treatments with 20% dose, the biofungicide that did not achieve total inhibition of B. cinerea was the BIO2
(A. sativum extract and DRO) because the bioactive compounds of the species do not effectively intervene in
the mycelial inhibition of B. cinerea (Chen et al., 2018). On the other hand, the three remaining biofungicides
achieved a total inhibition of the fungus in mention from the first day of incubation. Other researchers used
Thymus extract at a dose of 30%, and obtained B. cinerea mycelial inhibition results of less than 63%
(Šernaitė et al., 2020). (Hapon et al., 2017; Rodríguez-Rodríguez et al., 2017) succeeded in inhibiting B.
cinerea fungus by 65% and 84.3%, respectively, with extracts of Citrus limonia and Larrea divaricata.
3.3 Mycelial inhibition of F. oxysporum
The percentages of F. oxysporum inhibition are shown in Table 3. The biofungicide based on Z. officinale
extract and DRO, and the biofungicide composed of the three extracts and the DRO achieved total inhibition
of the fungus with doses of 15 and 20%. On the contrary, the remaining biofungicides (A. strain + DRO and A.
sativum + DRO) achieved the total inhibition of F. oxysporum only with the dose of 20%.
Table 3: Inhibition of mycelial growth of F. oxysporum from the beginning of treatment (day 3) to the end of
treatment (day 12)
Treatments
Mycelial inhibition (%)
Dose 10% Dose 15% Dose 20%
D3 D6 D9 D12 D3 D6 D9 D12 D3 D6 D9 D12
BIO1 88.20 71.04 61.80 53.54 100 91.51 89.52 87.96 100 100 100 100
BIO2 96.49 85.66 75.30 71.83 100 93.07 91.10 88.06 100 100 100 100
BIO3 87.43 76.04 67.65 64.89 100 100 100 100 100 100 100 100
BIO4 100 93.41 90.28 85.61 100 100 100 100 100 100 100 100
D3, D6, D9 y D12: day 3, day 6, day 9 y day 12, respectively
In Table 3, the biofungicide that achieved the highest mycelial inhibition (85.61%) of F. oxysporum, at 10%
doses, was BIO4 (A. cepa + A. sativum + Z. officinale + DRO) because it has organosulfurized components
such as alkaloids, phenolic acids, flavonoids and gingerol that inhibit mycelial growth of the fungus (Miralha
Franco et al., 2018). In other investigations, the authors were able to inhibit F. oxysporum by 58% from the
seventh day of treatment with a 30% dose of Syzygium aromaticum oil (Faggiani et al., 2015).
Regarding the treatments BIO3 (Z. officinale + DRO) and BIO4 (A. cepa + A. sativum + Z. officinale + DRO),
with doses of 15%, these biofungicides were effective in totally inhibiting the mycelial growth of F. oxysporum
from the third day of incubation due to the action of its bioactive components such as citral, verbenyl ethyl
ether, geranic acids and artemisiole (Gholamnezhad, 2019). In other works, Juglans mollis (4000 mg L-1),
Juglans microcarpa (5000 mg L-1) and Carya ovata (5000 mg L-1) ethanolic extracts showed the highest
antifungal effect against F. oxysporum (Jasso de Rodríguez et al., 2019). Already, for the treatments with
doses of 20%, the total inhibition of F. oxysporum was observed from the third day of treatment. In other
studies, panthropical plants such as Oxalis barrelieri L., Stachytarpheta cayennensis L. and Euphorbia hirta L.
inhibited mycelial growth of F. oxysporum by 80 and 100%, with application doses of 1.25 to 20 mg L-1
(Mekam et al., 2019).
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The mycelial inhibition of B. cinerea and F. oxysporum was possible based on vegetable extracts and
domestic residual oil, being an eco-friendly alternative to counteract phytopathogenic pests (Arici et al., 2019).
The biologically active compounds of the plant extracts could provide new alternatives for the development of
natural acaricides and fungicides that could be included as a set of strategies for an integrated pest
management program in order to produce the least damage to the environment (Jasso de Rodríguez et al.,
2019; Valdés-pérez et al., 2016).
4. Conclusions
The efficacy of biofungicides based on plant extracts (A. cepa, A. sativum and Z. officinale) and domestic
residual oil for mycelial inhibition of B. cinerea and F. oxysporum was favorable, obtaining values of 85.08%
and 91.88%, respectively. It was observed that the inhibition of B. cinerea and F. oxysporum fungi started from
the third day of exposure, and the best results were found at the 15% dose of BIO3 and 20% of the other
biofungicides, with inhibition values higher than 87.90%.
Acknowledgments
The authors are grateful to UCV (Universidad César Vallejo) for providing us with their laboratories for
experimental development.
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