3C Tecnología. Glosas de innovación aplicadas a la pyme. ISSN: 2254 – 4143 Ed. 33 Vol. 9 N.º 1 Marzo - Junio

EFFICACY OF TALAROMYCES FLAVUS COATED WITH

NANOPARTICLES IN THE GROWTH INHIBITORY OF FUSARIUM

OXYSPORUM F.SP. CUCUMERINUM

Laleh Naraghi

Iranian Research Institute of Plant Protection, Agricultural Research,

Education and Extension Organization (AREEO), Tehran, (Iran).

E-mail: lale_naraghi@yahoo.com ORCID: https://orcid.org/0000-0001-5767-2498

Maryam Negahban

Iranian Research Institute of Plant Protection, Agricultural Research,

Education and Extension Organization (AREEO), Tehran, (Iran).

E-mail: mnegahban2009@gmail.com ORCID: https://orcid.org/0000-0002-6602-9936

Recepción:

08/01/2020

Aceptación:

19/02/2020

Publicación:

13/03/2020

Citación sugerida:

Naraghi, L., y Negahban, M. (2020). Ecacy of Talaromyces Flavus coated with nanoparticles in the growth inhibitory

of Fusarium Oxysporum F.SP. Cucumerinum. 3C Tecnología. Glosas de innovación aplicadas a la pyme, 9(1), 31-45. http://

doi.org/10.17993/3ctecno/2020.v9n1e33.31-45

3C Tecnología. Glosas de innovación aplicadas a la pyme. ISSN: 2254 – 4143 Ed. 33 Vol. 9 N.º 1 Marzo - Junio

http://doi.org/10.17993/3ctecno/2020.v9n1e33.31-45

ABSTRACT

In this study, nanobioformulations were prepared containing the fungus Talaromyces avus including two

types of nano-capsules (F1 and F3), one type of nanoemulsion (F2), and one type of powdered nano-

formulation (F4). Comparative in vitro studies were performed on nanoformulations and formulations

made based on rice bran from T. avus in terms of inhibitory eect on the colony growth the pathogenic

fungus Fusarium oxysporum f. sp. cucumerinum in a completely randomized design. These studies began three

months after the production of nanoformulations and continued at 3 months intervals for one year. The

results showed that the nanopowder was the most eective nanoformulation in increasing the inhibitory

eect on the growth of the examined pathogen.

KEYWORDS

Nanoformulation, Talaromyces avus, Biological control, Plant pathogens.

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1. INTRODUCTION

Studies conducted in Iran have demonstrated favorable results of the antagonist fungus, Talaromyces avus,

for the control of some important pathogenic pathogens such as Verticillium dahliae, Verticillium albo-atrum,

Fusarium oxysporum, and Rhizoctonia solani in some crop varieties including cotton, sugar beet, potatoes,

tomatoes, and greenhouse cucumbers (Naraghi et al., 2010a; Naraghi et al., 2010b; Naraghi et al., 2010c).

Also, the application of this fungus as solid fermentation in the eld on plant residues or their mixture

with peat soil reduced the incidence of disease and increased the yield of the above-mentioned crops.

Reduction of Verticillium wilt (50%), reduction in seedling death rate (37%), and 30% increase in yield

were found in cotton plant, and 40% decrease in disease percentage and 17% yield increase were

reported in potato plant (Naraghi et al., 2014b). A 93% increase in the number of healthy seedlings and

a 50% increase in yield were observed in sugar beet plants (Naraghi et al., 2014a). A 27% decrease in

disease severity and a 23% rise in yield were noticed in tomato (Niya et al., 2015). And a 30% reduction

of disease severity and a 7% yield increase were achieved in greenhouse cucumber (Naraghi et al.,

2017). Since marketing and attracting consumers are considered as important issuesin mass production

and commercialization of biological agents (Husen et al., 2006; Alimi et al., 2006; Kaewchai, Soytong,

& Hyde, 2009; Pereira et al., 2009), the commercialization of T. avusas a biological agent and the

importance of producing its various bioformulations, including nanoformulations, seem to be necessary

at present time.

In recent decades, nanotechnology has expanded dramatically in various elds of chemistry,

pharmacology, medicine, and agricultural chemical pesticides. The phenomenon of pest resistance to

pesticides is an issue that necessitates research and development in the eld of nano-pesticides. Therefore,

the introduction of nano-pesticides to researchers will ourish in research and development in this eld.

The environmental problems, costs of consuming large quantities of conventional pesticides, and the

problems caused by pest resistance to these pesticides raise the necessity of research and development in

the eld of nano-pesticides.

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The use of biodegradable polymers in the production of high-performance nanoemulsions and

nanocapsules made of natural and biodegradable materials can be an eective step in this regard. To

increase ecacy and reduce environmental hazards, encapsulation formulation seems to be the best

option (Maji et al., 2014). Therefore, the production of nano and micro bioformulation creates controlled

ability, increased strength and stability, and protection of active ingredients under adverse environmental

conditions such as light and moisture. The use of nanocapsulated formulation also helps remarkably in

cost reduction of pesticide consumption dose, economic benet, protection of the environment, and

reduction of its environmental risks, and better export of the crop (Martín et al., 2010).

Nanoparticles have a larger surface area than the microparticles, which increases their active surface

area and controlled release. Moreover, another advantage of nanometer particles is that they do not

stimulate the immune system of humans and animals, and rapidly exit the body (Guan et al., 2008).

The technology of nanocapsules containing nano-scale fungicide or pesticide molecules is a method of

pesticide formulation that facilitates and accelerates pest elimination (Guan et al., 2008). An emulsion is

a heterogeneous system consisting of two immiscible liquids, one of which is dispersed as droplets in the

other. Emulsions with a droplet size of about nanometers, typically in the range of 1-2 nm, are called

nanoemulsions (Ostertag, Weiss, & McClements, 2012). Compared with conventional emulsions, the

unique structure and properties of nano-emulsions have provided advantages for their application in

many industries. Industrial applications of nano-emulsion systems include their role in the elimination

of the coating and controlled release of benecial compounds such as essential oils, vitamins, and so

forth (Kah & Hofmann, 2014).

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2. METHODS

2.1. IN VITRO EXAMINATIONS

2.1.1. PRODUCTION OF NANOCAPSULES CONTAINING THE BIOLOGICAL FUNGUS

TALAROMYCES FLAVUS

The production of nanocapsules combines polymerization and lattice formation. It was performed

through modications matching the biological fungal growth conditions (changing the amount or type

of polymer, surfactants, and oils, fatty acids, stirrer speed, and temperature). In the polymerization

process, the organic phase consisted of vegetable oil with a mixture of the biological fungus, which was

added to the aqueous phase consisting of hydrophilic polymeric monomers, such as a mixture of either

formaldehyde or alginate polymers, starch, and chitosan. Then, such cross-linkers as calcium chloride,

surfactants and associated materials, and fatty acid oils were added to the two phases and homogenized

with a homogenizer (5000-10,000 rpm) at 35 °C. Finally, lattice polymer particles were encapsulated

around the particle’s biological fungus.

2.1.2. PRODUCTION OF NANOEMULSIONS CONTAINING THE BIOLOGICAL FUNGUS T. FLAVUS

A self-assemble model was used to prepare nanoemulsions containing the biological fungus T. avus.

Finally, a nanoemulsion was formulated containing hydrophobic nanoparticles of vegetable oil in a

biocompatible formulation. Components of this formulation were active ingredients of the biological

fungus and vegetable oils (e.g. hydrophobic castor oil), twin surfactant, viscose materials of carboxymethyl

cellulose, coconut moisturizer, fatty acid ethanol amide, and polyvinyl acetate stabilizer (e.g. alcohol

polyvinyl), linkers (e.g. calcium chloride), and biocompatible polymers (e.g. ethylene glycol, and starch).

First, a homogeneous solution of biocompatible polymers was prepared, followed by the addition of

such surfactants as a tween and the associated materials to the solution. A completely homogeneous

mixture of polymer and solvent was prepared using a homogenizer (2000-12000 rpm) at 25 °C. Then,

3C Tecnología. Glosas de innovación aplicadas a la pyme. ISSN: 2254 – 4143 Ed. 33 Vol. 9 N.º 1 Marzo - Junio

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the suspension containing the spores of biological fungus was added drop wise together with castor oil

and coconut fatty acids. Next, a cross-linker (calcium chloride) was added to both the two phases to form

nanoparticles around the biological fungal spores. Finally, the nanoparticles were coated around the

biological fungal spores.

2.1.3. PRODUCTION OF NANOPOWDERS CONTAINING THE BIOLOGICAL FUNGUS T. FLAVUS

The suspension containing biological fungal spores was dispersed in the aqueous phase including

maltodextrin, xanthan gum, methyl xanthan, fatty acid ethanolamide, and oleic acid. It was then fully

powdered in a homogenizer (2000-12000 rpm) at 25 °C.

2.1.4. COMPARISON OF GROWTH INHIBITORY EFFICIENCIES OF DIFFERENT

NANOFORMULATIONS CONTAINING T. FLAVUS AGAINST FUSARIUM WILT PATHOGEN

IN GREENHOUSE CUCUMBERS

The eciencies of dierent T. avus nanoformulations for growth inhibition of soil pathogen (F.

oxysporum f. Sp. cucumerinum: FOC) were evaluated in a completely randomized design three months after

production and continued at three-month intervals for one year. To investigate each nanoformulation,

a petri dish containing the PDA medium was subdivided into two halves using an assumed line. A

0.5 mm piece of the pathogen was placed by a cork borer in one half and the other half received

0.1 g of a nanoformulation. Each of the afore mentioned pathogens was examined separately in a

completely randomized design with ve treatments (four new and control nanoformulations) in three

replications. For the control petri dish, the pathogen fragment was placed in only half of the petri dish.

The colony diameter was measured in the treatment and control 7 days after placement of the pathogen

and formulation on the petri dish to determine the inhibition percentage for each studied pathogen by

the nanoformulation, which was calculated using the following formula:

Inhibition percentage =D

-D

× 100, where D

and D

are the growth diameters of pathogen colonies

in the treatment and the control, respectively.

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Data analysis and comparison of mean growth inhibition percentages of pathogen colonies by the

nanoformulation were performed by Duncan’s multiple range test using the MS TAT C software.

The pathogen, F. oxysporum f. sp. cucumerinum studied here was conrmed earlier in terms of pathogenicity,

which was obtained from the collection of the research laboratory for useful microorganisms in the

Iranian Institute of Botanical Research.

3. RESULTS

３.1. QUALITATIVE AND QUANTITATIVE INTRODUCTION OF COMPOUNDS USED IN

100 G OF PREPARED NANOFORMULATIONS

Four nanoformulations, namely two types of nanocapsules, one type of nanoemulsion, and one type

of nanopowderswere produced in this study (Figure 4), and the compounds used in 100 g of the

nanocapsulesare shown qualitatively and quantitatively in (Table 1).

Figure 1. The prepared nanoformulations (right toleft): Nanocapsules 1 (F1), Nanoemulsions (F2), Nanocapsules 2 (F3), and

Nanopowders (F4).

The biological fungus was prepared using T. avus suspension with a concentration of 10 spores/ml.

**Because the nano-formulations were prepared under non-sterile conditions, butanol was used to

prevent bacterial and fungal contamination in the evaluation of the nano-formulation ecacies in

growth inhibition of the fungal pathogen.

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Table 1. The types of prepared nanoformulations and the amounts of compounds used in 100 g of each nanoformulation type.

Types of nanoformulations prepared and the number of compounds used in 100 grams of each nanoformulation

Nanocapsules 1 (F1) Nanoemulsions (F2) Nanocapsules 2 (F3) Nanopowders (F4)

Compound

Amount

(g)

Compound

Amount

(g)

Compound

Amount

(g)

Compound

Amount

(g)

Biological

fungus *

Biological

fungus *

Biological

fungus *

Biological fungus

Alginate 8 Lauryl alcohol 5.17 Urea 9 Maltodextrin 5.14

Castor oil 16 Castor oil 9 Castor oil 5.4 Castor oil 5.33

Coconut fatty

acids

Coconut fatty

acids

5.17

Coconut fatty

acids

5.4

Fatty acid )

diethanolamide -

Oleic acid(

5.8

Sodium

chloride

Sodium

chloride 1.0

Sodium

chloride 1.0%

Xanthangam 5.8

Twin

surfactant

4 Twin surfactant 4

Polyethylene

glycol

Polyethylene

glycol

12 Formaldehyde 5.18 - -

Butanol** 3 Butanol 3 Butanol 3 Butanol 3

*For preparation of biologic fungi, suspension of Talaromyces avus with concentration of 10

spore per liter was used.

** Due to the preparation of nanoformulation in non-sterile conditions, butanol was used to prevent bacterial and fungal

contamination to evaluate the efcacy of nanoformulation in inhibiting the growth of the disease agent.

3.2. COMPARISON OF GROWTH INHIBITORY EFFICIENCIES OF DIFFERENT

NANOFORMULATIONS CONTAINING T. FLAVUS AGAINST FOC

In the rst and the second trimester after production, the eciency of nanoformulation in inhibition

of FOC colony growth (Figure 2) and (Figure 3) decreased from the rst to the second trimester in all

nanoformulations (Table 2). From the third trimester, the inhibition was only observed for nanopowders

on FOC colony growth (Figure 4 and Table 2). The ecacies of dierent nanoformulations in inhibition

of FOC colony growth were signicant in the rst, second, third, and fourth trimesters after production

at a 1% probability level.

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In the rst trimester of production, a comparison of average FOC colony growth inhibition of

each formulation revealed that the formulations were in two statistical groups, with nanocapsule 1,

nanoemulsions, and nanopowders being most eective in terms of inhibition level (Table 2). Comparison

of FOC inhibition averages from each formulation in the second trimester also indicated that the

formulations were in two statistical groups and nanopowder and nanocapsule 2 nanoformulations

presented the highest ecacy in growth inhibition of FOC colony (Table 2). The third and fourth-

trimester comparisons of FOC inhibition averages represented that the formulations were also in

two statistical groups and only an inhibition eect on FOC colon growth was observed only in the

nanopowders in these periods (Table 2).

Figure 2. Growth inhibition rate of Fusarium oxysporum f. sp. cucumerinum by different nanoformulations on PDA media in the

rst trimester after production. CONTROL, F1 (nanocapsule 1), F2 (nanoemulsion), F3 (nanocapsule 2), and F4 (nanopowder).

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Figure 3. Growth inhibition rate of Fusarium oxysporum f. sp. cucumerinu by different nanoformulations on PDA medium

in the second trimester after production. CONTROL,F1 (nanocapsule 1), F2 (nanoemulsion), F3 (nanocapsule 2), and F4

(nanopowder).

Figure 4. Growth inhibition of Fusarium oxysporum f. sp. cucumerinumcolony growth by the nanopowder (right) compared with

the control (left) in the fourth trimester after production.

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Table 2. Comparison of mean growth inhibition rates of Fusarium oxysporum f. sp. cucumerinum (FOC) in different

nanoformulation treatments.

Formulation

Mean FOC growth inhibition (%)

trimester

F1(Nanocapsule 1-polyalginate)

a25∙31 c00∙10 b0 b0

F2 (Nanoemulsion-polyethylene

glycol)

ab12∙26 bc44∙14 b0 b0

F3 (Nanocapsule 2-polyurea

formaldehyde)

b00∙20 ab61∙16 b0 b0

F4 (Nanopowder-maltodextrin,

xanthan gum)

a77∙27 a42∙21 a00∙24 a42∙20

Without nanoformulation

(control)

- - - -

*Means with similar letters are not signicantly different at 1% probability level.

**The inhibition rate of the pathogen colony growth in nanoformulation treatments was compared to the without nano-formulation

(control) and no inhibition was observed in the control.

4. DISCUSSION

Overall, the present results showed that the nanopowder had the uppermost eciency among the

prepared nanoformulations (two types of nanocapsules, nanoemulsions, and nanopowders) in terms of

Fusarium wilt growth inhibition. The results obtained from the eect of prepared nanoformulations on

the growth of some plant pathogens are in line with those of previous research (Khan & Jameel, 2016) on

the inhibitory eect of a nanoformulation containing Penicillium fellutanum on Candida albicans. The in vitro

study observed inhibition zones of the pathogenic fungal growth in petri dishes around nanoformulation

tablets.

Naratghi et al. (2012) reported that some mechanisms play a more eective role in dierent plant

pathogens than other mechanisms. For example, the above study found that mycoparasitism was the

most eective mechanism for Fusarium growth inhibition. On the other hand, the eective metabolites of

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the production mechanisms of non-volatile compounds and mycoparasitism were reported to be glucose

oxidase and chitinase, respectively (Kim, Fravel, & Papavizas, 1990; Inbar & Chet, 1995) and levels of

these metabolites and their activity to be variable depending on time and environmental conditions

(Zhai et al., 2016).Thus, the eects of dierent nano compounds cannot be ignored on the amount and

intensity of dierent T. avus metabolites. In the present study, the time and environmental conditions in

the second trimester were likely such that the intensity and activity of the Fusarium eective metabolite

(chitinase) were lower than those of other T. avus metabolites present in the nanoformulation.

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