Sodium silicate and chitosan: an alternative for the in vitro control of Colletotrichum gloeosporioides isolated from papaya (Carica papaya L.)

Rayón-Díaz, E.; Birke-Biewendt, A. B.; Velázquez-Estrada, R. M.; González-Estrada, R. R.; Ramírez-Vázquez, M.; Rosas-Saito, G. H.; Gutiérrez-Martínez, P.; Rayón-Díaz, E.; Birke-Biewendt, A. B.; Velázquez-Estrada, R. M.; González-Estrada, R. R.; Ramírez-Vázquez, M.; Rosas-Saito, G. H.; Gutiérrez-Martínez, P.

doi:10.15741/revbio.08.e1059

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Revista bio ciencias

versão On-line ISSN 2007-3380

Revista bio ciencias vol.8 Tepic 2021 Epub 04-Out-2021

https://doi.org/10.15741/revbio.08.e1059

Original articles

Sodium silicate and chitosan: an alternative for the in vitro control of Colletotrichum gloeosporioides isolated from papaya (Carica papaya L.)

E. Rayón-Díaz¹

A. B. Birke-Biewendt²

R. M. Velázquez-Estrada¹

R. R. González-Estrada¹

M. Ramírez-Vázquez³

G. H. Rosas-Saito³

P. Gutiérrez-Martínez¹^*

^¹ Tecnológico Nacional de México/I.T. Tepic. Av. Tecnológico No. 2595, Lagos del Country, 63175 Tepic, Nayarit, México.

^² Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico BioMimic®, Instituto de Ecología, A.C. Carretera Antigua a Coatepec, No. 351, El Haya, 91073 Xalapa, Veracruz, México.

^³ Red de Estudios Moleculares Avanzados, Unidad de Microscopía Clúster Científico y Tecnológico BioMimic®, Instituto de Ecología, A.C. Carretera Antigua a Coatepec, No. 351, El Haya, 91073 Xalapa, Veracruz, México.

Abstract

Colletotrichum gloeosporioides is one of the main fungi that attacks tropical and subtropical fruits. In this study, sodium silicate and chitosan were applied individually and in conjunction at different concentrations to evaluate their efficacy in vitro on mycelial growth and conidia sporulation. Besides, morphological changes on treated fungi were determined through scanning electron microscopy (SEM). Sodium silicate alone did not reduce C. gloeosporioides development, only a 9 % inhibition was recorded. In contrast, chitosan treatments ranging from 0.1 to 1.5 % showed the highest effectiveness and decreased fungal development the most (97-99 %). However, the combined treatments showed an additive effect, by inhibiting the mycelial development between 51-99 %. SEM micrographs showed morphological alterations in mycelium development, changes in size, and the presence of deformations. Therefore, these treatments could be used as an eco-friendly alternative in the control of C. gloeosporioides in fruits.

Keywords: Alternative System; Biopolymer; GRAS compounds; Pathogen

Resumen

Colletotrichum gloeosporioides es uno de los principales hongos que ataca a frutos tropicales y subtropicales. En este estudio, se aplicaron tratamientos de silicato de sodio y quitosano individualmente y en conjunto a diferentes concentraciones para evaluar su eficacia in vitro sobre el desarrollo micelial y esporulación de conidios. Además, los cambios morfológicos en los hongos tratados se determinaron mediante microscopía electrónica de barrido (SEM). El silicato de sodio solo no redujo el desarrollo de C. gloeosporioides, registrando una inhibición del 9 %. Por el contrario, los tratamientos de quitosano que van del 0.1 a 1.5 % mostraron la mayor eficacia y la mayor disminución del desarrollo del hongo (97-99 %). Sin embargo, los tratamientos combinados mostraron un efecto aditivo, al inhibir el desarrollo micelial entre un 51-99 %. Las micrografías SEM mostraron alteraciones morfológicas en el micelio, como cambios de tamaño y presencia de deformaciones. Por tanto, estos tratamientos podrían utilizarse como alternativa ecológica en el control de C. gloeosporioides en frutos.

Palabras clave: Sistemas alternativos; Biopolímero; Compuestos GRAS; Patógeno

Introduction

Colletotrichum gloeosporioides (Penz & Sacc.) is considered an important pathogen that affects various tropical and subtropical fruits (^{Gutiérrez-Martínez et al., 2017}), some of the most affected fruits are: soursop (Annona muricata L.) (^{Ramos-Guerrero et al., 2018}), mango (Mangífera indica L.) (^{Gutiérrez-Martínez et al., 2017}), papaya (Carica papaya L.) (^{Molina-Chaves et al., 2017}) and avocado (Persea americana Mill.) (^{Rodríguez-López et al., 2009}). The lack of protocols at post-harvest handling can favor infections by this fungus, leading to post-harvest fruit losses ranging from 10 to 50 % of total production (^{Torres-Calzada et al., 2013}). Conventionally, the use of fungicides that Benomyl, is the main strategy to reduce fungal infections by C. gloeosporioides, however resistance to the effect of these compounds has been reported (^{Ali & Mahmud, 2008}). On the other hand, consumers are aware of the residuality of these chemical compounds in the environment and their negative impact on human health (^{Abd-Elsalam et al., 2019}). Due to the above-mentioned reasons, it is necessary to search for eco-friendly, safe, and effective alternative treatments. Thus, chitosan is a non-toxic, harmless, polycationic biopolymer with edible coating functionality, has been tested for the control of various fungi such as C. gloeosporioides and Rhizopus stolonifer (soursop) (^{Ramos-Guerrero et al., 2018}), Colletotrichum sp. (mango) (^{Gutiérrez-Martínez et al., 2017}), Botryosphaeria sp. (pear) (^{Wang et al., 2017}) and Penicilium digitatum Pers. y Penicillium italicum Pers. (citrus) (^{Al-Sheikh & Yehia, 2016}) isolated from various tropical and subtropical fruits. The nanocomposite silica-chitosan has been also evaluated against gray mold (Botrytis cinerea) in table grapes (^{Youssef et al., 2019}). Sodium silicate is considered a GRAS compound (^{Palou, 2018}), the efficacy of this salt has been reported against Alternaria alternata (melon) (^{Bi et al., 2006}), Monilinia fructicola (peach) (^{Pavanello et al., 2016}), G. citri-aurantii (citrus) (^{Li et al., 2019}), Musicillium theobromae (banana) (^{Youssef et al., 2020}) with good results. This research aimed to evaluate the effectiveness of chitosan and sodium silicate alone and in conjunction at different concentrations on C. gloeosporioides mycelial growth and sporulation. We also determined through scanning electron microscopy (SEM) the effect on the fungus hypha.

Material and Methods

Raw materials

Chitosan was purchased from America Natural Ingredients® (Food grade, DAC 90 %, Viscosity 50-200 mpa s^-1) and sodium silicate was purchased from SigmaAldrich® (St. Louis, MO, USA). Potato dextrose agar (Sigma-Aldrich®, USA) was used for the incorporation of the chitosan and sodium silicate in the in vitro assay.

Isolation of C. gloeosporioides

The fungus used in this work was obtained from a strain identified in previous works, it was reactivated by inoculating fruits and later its macro and microscopic identification was carried out with the help of dichotomous keys.

Preparation of sodium silicate and chitosan solutions

Chitosan solutions were prepared by adding 0.1 %, 0.5 %, 1 %, and 1.5 % (w / v) of chitosan in 100 mL of 2 % (v / v) glacial acetic acid. The solution was in constant agitation for 3 to 5 hours at room temperature and pH was adjusted to 5.6 by adding NaOH solution (1N) (^{González-Estrada et al., 2020}). Sodium silicate solutions were prepared using the protocol proposed by ^{Ge et al. (2017)} with some modifications, the solutions were prepared by adding 0.5 %, 1 %, 1.5 %, and 2 % of sodium silicate in 100 mL of distilled water (v / v). The technique proposed by ^{Guo et al. (2019)} was used for the preparation of the combined treatments with some modifications, in previously prepared chitosan solutions (100 mL) at concentrations of 0.1 %, 0.5 %, 1 %, and 1.5 %, sodium silicate was added at different concentrations (0.5 %, 1 %, 1.5 %, and 2 %), the combined treatments were stabilized (pH of 5.6) with a NaOH solution (1N). The positive control consisted of a solution of 2 % acetic acid (pH 5.6) and a negative control consisted in PDA culture medium without treatments.

In vitro assays

Inhibition of mycelial growth

The radial measurement of the mycelial growth of the fungus was carried out following the protocol proposed by ^{Gutiérrez-Martínez et al. (2017)} with some modifications. Petri dishes that contained the treated chitosan (CHI), sodium silicate (Na₂SiO₃), and the combined CHI-Na₂SiO₃ PDA treatments were inoculated by placing PDA disks (3 mm of diameter) with the mycelium of the fungus (n=3, in duplicate). The mycelial growth development was recorded using a digital Vernier (Truper®). The results were expressed in percentage of inhibition.

Effects on sporulation

For sporulation, it was followed the protocol proposed by ^{Cortés-Rivera et al. (2019)}, was added sterile distilled water (10 ml) in the Petri dishes of the mycelial growth test containing the fungus, then the fungal colony was rubbed using a sterile glass bar, the obtained solution was filtered with sterile gauze and transferred into tubes of 10 mL. Finally, a Neubauer chamber (Hausser Scientific®) was used to determine the number of spores/mL.

Evaluation of the interaction of Chitosan and Sodium silicate mixtures

The interaction of the combination of treatments was carried out according to the Abbott method, with the protocol proposed ^{De Oliveira et al. (2017)}, considering factors such as concentration, the effect individual application of treatments and their combination, and the type of interaction. The following formula was used:

MGI%exp = Treatment1%obs+Treatment2%obs - (Treatment1%obs*Treatment2%obs/100)

Scanning electron microscopy (SEM)

The most effective treatments were selected to visualize their effect on the development of C. gloeosporioides by using scanning electron microscopy (SEM). We followed the method outlined in ^{Ramos-Guerrero et al. (2018)} with some modifications, samples of mycelial disks (3 mm) were cut from each treatment and placed in glass vials containing 3 mL of Karnovsky solution (pH 7.4) for 24 h at 4 °C, samples were agitated seven times manually during the first 7 hours and finally the samples left under refrigeration until complete the 24 h.

Statistical analysis

For the individual application of treatments, a completely randomized block design was applied. The generalized linear model was applied to know the growth kinetics of the pathogen during the incubation days of the combined treatments. Each experiment was repeated twice. The data obtained were analyzed by the ANOVA (Analysis of variance) and a Tukey test (p ≤ 0.05) was applied for the comparison of means using the software Statistica 10^®.

Results and Discussion

Mycelial inhibition assay

The application of chitosan treatments showed a percentage of inhibition ranging from 97 to 99 % of C. gloeosporioides mycelial growth (Figure 1). According to the statistical analysis, significant differences (p ≤ 0.05) were obtained compared to the sodium silicate, control, and negative control treatments (Table 1). The efficacy of chitosan is due to the interaction of free amino groups with structures of the pathogen and not by the presence of acetic acid, the stabilization of chitosan at pH (5.6) avoids the antifungal activity of acetic acid present in the chitosan solution, as previously reported (^{Hassan et al., 2012}; ^{Kang et al., 2003}; ^{Narendranath et al., 2001}). In this sense, with the application of acetic acid, only 11 % of mycelial growth inhibition was obtained. One of the main physicochemical properties of chitosan is its cationic property by generating electrostatic attractions, inducing changes in the permeability of the plasma membrane with the subsequent destabilization in vital functions of the pathogen, as previously reported (^{Gutiérrez-Martínez et al., 2018}; ^{Rahman et al., 2014}; ^{Ramos-Guerrero et al., 2018}). Sodium silicate treatments showed unfavorable effects in controlling the development of the fungus (Figure 1). We only achieved a 9 % mycelial inhibition (Table 1). These results are not following those reported by ^{Ge et al. (2017)} and ^{Bi et al. (2006)}. Both authors reported fungicidal effectiveness by the sodium silicate application (100 mM) treatments against fungi T. roseum and A. alternata, respectively. However, morphological changes in hypha development were noticed by SEM micrography (Figure 3D), Sodium silicate seems to cause hypha dehydration as part of its fungistatic mechanism, which is based on the pH modification in the medium (making it more alkaline) causing alterations in the plasma membrane and disorganized organelles, as previously reported (^{Niu et al., 2016}).

Figure 1 Effect of sodium silicate and chitosan at different concentrations on the mycelial growth of C. gloeosporioides at 10 days of incubation (27 ± 2 °C).

Table 1 Effect of the application of sodium silicate and chitosan on the mycelial growth inhibition and sporulation of C. gloeosporioides incubated during 10 days at 27 ± 2 °C.

Treatments	Mycelial growth (% of inhibition)	Sporulation (spores*10⁶/mL)
Negative control	0 ± 0 ^a	3.5 ± 2.86 ^e
Control	11.39 ± 10.67 ^a	0.4 ± 0.83 ^abc
Chitosan 0.1 %	99.3 ± 0.06 ^b	0 ^a
Chitosan 0.5 %	99.3 ± 0.15 ^b	0 ^a
Chitosan 1 %	99.3 ± 0.17 ^b	0 ^a
Chitosan 1.5 %	99.3 ± 2.02 ^b	0 ^a
Sodium silicate 0.5 %	9.87 ± 7.83 ^a	2.6 ± 0.44 ^abc
Sodium silicate 1 %	9.42 ± 4.36 ^a	0.6 ± 2.00 ^c
Sodium silicate 1.5 %	7.65 ± 0.55 ^a	0.9 ± 2.30 ^d
Sodium silicate 2 %	4.07 ± 0.66 ^a	2.7 ± 2.86 ^de

Data in the same column followed by different lower‐case letters are significantly different (p ≤ 0.05) according to Tukey test. Values are expressed as means ± standard deviation (n=3).

Figure 2 Effect of the combination of sodium silicate and chitosan on the mycelial development of C. gloeosporioides during 10 days of incubation (27 ± 2 °C).

Figure 3 Micrographs of C. gloeosporioides in contact with different treatments at x1000 magnifications, bar = 200 µm. A) Negative control, B) Control (Acetid acid 2 %), C) Chitosan 1 %, D) Sodium silicate 0.5 %, E) Chitosan 0.5 % + Sodium silicate 1.5 %, F) Chitosan 1 % + Sodium silicate 0.5 %.

The combination of both treatments and concentration showed a significant effect (p ≤ 0.05) on the mycelial development of the fungus compared with control and the negative control (Table 2). According to the Abott index (Table 3), the combinations of these treatments show an additive effect at all concentrations tested, these results are in agreement with the investigation of ^{Guo et al. (2019)}, in their study an additive effect was obtained by the combination of chitosan and sodium silicate improving the effectiveness of both treatments by reducing the incidence of A. alternata up 50 % compared to control treatment.

Table 2 Effect of the combination treatments of sodium silicate and chitosan on the mycelial growth inhibition and sporulation of C. gloeosporioides incubated during 10 days at 27 ± 2 °C.

Treatments	Mycelial growth (% of inhibition)	Sporulation (spores*10⁶/mL)
Negative control	0 ± 0 ^a	3.5 ± 2.86 ^e
Control (acetic acid 2%)	11.39 ± 10.67 ^ab	0.4 ±0.83 ^abc
Chitosan 0.1%+ Sodium silicate 0.5%	75.35 ± 33.28 ^bc	2.6 ± 1.67 ^d
Chitosan 0.1% + Sodium silicate 1%	75.65 ± 32.53 ^bc	0.6 ± 1.94 ^abc
Chitosan 0.1% + Sodium silicate 1.5%	64.46 ± 43.41 ^abc	0.9 ± 2.30 ^bc
Chitosan 0.1%+Sodium silicate 2%	70.51 ± 27.26 ^bc	2.7 ± 1.87 ^d
Chitosan 0.5%+Sodium silicate 0.5%	96.26 ± 4.56 ^c	0.8 ± 1.51 ^bc
Chitosan 0.5%+Sodium silicate 1%	95.93 ± 5.28 ^c	0 ^a
Chitosan 0.5% + Sodium silicate 1.5%	99.51 ± 0.34 ^c	0.1 ± 0.89 ^ab
Chitosan 0.5% + Sodium silicate 2%	99.55 ± 0.11 ^c	0 ^a
Chitosan 1% + Sodium silicate 0.5%	99.47 ± 0.20 ^c	0 ^a
Chitosan 1% + Sodium silicate 1%	95.31 ± 4.13 ^c	0 ^a
Chitosan 1% + Sodium silicate 1.5%	99.63 ± 0.36 ^c	0 ^a
Chitosan 1% + Sodium silicate 2%	96.38 ± 4.47 ^ab	0 ^a
Chitosan 1.5% + Sodium silicate 0.5%	50.97 ± 17.32 ^abc	0 ^a
Chitosan 1.5% + Sodium silicate 1%	60.07 ± 8.70 ^bc	0 ^a
Chitosan 1.5% + Sodium silicate 1.5%	74.55 ± 6.05 ^c	0 a
Chitosan 1.5% + Sodium silicate 2%	99.59 ± 0.23 ^c	0 ^a

Data in the same column followed by different lower‐case letters are significantly different (p ≤ 0.05) according to Tukey test. Values are expressed as means ± standard deviation (n=3).

Table 3 Determination of the effectiveness of combination treatments of sodium silicate and chitosan on the mycelial growth inhibition of C. gloeosporioides incubated during 10 days at 27 ± 2°C using Abbott´s method.

Mixtures	Individual application of treatments		Combination of treatments		Abbott method
Mixtures	MGI % Chitosan	MGI % Sodium silicate	MGI % observed	MGI % expected	AI	Effect
Chitosan 0.1% + Sodium Silicate 0.5%	99.3	9.87	75.35	99.37	0.76	Additive
Chitosan 0.1% + Sodium Silicate 1%	99.3	9.42	75.65	99.37	0.76	Additive
Chitosan 0.1% + Sodium Silicate 1.5%	99.3	7.65	64.46	99.35	0.65	Additive
Chitosan 0.1% + Sodium Silicate 2%	99.3	4.07	70.51	99.33	0.71	Additive
Chitosan 0.5% + Sodium Silicate 0.5%	99.18	9.87	96.26	99.26	0.97	Additive
Chitosan 0.5% + Sodium Silicate 1%	99.18	9.42	95.93	99.25	0.97	Additive
Chitosan 0.5% + Sodium Silicate 1.5%	99.18	7.65	99.51	99.24	1.00	Additive
Chitosan 0.5% + Sodium Silicate 2%	99.18	4.07	99.55	99.21	1.00	Additive
Chitosan 1% + Sodium Silicate 0.5%	99.26	9.87	99.47	99.33	1.00	Additive
Chitosan 1% + Sodium Silicate 1%	99.26	9.42	95.31	99.33	0.96	Additive
Chitosan 1% + Sodium Silicate 1.5 %	99.26	7.65	99.63	99.32	1.00	Additive
Chitosan 1% + Sodium Silicate 2 %	99.26	4.07	96.38	99.29	0.97	Additive
Chitosan 1.5% + Sodium Silicate 0.5 %	97.82	9.87	50.97	98.04	0.52	Additive
Chitosan 1.5% + Sodium Silicate 1 %	97.82	9.42	60.07	98.03	0.61	Additive
Chitosan 1.5% + Sodium Silicate 1.5%	97.82	7.65	74.55	97.99	0.76	Additive

MGI % = Mycelial growth inhibition (%), Abbott Index (AI) ≥ 1.5 (synergistic), (AI) in range ≥ 0.5 to 1.5 (Additive) and (AI) ≤ 0.5 (antagonist).

Sporulation inhibition assay

In the sporulation test, in the individual application of treatments chitosan showed the best performance with a total inhibition on the spore formation (Table 1). Conversely, sodium silicate treatments reduced the number of spores from 9 to 80 % depending on the concentration tested. For combined treatments, even when the Abbott test showed an additive effect, the concentration of chitosan seems to play a key role in the efficacy of treatments (Table 2). The combination of chitosan at 0.1 % and sodium silicate reduced the sporulation from 22 to 81 %. Better results were obtained with the concentrations of chitosan at 0.5 % by reducing the sporulation from 76 to 100 %. Total inhibition of the sporulation process was obtained using chitosan at 1 and 1.5 %. These results indicate that the fungicidal effect of chitosan not only affects mycelial development but is also capable of inducing changes at the molecular level, causing mainly structural and morphological affectations in the fungal cell as evidenced by SEM (Figure 3F) and previously reported (^{Sun et al., 2008}; ^{Song et al., 2016}). These results are important due to a positive inhibition in this process can reduce the dispersion of the fungus and avoid infections on susceptible hosts to this fungus.

Scanning electron microscopy

The micrographs of the pathogen are shown in Figure 3. In the negative control (Figure 3A) mycelium with healthy aspect and without affectations was observed. In control treatment (2 % acetic acid), swelling and deformation of the hyphae are observed (Figure 3B), which implies affectations at the structural level and also in a reduction in the respiration process of the fungus, as reported (^{Kang et al., 2003}). Chitosan treatments (Figure 3C) showed compacted and reduced (size) mycelium, this effect can be due to the interaction of the biopolymer with the cell wall as well the membrane causing hyphae contraction, as previously reported (^{Ramos-Guerrero et al., 2018}; ^{Berumen-Varela et al., 2015}). In sodium silicate micrographs (Figure 3D), compared to negative control a dehydration effect can be observed on hyphae, these alterations could be caused due by damage of cell membrane affecting its permeability, as previously reported (^{Wang et al., 2010}). Combined treatments (Figure 3F) showed unhealthily and contracted mycelium, multiple deformations, and the dehydration effect also can be observed, as a result of the additive effect of treatments.

Conclusions

The application of sodium silicate with chitosan can be used as an eco-friendly alternative in the control of C. gloeosporioides in papaya fruits.

Acknowledgement

The authors are grateful to Institute of Ecology (INECOL) and CONACYT for the fellowship granted to Edson Rayón-Díaz, this study is the product of ERD´s master´s thesis.

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Cite this paper: Rayón-Díaz, E., Birke-Biewendt, A. B., Velázquez-Estrada, R. M., González-Estrada, R. R., Ramírez-Vázquez, M., Rosas-Saito, G. H., Gutiérrez-Martínez, P. (2021). Sodium silicate and chitosan: an alternative for the in vitro control of Colletotrichum gloeosporioides isolated from papaya (Carica papaya L.). Revista Bio Ciencias 8, e1059. doi: https://doi.org/10.15741/revbio.08.e1059

Authors’ contributions ERD: Ran the experiments and collected the experimental data, wrote de manuscript, ABBB: determining the effectiveness of treatments using the Abbott method, reviewed the manuscript, RMVE: performed the statistical analysis, RRGE: reviewed the manuscript, MRV, and GHRS: prepared the SEM samples, and analyzed the images, PGM: designed the experiment, supervised the experimental research, wrote the manuscript.

Received: September 09, 2020; Accepted: March 22, 2021

Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons