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Journal of Phytopathology - 2021 - González‐Merino - Antifungal activity of zinc oxide nanoparticles in Fusarium
Journal of Phytopathology - 2021 - González‐Merino - Antifungal activity of zinc oxide nanoparticles in Fusarium
Journal of Phytopathology - 2021 - González‐Merino - Antifungal activity of zinc oxide nanoparticles in Fusarium
DOI: 10.1111/jph.13023
ORIGINAL ARTICLE
1
Departamento de Parasitología,
Universidad Autónoma Agraria Antonio Abstract
Narro, Saltillo, México Antifungal activity of zinc oxide (ZnO) and ZnO nanoparticles (ZnO NPs) was evalu-
2
Centro de Investigación en Química
ated on the control of Fusarium oxysporum Schltdl. (Nectriaceae) under laboratory
Aplicada, Saltillo, México
3
Departamento de Horticultura, Universidad
and greenhouse conditions. In vitro evaluation, poisoned culture media was pre-
Autónoma Agraria Antonio Narro, Saltillo, pared, and an explant was placed in the centre of solid medium. The experimental
México
design was completely randomized with 18 treatments. Mycelial growth and co-
Correspondence nidia concentration were evaluated. Subsequently, three treatments (3,000, 1,500,
Agustín Hernández-Juárez, Departamento
de Parasitología, Universidad Autónoma
100 ppm) of ZnO NPs and ZnO were chosen for their evaluation in the greenhouse in
Agraria Antonio Narro, Calzada Antonio tomato plants of Floradade variety under a randomized block design. Inoculation was
Narro # 1923, C.P. 25315. Buenavista,
Saltillo, Coahuila, México.
carried out with a 1x107 conidia per mL suspension of F. oxysporum, when the plants
Email: chinoahj14@hotmail.com presented the third pair of true leaves. Later, the application of different concentra-
tions of ZnO and ZnO NPs was carried out; in this investigation, the incidence and
severity and plant height were evaluated into account to determine the treatment ef-
fect on F. oxysporum. In vitro, the best treatments in mycelial growth inhibition were
the high concentrations of ZnO NPs from 1,600 to 3,000 ppm with 81%–83%, and
in the sporulation of the fungus, they were also those that inhibited from 82.57% to
83.85%. In greenhouse, the treatments that reached the highest plant height were
ZnO NPs from 1,500 to 3,000 ppm, with a range of 166.0–175.40 cm, with a severity
on the scale of 0.40–0.80 and an incidence of 20%–40%. ZnO NPs have a potential
application as an antifungal agent and can be used to control the spread of F. oxyspo-
rum in tomato plants, in addition to improving the promoter effect related to the Zinc
activity as a precursor in auxins synthesis, cytokinins and gibberellins biosynthesis,
as well as the induction of higher activity of antioxidant enzymes useful in response
to the pathogens attack.
KEYWORDS
Potato Dextrose Agar (PDA) (Bioxon®) and incubated at 27 ± 2℃ in a 100 ppm) and an absolute control (PDA = 0 ppm) with 4 replicates,
®
growth chamber (Yamato ), and from their growth, the strains were and it considered a Petri dish as one repetition.
purified by hypha point.
Morphological identification was carried out by mycelium struc- The evaluation consisted of measuring the mycelial growth, in two
tures and their respective conidia on slide with a lactophenol and axes (horizontal and vertical) of the phytopathogen, every 24 hr,
cotton blue solution. Its observation was performed at 40 and until the filling of the control (8 days), using as support a calliper
100X in a compound microscope, and for identification at the genus (vernier) with digital compound (Titan®). To count the conidia, the
level, it was supported by the taxonomic keys for imperfect fun- mycelium from Petri dishes was collected in dH2O, the suspen-
gal genera of Barnett and Hunter (1998) and at the species level sion was shaken to homogenize the concentration of conidia, and
with the keys of Leslie and Summerell (2006). Molecular identifi- then, 10 µl was taken and placed in the hemocytometer (Marienfeld
cation was performed by extracting DNA from the fungus, using Germany), following the steps and formulas of the guide provided
the CTAB protocol (Lee & Taylor, 1990). DNA was resuspended in by Celeromics (Total Cells Counted / Number of Frames × 10,000).
30 µl of nuclease-free water and stored at −20℃. The polymerase With the data obtained in the evaluation, the per cent of inhibition
chain reaction (PCR) was carried out in 25 µl containing 12.5 µl of of mycelial growth was calculated using the formula described by
Gotaq® DNA Polymerase (Promega corporation), 1 µl of each oligo- Orberá et al. (2009), taking as 100% the mycelial growth of the con-
nucleotide, FOF1: (5'-ACATACCACTTGTTGCCTCG-3') and FOR1: trol (0 ppm).
(5'-CGCCAATCAATTTGAGGAACG-3 ') at 0.35 µM and 20 ng of
genomic DNA, and the final volume was adjusted with nuclease-free
( )
R1 − R2
PIRG = × 100
water. The amplification conditions were as follows: an initial dena- R1
turation of 1 min at 95℃, followed by 25 cycles of 94℃ for 1 min,
52℃ for 30 s, 72℃ for 1 min and a final extension of 7 min at 72℃. Where:
The length of the amplified fragments was 340 bp, which were visu- PIRG: is the per cent of inhibition of radial growth.
alized on a 1% agarose gel (Mishra et al., 2003). R1: represents the average value of the radius of the fungus
growth (control).
R2: is the average value of the radius of the inhibited colony
2.6 | Evaluation in vitro (treatment).
When the seedlings presented the third pair of true leaves, the first
2.6.2 | Experimental design inoculation of F. oxysporum was performed with a suspension con-
taining 1 × 107 conidia. The pathogen was inoculated again 15 and
The in vitro effect of F. oxysporum by ZnO NPs and ZnO was evalu- 30 days after the first inoculation to clearly observe the manifesta-
ated in 8 concentrations (3,000, 2000, 1,600, 1,200, 800, 400, 200, tion of the disease. The different concentrations of ZnO NPs and
14390434, 2021, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jph.13023 by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [09/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
536 | GONZÁLEZ-MERINO et al.
ZnO were sprayed onto the foliage with a manual sprayer (RLFlo phytopathogen. Diseased plant tissue was disinfected and placed on
Master) 1900 ml capacity, the next day after each F. oxysporum PDA as previously described.
inoculation.
61%, the absolute control (without inoculation) 115% and the treat-
ments with ZnO NPs up to 118%, even higher than the control with-
out inoculation (Figures 4 and 5).
4 | D I S CU S S I O N
Rajiv et al. (2013) synthesized ZnO nanoparticles from Parthenium Regarding the sporulation of the fungus, with the treatment with
hysterophorus L. (Asteraceae) in different sizes and explored their an- ZnO NPs, its effect was correlated with the mycelial growth, inhib-
tifungal activity against A. flavus and A. niger, showing that ZnO NPs iting the conidia to a greater degree, compared with the control and
are good antifungal agents, inhibiting these phytopathogens with a the eight treatments with ZnO, an effect that can be attributed to
size of 27 ± 5 nm, in addition to being respectful to the environment. the fact that the nanoparticles induce damage to the hypha of the
Dimkpa et al. (2013) ratified the antifungal effect of ZnO NPs on fungus and at the same time to the conidia, a characteristic observed
Fusarium graminearum Schwabe (Nectriaceae), reducing the growth by Jo et al. (2009) and Lamsal et al. (2011) with Ag NPs (silver), who
of the phytopathogen, in addition to being supplemented with indicated that NPs influence the formation of spore colonies, damag-
the biological control agent Pseudomonas chlororaphis O6 Bergey ing and penetrating the cell membrane, and the disease progression
(Pseudomonadaceae), by not inhibiting the metabolites of the bac- of plant pathogenic fungi.
teria, though it inhibit the development of F. graminearum, opening On the one hand, He et al. (2011) describe that ZnO NPs can
the possibility of using them as formulations to complement existing exhibit different antifungal activities. On the other hand, they ob-
strategies to improve crop health. served that P. expansum in PDA with ZnO NPs not only produced
Recently, Pariona et al. (2020) studied the in vitro antifungal ac- conidia but also inhibited their development and distorted conidio-
tivity of ZnO in three forms of particles, including NPs with a size phores, whereas the biomass of B. cinerea developed mainly hyphae,
of 18 ± 2 nm, for three species of fungi: F. oxysporum f.sp. lycop- with apparently more resistance to ZnO NPs, conserving the fine
ersici, Fusarium solani (Mart.) Sacc. (Nectriaceae) and Colletotrichum structure of the mycelia, although the surface of the hyphae of the
gloeosporioides (Penz.) Penz & Sacc. (Glomerellaceae), finding very fungi was deformed.
similar control results with 1 mg/ml against F. oxysporum with 54% Wani and Shah (2012) reported a high rate of inhibition in
and 53% inhibition by ZnO and ZnO NPs, respectively. At the same the germination of spores of the fungi Alternaria alternata (Fr.)
concentration in F. solani, the inhibition was 65% and 55% and for Keissl. (Pleosporales: Pleosporaceae), F. oxysporum, Rhizopus sto-
C. gloeosporioides 60% and 59% by ZnO and ZnO NPs, respectively. lonifer (Ehrenb.) Vuill. and Mucor plumbeus Bonord. (Mucorales:
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GONZÁLEZ-MERINO et al. | 539
F I G U R E 2 Antifungal activity of
(a) (b) (c)
ZnO NPs on Fusarium oxysporum in
vitro test: (a) 0 ppm, (b) 3,000 ppm, (c)
2000 ppm, (d) 1,600 ppm, (e) 1,200 ppm,
(f) 800 ppm, (g) 400 ppm, (h) 200 ppm and
(i) 100 ppm [Colour figure can be viewed
at wileyonlinelibrary.com]
TA B L E 3 Concentration inhibitory of
ppm
mycelial growth and sporulation inhibition
Fiducial limits 95% Fiducial limits 95% and fiducial limits of ZnO and ZnO NPs
applied to Fusarium oxysporum in PDA at
Treatments IC50 Lower Upper IC90 Lower Upper 8 days of evaluation
Mycelial growth inhibition (%)
ZnO NPs 364.40 286.54 446.37 5,017 3,537 8,081
ZnO 776.04 465.94 1,191 3,329 1943 11,401
Sporulation inhibition (%)
ZnO NPs 186.46 111.94 264.71 8,327 4,744 20,327
ZnO 545.68 416.40 694.56 17,072 9,245 43,671
Abbrevaitions: IC50, 50% growth inhibitory concentration; IC90, 90% growth inhibitory
concentration; ppm, parts per million.
TA B L E 4 Plant height, incidence and severity of damage by Fusarium oxysporum ± standard deviation at different concentrations of ZnO
NPs and ZnO at 75 days after the first inoculation
Concentration
Treatments (ppm) Plant height (cm)a Incidence (%)a,b Severitya,c
(a) (b)
F I G U R E 4 Tomato plants S.
lycopersicum (a) inoculated with Fusarium
oxysporum, (b) absolute control without
inoculation of the phytopathogen [Colour
figure can be viewed at wileyonlinelibrary.
com]
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GONZÁLEZ-MERINO et al. | 541
(b) (e)
(c) (f)
Rhizpodaceae) to the exposure of ZnO NPs and NPs of magnesium The effect of ZnO NPs on plant growth is not fully distinguished.
oxide (MgO) at concentrations of 100 mg/L. In this regard, Navarro et al. (2008) suggest that nano-sized materials
Among the antifungal properties, attributed to the nanoscale with larger surface areas could more efficiently absorb, translocate
surface-to-volume ratio of ZnO NPs (Kriti et al., 2020), is the in- and retain nutrients in plants.
duction of deformations in the structure of fungal hyphae, nota- In other crops such as Capsicum annuum L. (Solanaceae), Méndez-
ble thinning of fibres in the hyphae and tendency to agglutinate Argüello et al. (2015) evaluated ZnO NPs doped with Ag at 2.5% in
(Arciniegas-Grijalba et al., 2017; Yehia & Ahmed, 2013); causing liq- the growth and production of biomass in seedlings, finding only an
uefaction of the cytoplasmic content, making it less electron-dense, increase in height of 16.8% compared with control plants.
with a significant detachment of the cell wall, which causes cell Most of the studies on NPs in plant pathology have examined
death of the pathogen, causing growth to stop (Arciniegas-Grijalba the direct antifungal and antibacterial activity against the pathogen
et al., 2017; Sawai & Yoshikawa, 2004; Yehia & Ahmed, 2013). in question (Ocsoy et al., 2013; Saharan et al., 2015; Strayer-Scherer
Additionally, ZnO NPs generate various other reactive oxygen spe- et al., 2018; Wani & Shah, 2012; Zabrieski et al., 2015).
cies, such as hydroxyl radicals and singlet oxygen, which in turn stim- In the present study, it was demonstrated that foliar application
ulate cell death (Jamdagni et al., 2018). of ZnO NPs inhibits the development of the disease and positively
14390434, 2021, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jph.13023 by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [09/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
542 | GONZÁLEZ-MERINO et al.
affects plant growth, presumably through better mineral nutrition samplings and experiments, revised the original draft and prepared
and host defence. The effect of ZnO at the nanoscale (25 nm) on the final manuscript. Rebeca Betancourt-Galindo designed the re-
plant growth and development was verified by Prasad et al. (2012) search and methodology and conducted samplings and experiments,
in the peanut crop Arachis hypogaea L. (Fabaceae), observing that and involved in writing—review and editing the final version of the
at 1,000 ppm it promoted the germination of seeds, plant vigour, manuscript. Yisa María Ochoa-Fuentes analyzed data, revised the
as well as increased stem and root growth, early flowering and in- original draft and prepared the final manuscript. Luis Alonso Valdez-
creased chlorophyll content and pod yield, although the increase in Aguilar revised the original draft and prepared the final manuscript
concentration (2000 ppm) presented adverse effects such as toxic- and involved in writing—review and editing the final version of the
ity in the growth and performance. manuscript; Mónica Lorena Limón-Corona conducted samplings and
Stampoulis et al. (2009) investigated the effects of five nano- experiments, revised the original draft and prepared the final manu-
materials including ZnO NPs in Cucurbita pepo L. (Cucurbitaceae) script. All authors have read and agreed to the published version of
in a hydroponic medium at 1,000 mg / L, finding that the NPs did the manuscript.
not affect germination, but did present toxicity on root length and
biomass. PEER REVIEW
In watermelon plants, Citrullus lanatus (Thunb.) Matsum. and The peer review history for this article is available at https://publo
Nakai, Elmer et al. (2018) evaluated the efficiency of the ZnO NPs ns.com/publon/10.1111/jph.13023.
and CuO on F. oxysporum and observed that the plants treated with
the nanoparticles had a range of disease classification values signifi- DATA AVA I L A B I L I T Y S TAT E M E N T
cantly lower than the control plants that were not treated. Data are available on request from the authors. All the data are in-
Recently, different antifungal activity of ZnO NPs effective in in- corporated in the manuscript.
terfering with the metabolism of phytopathogenic fungi was deter-
mined; it was observed that ZnO NPs at a concentration of 20 ppm ORCID
were effective in inhibiting spore germination on Bipolaris sorokin- Agustín Hernández-Juárez https://orcid.
iana (Sorokin) Shoemaker (Pleosporaceae) and at 10 ppm effective org/0000-0001-7059-4471
for Alternaria brassicicola (Schwein.) Wiltshire (Pleosporaceae) and
at 100 ppm significantly inhibit mycelial growth of both pathogens REFERENCES
(Kriti et al., 2020). Abdallah, R. A. B., Jabnoun-Khiareddine, H., Nefzi, A., Ayed, F., & Daami-
The lower mycelial growth in vitro and the reduction of the Remadi, M. (2019). Field suppression of Fusarium wilt and microbial
population shifts in tomato rhizosphere following soil treatment with
disease in the crop suggest an effective action of ZnO NPs, on the
two selected endophytic bacteria. Eurasian Journal of Soil Science, 8,
growth of the fungus F. oxysporum; in addition, enhancing the pro- 208–220.
moter effect by the action of zinc as a precursor of various phys- Apodaca-Sánchez, M. A., Zavaleta-Mejía, E., Osada-Kawasoe, S., & García-
iological mechanisms in plants highlights the feasibility of these Espinoza, R. (2004). Pudrición de la corona de chile (Capsicum annum
L.) en Sinaloa, México. Revista Mexicana de Fitopatología, 22, 22–29.
nanoparticles as an alternative management of F. oxysporum in
Arciniegas-Grijalba, P. A., Patiño-Portela, M. C., Mosquera-Sánchez, L. P.,
tomato. Guerrero-Vargas, J. A., & Rodríguez-Páez, J. E. (2017). ZnO nanopar-
ticles (ZnO NPs) and their antifungal activity against coffee fungus
Erythricium salmonicolor. Applied Nanoscience, 7, 225–241. https://
doi.org/10.1007/s13204-017-0561-3
5 | CO N C LU S I O N
Aydi Ben Abdallah, R., Mokni-Tlili, S., Nefzi, A., Jabnoun-Khiareddine, H.,
& Daami-Remadi, M. (2016). Biocontrol of Fusarium wilt and growth
ZnO NPs showed antifungal activity inhibiting in vitro mycelial promotion of tomato plants using endophytic bacteria isolated from
growth and sporulation of Fusarium oxysporum. Foliar application Nicotiana glauca organs. Biological Control, 97, 80–88. https://doi.
of ZnO NPs decreased the incidence and severity of the disease org/10.1016/j.biocontrol.2016.03.005
Barnett, H. L., & Hunter, B. B. (1998). Illustrated genera of imperfect fungi.
caused by F. oxysporum, allowing the growth of tomato plants. ZnO
APS Press.
NPs have the potential as a biostimulant to promote plant growth Betancourt, G. R., Berlanga, D. M. L., Puente, U. B., Rodríguez, F. O., &
and to be used in the prevention and control of plant deterioration Sanchez-Valdes, S. (2010). Surface modification of ZnO nanoparti-
by phytopathogenic microorganisms. cles. Materials Science Forum, 644, 61–6 4.
Cardona-Piedrahíta, L. F., & Castaño-Zapata, J. (2019). Comparación
de métodos de inoculación de Fusarium oxysporum f. sp. lycopersici
C O N FL I C T O F I N T E R E S T (Sacc.) Snyder & Hansen, causante del marchitamiento vascular del
The authors declare no conflict of interest. tomate. Revista De La Academia Colombiana De Ciencias Exactas,
Físicas Y Naturales, 43, 227–233.
Clavijo, C. S. D. (2014) Búsqueda de resistencia a la pudrición causada por
AU T H O R C O N T R I B U T I O N S
Fusarium spp. en Capsicum. Universidad Nacional de Colombia. Thesis.
Ana María González-Merino designed the research and methodol- Coromoto, A. Y., & Reyes, I. (2018). Microorganismos promotores de cre-
ogy, and conducted samplings and experiments. Agustín Hernández- cimiento en el biocontrol de Alternaria alternata en tomate (Solanum
Juárez designed the research and methodology, conducted lycopersicum L.). Bioagro, 30, 59–66.
14390434, 2021, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jph.13023 by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [09/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
GONZÁLEZ-MERINO et al. | 543
Dimkpa, C. O., McLean, J. E., Britt, D. W., & Anderson, A. J. (2013). Méndez-Argüello, B., Vera-Reyes, I., Mendoza-Mendoza, E., García-
Antifungal activity of ZnO nanoparticles and their interactive ef- Cerda, L. A., Puente Urbina, B. A., & Lira-Saldívar, R. H. (2016).
fect with a biocontrol bacterium on growth antagonism of the plant Promoción del crecimiento en plantas de Capsicum annuum por
pathogen Fusarium graminearum. BioMetals, 26, 913–924. https://doi. nanopartículas de óxido de zinc. Nova Scientia, 8, 140–156. https://
org/10.1007/s10534-013-9667-6 doi.org/10.21640/ns.v8i17.544
Elmer, W., De La Torre-Roche, R., Pagano, L., Majumdar, S., Zuverza- Mishra, P. K., Fox, R. T., & Culham, A. (2003). Development of a PCR-
Mena, N., Dimkpa, C., Gardea-Torresdey, J., & White, J. C. (2018). based assay for rapid and reliable identification of pathogenic
Effect of metalloid and metal oxide nanoparticles on Fusarium Fusaria. FEMS Microbiology Letters, 218, 329–332. https://doi.
wilt of watermelon. Plant Disease, 102, 1394–1401. https://doi. org/10.1111/j.1574-6968.2003.tb11537.x
org/10.1094/PDIS-10-17-1621-RE Navarro, E., Piccapietra, F., Wagner, B., Marconi, F., Kaegi, R., Odzak,
Elmer, W., & White, J. C. (2018). The future of nanotechnology in plant N., Sigg, L., & Behra, R. (2008). Toxicity of silver Nanoparticles to
pathology. Annual Review of Phytopathology, 56, 111–133. https://doi. Chlamydomonas reinhardtii. Environmental Science and Technology, 42,
org/10.1146/annurev-phyto- 0 80417-050108 8959–8964.
Esparza, A. I. J. E. (2016) Potencial antimicrobial de nanopartículas metáli- Ocsoy, I., Paret, M. L., Arslan, O. M., Kunwar, S., Chen, T., You, M., &
cas en microorganismos fitopatógenos y su potencial como promotores Tan, W. (2013). Nanotechnology in plant disease management: DNA-
de crecimiento en plantas. Universidad Autónoma Agraria Antonio directed silver nanoparticles on graphene oxide as an antibacterial
Narro. Thesis. against Xanthomonas perforans. ACS Nano, 7, 8972–8980.
Esparza-Rivera, E., Lira-Saldivar, R. H., Hernández-Suárez, M., Orberá, R. T. M., Serrat, D. M. J., & González, G. Z. (2009). Potencialidades
Betancourt-Galindo, R., García-Cerda, L. A., & Puente-Urbina, B. de bacterias aerobias formadoras de endosporas para el biocontrol
(2014). Actividad antimicrobial de nanopartículas de cobre y óxido de en plantas ornamentales. Fitosanidad, 13, 95–100.
zinc contra bacterias y hongos fitopatógenos. Conference 36 Congreso Pariona, N., Paraguay-Delgado, F., Basurto-Cereceda, S., Morales-
Internacional de Metalurgia y Materiales. Mendoza, J. E., Hermida-Montero, L. A., & Martinez-Enriquez, A. I.
FIRA (Fideicomisos Instituidos en Relación con la Agricultura). (2019) (2020). Shape-dependent antifungal activity of ZnO particles against
Panorama Agroalimentario. Tomate Rojo. Internet Resource: https:// phytopathogenic fungi. Applied Nanoscience, 10, 435–4 43.
www.inforu ral.com.mx/wp-content/upload s/2019/06/Panora ma- Prasad, T. N. V. K. V., Sudhakar, P., Sreenivasulu, Y., Latha, P., Munaswamy,
Agroaliment ario-Tomate-rojo-2019.pdf (verified Dec 08, 2020) V., Reddy, K. R., Sreeprasad, T. S., Sajanlal, P. R., & Pradeep, T. (2012).
He, L., Liu, Y., Mustapha, A., & Lin, M. (2011). Antifungal activity of zinc Effect of nanoscale zinc oxide particles on the germination, growth
oxide nanoparticles against Botrytis cinerea and Penicillium expansum. and yield of peanut. Journal of Plant Nutrition, 35, 905–927. https://
Microbiological Research, 166, 207–215. https://doi.org/10.1016/j. doi.org/10.1080/01904167.2012.663443
micres.2010.03.003 Rajiv, P., Rajeshwari, S., & Venckatesh, R. (2013). Bio-Fabrication of zinc
Jamdagni, P., Khatri, P., & Rana, J. S. (2018). Green synthesis of zinc oxide oxide nanoparticles using leaf extract of Parthenium hysterophorus
nanoparticles using flower extract of Nyctanthes arbor-tristis and L. and its size-dependent antifungal activity against plant fungal
their antifungal activity. Journal of King Saud University-Science, 30, pathogens. Spectrochimica Acta Part A: Molecular and Biomolecular
168–175. Spectroscopy, 112, 384–387.
Jamdagni, P., Rana, J. S., & Khatri, P. (2019). Antioxidant activity and Raskar, S. V., & Laware, S. L. (2014). Effect of zinc oxide nanoparticles on
antifungal fractional inhibitory concentration indices of zinc oxide cytology and seed germination in onion. The International Journal of
nanoparticles in combination with carbendazim, mancozeb, and thi- Current Microbiology and Applied Science, 3, 467–473.
ram. Micro & Nano Letters, 14, 1037–1040. https://doi.org/10.1049/ Rivero, J. C. A., Díaz, G. J. A., & López, N. J. I. (2014). Agricultura
mnl.2019.0104 orgánica vs agricultura moderna como factores en la salud pública.
Jo, Y. K., Kim, B. H., & Jung, G. (2009). Antifungal activity of silver ions ¿Sustentabilidad? Horizonte Sanitario, 4, 28–4 0. https://doi.
and nanoparticles on phytopathogenic fungi. Plant Disease, 93, 1037– org/10.19136/hs.a4n1.304
1043. https://doi.org/10.1094/PDIS-93-10-1037 S.A.S. Institute. 2002. (2002). The SAS system for windows, release 9.0.
Kriti, A., Ghatak, A., & Mandal, N. (2020). Antimycotic efficacy of zinc SAS, Institute.
nanoparticle on dark-spore forming phytopathogenic fungi. Journal Saharan, V., Sharma, G., Yadav, M., Choudhary, M. K., Sharma, S. S., Pal,
of Pharmacognosy and Phytochemistry, 9, 750–754. A., Raliya, R., & Biswas, P. (2015). Synthesis and in vitro antifungal
Lamsal, K., Kim, S. W., Jung, J. H., Kim, Y. S., Kim, K. S., & Lee, Y. S. (2011). efficacy of Cu-chitosan nanoparticles against pathogenic fungi of to-
Application of silver nanoparticles for the control of Colletotrichum mato. International Journal of Biological Macromolecules, 75, 346–353.
species in vitro and pepper anthracnose disease in field. Mycobiology, Sawai, J., & Yoshikawa, T. (2004). Quantitative evaluation of antifungal
39, 194–199. activity of metallic oxide powders (MgO, CaO and ZnO) by an indirect
Lee, S. B., & Taylor, J. W. (1990). Isolation of DNA from fungal mycelia and conductimetric assay. Journal of Applied Microbiology, 96, 803–8 09.
single spores. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White Servin, A., Elmer, W., Mukherjee, A., De la Torre-Roche, R., Hamdi, H.,
(Eds.), PCR protocols a guide to methods and applications (pp. 282–314). White, J. C., Bindraban, P., & Dimkpa, C. (2015). A review of the use
Academic Press. of engineered nanomaterials to suppress plant disease and enhance
Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual. crop yield. Journal of Nanoparticle Research, 17, 17–92. https://doi.
Blackwell Publishing. org/10.1007/s11051-015-2907-7
Mejía, A. J., & Hernández, M. (2001). Evaluación de azoxystrobin en el SIAP (Servicio de Información Agroalimentaria y Pesquera). (2020)
control de la candelilla temprana (Alternaria solani) en el cultivo de Anuario estadístico de la producción agrícola. Cierre de la producción
tomate. Revista De La Facultad De Agronomía, Universidad Del Zulia, agrícola. Internet Resource: http://www.siap.go b.mx. (verified Dec
18, 106–116. 01, 2020).
Méndez-Argüello, B., Lira-Saldívar, R. H., Ruíz-Torres, N. A., Cárdenas- Singh, B. K., Rakesh, E. S., Yadav, V. P. S., & Singh, D. K. (2010). Adoption
Flores, A., Ponce-Zambrano, R., Vera-Reyes, I., Mendoza-Mendoza, of commercial cut flower production technology in Meerut. Indian
E., García-Cerda, L. A., & De los Santos, G., (2015). Influencia de Research Journal of Extension Education, 10, 50–53.
nanopartículas de óxido de zinc puras y dopadas con plata en el crec- Stampoulis, D., Sinha, S. K., & White, J. C. (2009). Assay-dependent
imiento y producción de biomasa en plántulas de chile. XVI Congreso phytotoxicity of nanoparticles to plants. Environmental Science and
Nacional de Biotecnología y Bioingeniería. Technology, 43, 9473–9479. https://doi.org/10.1021/es901695c
14390434, 2021, 9, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jph.13023 by Egyptian National Sti. Network (Enstinet), Wiley Online Library on [09/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
544 | GONZÁLEZ-MERINO et al.
Strayer-S cherer, A., Liao, Y. Y., Young, M., Ritchie, L., Vallad, G. E., on plant pathogenic isolates of Pythium. Ecotoxicology, 24, 1305–
Santra, S., Freeman, J. H., Clark, D., Jones, J. B., & Paret, M. L. 1314. https://doi.org/10.1007/s10646-015-1505-x
(2018). Advanced copper composites against copper-tolerant
Xanthomonas perforans and tomato bacterial spot. Phytopathology,
108, 196–205.
How to cite this article: González-Merino, A. M., Hernández-
Wani, A. H., & Shah, M. A. (2012). A unique and profound effect of MgO
Juárez, A., Betancourt-Galindo, R., Ochoa-Fuentes, Y. M.,
and ZnO nanoparticles on some plant pathogenic fungi. Journal of
Applied Pharmaceutical Science, 2, 40–4 4. Valdez-A guilar, L. A., & Limón-Corona, M. L. (2021).
Yehia, R. S., & Ahmed, O. F. (2013). In vitro study of the antifungal ef- Antifungal activity of zinc oxide nanoparticles in Fusarium
ficacy of zinc oxide nanoparticles against Fusarium oxysporum and oxysporum-Solanum lycopersicum pathosystem under
Penicilium expansum. African Journal of Microbiology Research, 7,
controlled conditions. Journal of Phytopathology, 169,
1917–1923.
Zabrieski, Z., Morrell, E., Hortin, J., Dimkpa, C., McLean, J., Britt, D., & 533–544. https://doi.org/10.1111/jph.13023
Anderson, A. (2015). Pesticidal activity of metal oxide nanoparticles