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Original article
05 2023
:16;
104677
doi:
10.1016/j.arabjc.2023.104677

Leaves of Chenopodium album as source of natural fungicides against Sclertium rolfsii

, , ,
aDepartment of Plant Pathology, Faculty of Agricultural Sciences, University of the Punjab, Quaid-i-Azam Campus, Lahore 54590, Pakistan
bDepartment of Horticulture, Faculty of Agricultural Sciences, University of the Punjab, Quaid-i-Azam Campus, Lahore 54590, Pakistan

⁎Corresponding author. malikferdosi@yahoo.com (Malik F. H. Ferdosi) fiaz.iags@pu.edu.pk (Malik F. H. Ferdosi)

Received: , Accepted: ,
© The Author(s) 2023
Disclaimer:
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.

Peer review under responsibility of King Saud University.

Abstract

Series of experiments were conducted to identify the possible antifungal components of Chenopodium album leaves for the management of a highly destructive soil-borne fungal pathogen Sclerotium rolfsii. A 4% methanolic extract caused up to 82% reduction in biomass of the target organism. This extract was partitioned using solvents of variable polarities, and the obtained subfractions were evaluated for their activity against S. rolfsii. The best antifungal activity was detected for the ethyl acetate subfraction (60–74%) followed by n-hexane (51–69%), n-butanol (50–60%), chloroform (20–40%) while the aqueous sub-fraction had the lowest activity (9–35%) as detected by the decrease in biomass of the pathogen. Ethyl acetate and n-hexane sub-fractions were analyzed for their chemical constituents by GC–MS technique. Literature survey showed that among the identified compounds kitazin P, imidazole-4-carboxylic acid, 2-fluoro-1-methoxymethyl-, ethyl ester and 9,12,15-octadecatrienoic acid, 2,3-dihydroxypropyl ester, (Z,Z,Z)- had antifungal activities against other fungal species and could be responsible for control of S. rolfsii by methanolic extract in the present study.

Keywords

Environmental friendly
Lamb's quarters
Natural fungicides
Sclerotium rolfsii
1

1 Introduction

The soil-borne fungus S. rolfsii commonly occurs in tropical and sub-tropical as well as warmer areas of the globe (Rajani et al., 2019). It can cause stem, root and foot rot diseases in above 500 diverse plant species (Awasthi et al., 2018; Jabeen et al., 2022). It has the ability to produce resistant sclerotia in large quantities under humid weather conditions that can survive in the soil for several years (Kumar, 2018). Its management has become a major concern in agriculture (Tarafdar et al., 2018). The use of chemical fungicides is considered as the most effective management strategy for the control of this devastating pathogen (Faruk, 2019). However, this strategy has some complexities as synthetic fungicides also pollute the environment, induce harmful effects on non-targeted beneficial microorganisms, and are toxic to the human and wild life (Rani et al., 2018). Therefore, many scientists have focused to develop alternative management strategies to control plant diseases that are safe in use with less or no toxic effects (Smolinska and Kowalska, 2018; Javaid et al., 2019; Khan and Javaid, 2023).

Among the various practices, the application of natural plant products has provided a promising substitute to synthetic products for the effective control of S. rolfsii with no hazardous impact on the natural habitats (Ragavi et al., 2017). The application of Moringa oleifera (Nweke, 2015); Hydnocarpus anthelminthicus (Jantasorn et al., 2016); Lantana camara and Acorus calamus (Bapat et al., 2016); Melia azedarach (Javaid and Khan, 2016), Cymbopogon nardus and Azadirachta indica (Ali et al., 2017), Ocimum basilicum (Nugroho et al., 2019), Eucalyptus citriodora (Javaid et al., 2020), Chenopodium album (Ali et al., 2020), Azadirachta indica (Khan et al., 2020) and Datura metel (Jabeen et al., 2021) have been used previously to control S. rolfsii. Chenopodium album is a weed plant distributed widely in Europe, America and Asia (Bajwa et al., 2019). In Pakistan, it is commonly known as “Bathu” and is utilized in traditional medicinal system to treat rheumatism, sunstroke, chronic fever, asthma, insect bites, urinary and skin problems (Trivedi and Singh, 2018). It contains alkaloids, aldehydes, flavonoids, isoflavonoids, saponins, polyphenols and apocarotenoids with potent fungicidal activities against Rhizoctonia solani, Fusarium solani, F. oxysporum, Macrophomina phaseolina, Pythium sp., Sclerotinia sclerotium and Ascochyta rabiei (Rauf and Javaid, 2013; Sherazi et al., 2016; Alkooranee et al., 2020; Shirazi et al., 2020). However, literature about its antifungal properties against S. rolfsii is scarce. Thus the aim of this study was to assess fungicidal potential of leaf extract of C. album against S. rolfsii and to identify possible antifungal phytoconstituents through GC–MS study.

2

2 Experimental

2.1

2.1 Isolation of S. rolfsii from diseased chickpea seedlings

The fungal pathogen S. rolfsii was isolated from infected chickpea seedlings. For this purpose, soil was collected from four fields from Lahore, Pakistan with different cropping histories. Earthen pots (20 cm diameter) were filled with different soil samples in triplicates. Chickpea seeds were surface sterilized with 1 % sodium hypochlorite for 3 min followed by thorough washing with sterilized water. These seeds were sown in the pots and irrigated with tap water. After two weeks of germination, the seedlings showing symptoms of collar rot disease were collected. Diseased portions were separated and surface sterilized with 1 % sodium hypochlorite followed by culturing on autoclaved malt extract agar medium. After three days, the emerging hyphae were cultured on fresh media plates and incubated at 28 °C for 10 days. The fungus was identified on the basis of morphological characters, especially the formation of sclerotia. In order to confirm its pathogenicity, the isolated fungal pathogen was artificially inoculated in heat sterilized soil and chickpea seeds were sown in the pots. Appearance of collar rot disease followed by isolation of the same fungal pathogen confirmed the pathogenicity of the fungus.

2.2

2.2 Antifungal bioassays with methanolic extract

Leaves were collected from mature plants of C. album from Lahore, Pakistan. After washing under tap water, the leaves were dried under shade, and crushed thoroughly. Three kilograms of this material were drenched in 10 L of methanol for two weeks. After filtration, the solvent was evaporated on a rotary evaporator and a gummy biomass (200 g) was obtained that was used in laboratory bioassays as well as for further fractionation. For antifungal bioassays with methanolic leaf extract, 9 g of the gummy mass was dissolved in 5 mL dimethyl sulfoxide (DMSO) and 1, 2, 3, 4 and 5 % concentrations were made using malt extract (ME) broth. Media flasks were inoculated with mycelial disks of S. rolfsii (5 mm), incubated at 28 °C and left for 7 days. Experiment was conducted in a completely randomized design with four replications. After one-week, fungal mats from each test tube were filtered, dried and weighed (Javaid et al., 2020).

2.3

2.3 Antifungal bioassays with fractions of methanolic extract

Two hundred milliliters of d·H2O was added to the remaining methanolic extract (191 g), shacked well and sequentially partitioned with four organic solvents. After evaporation of the solvents, finally 10.4 g n-hexane, 17.5 g chloroform, 2.1 g ethyl acetate, 5.8 g n-butanol and the remaining aqueous sub-fraction was collected. For antifungal bioassays, 1.2 g of each sub-fraction was dissolved in 1 mL of DMSO and then 5 mL of ME broth was added to prepare a medium of 200 mg/mL that was used to prepare lower concentrations viz. 100, 50, 25, 12.5, 6.25 and 3.125 mg/mL. A similar control set was also prepared only with DMSO and without extracts. Antifungal experiments were done in test tubes using 1 mL of the growth medium. Experiment was done in a completely randomized design in triplicates in 10-mL tubes each with 1 mL of the medium. Fungal harvest was taken after 7 days growth at 28 ℃. The collected fungal material was dried at 70 °C and weighed (Khan and Javaid, 2020). The whole extraction procedure is presented in Fig. 1.

Schematic diagram showing extraction procedure of Chenopodium album leaves.
Fig. 1
Schematic diagram showing extraction procedure of Chenopodium album leaves.

2.4

2.4 GC–MS analysis

Two sub-fractions of leaf extract viz. ethyl acetate and n-hexane were analyzed by GC–MS. These fractions were dissolved in the respective solvents and passed through Millipore filter papers to remove any suspended particles. Analysis of GC–MS was done on an Agilant technologies model GC-7890A, attached to MS 5975C mass spectrometer.

2.5

2.5 Statistical analysis

Data regarding bioassays with methanolic leaf extract as well as with sub-fractions of methanolic leaf extract were subjected to ANOVA and then LSD test was applied at P ≤ 0.05 by using Statistix 8.1 software.

3

3 Results and discussion

3.1

3.1 Antifungal activity of methanolic leaf extract

Methanolic leaf extract was very effective in controlling the growth of S. rolfsii. The inhibitory effect was increased with increase in concentrations of the extract. There was 29 % decrease in biomass of S. rolfsii due to 1 % extract while a 4 % concentration of the extract caused 82 % decline in the fungal growth (Fig. 2 A&B). A linear relationship was observed between concentrations of the extract and biomass of S. rolfsii with R2 = 0.97 (Fig. 2C). In accordance to the present study, earlier Sherazi et al. (2016) reported that a 7 % concentration of methanolic leaf extract of C. album inhibited the growth of A. rabiei by 68 %. Similarly, Alkooranee et al. (2020) worked on C. album leaves and root extracts that caused a significant reduction in growth of Rhizoctonia solani, Sclerotinia sclerotium, Fusarium solani, Alternaria alternata and Pythium aphanidermatum. C. album also found to be highly effective in arresting the growth of Fusarium Oxysporum and Macrophomina phaseolina even at lower concentrations (Shirazi et al., 2020). Semina et al. (2016) also exhibited a remarkable decrease in Bipolaris sorokiniana and A. alternata biomasses by exploiting the antifungal potential of C. album seed extracts. Previously, C. album leaf extracts showed a remarkable growth inhibition against Stagonospora nodorum, Phytophthora infestans, F. oxysporum, Fusarium culmorum, Alternaria tenuissima, A. alternata and F. solani (Javaid and Rauf, 2015; Pushkareva et al., 2017; Ullah et al., 2018).

Effect of different concentrations of methanolic leaf extract of Chenopodium album on biomass of Sclerotium rolfsii. Vertical bars show standard errors of means of four replicates. Values with different letters at their top show significant difference (P ≤ 0.05) as determined by LSD Test.
Fig. 2
Effect of different concentrations of methanolic leaf extract of Chenopodium album on biomass of Sclerotium rolfsii. Vertical bars show standard errors of means of four replicates. Values with different letters at their top show significant difference (P ≤ 0.05) as determined by LSD Test.

3.2

3.2 Antifungal activity of sub-fractions of methanolic extract

The effect of various sub-fractions of leaf extract on S. rolfsii growth is demonstrated in Figs. 3 and 4. These sub-fractions of the methanolic extract had variable suppressive effects on the growth of S. rolfsii. n-Hexane and ethyl acetate sub-fractions showed the better activity than the other fractions and reduced fungal biomass by 51–69 % and 60–74 % over respective control treatments. n-Butanol sub-fraction also showed a considerable antifungal potential by suppression fungal biomass production by 50–60 %. By contrast, chloroform and aqueous sub-fractions presented very low antifungal activities and caused only 25–40 % and 9–35 % reduction in biomass of the target pathogen, respectively. Methanolic leaf extract was partitioned using different organic solvents of diverse polarities. This technique is very useful in separating compounds into smaller groups on the basis of their polarities. In the present study, bioassays with the sub-fractions of methanolic leaf extracts showed that different organic solvent sub-fractions had highly variable antifungal potentials against the target pathogen. Ethyl acetate and n-hexane sub-fractions were the most antifungal in nature while n-butanol and chloroform sub-fractions were proved moderately and less antifungal. Previous studies also showed a highly variability in fungicidal potential of various sub-fractions of methanolic extracts. Similar to that in the present study, ethyl acetate and n-hexane sub-fractions of Cenchrus pennisetiformis and Senna occidentalis were highly effective in controlling growth of Fusarium oxysporum and Macrophomina phaseolina, respectively (Javaid et al., 2017; Khurshid et al., 2018). In contrast to the present study where chloroform sub-fraction showed very low antifungal activity, previously chloroform sub-fractions of Sisymbrium irio, Nogella sativa and Tribulus terrestris showed remarkable antifungal activities causing 80–96 %, 48–100 % and 54–82 % reduction in biomass of F. oxysporum, M. phaseolina and Pyricluaria oryzae, respectively (Aftab et al., 2019; Javaid et al., 2019; Akhtar et al., 2020).

Effect of different concentrations of sub-fractions of methanolic leaf extract of Chenopodium album on growth of Sclerotium rolfsii. Vertical bars show standard errors of means of three replicates. Values with different letters at their top show significant difference (P ≤ 0.05) as determined by LSD Test.
Fig. 3
Effect of different concentrations of sub-fractions of methanolic leaf extract of Chenopodium album on growth of Sclerotium rolfsii. Vertical bars show standard errors of means of three replicates. Values with different letters at their top show significant difference (P ≤ 0.05) as determined by LSD Test.
Percentage decrease in biomass of Sclerotium rolfsii due to different fractions of methanolic leaf extract of Chenopodium album over control.
Fig. 4
Percentage decrease in biomass of Sclerotium rolfsii due to different fractions of methanolic leaf extract of Chenopodium album over control.

3.3

3.3 GC–MS analysis

There were 8 compounds in n-hexane sub-fraction as presented in Table 1. The most abundant compound was 9,10-dimethyltricyclo[4.2.1.1(2,5)]decane-9,10-diol with 44 % peak area. Three compounds namely estra-1,3,5(10)-trien-17.beta-ol (10.42 %), 5,6,6-trimethyl-5-(3-oxobut-1-enyl)-1-oxaspiro[2.5]octan-4-one (8.89 %) and kitazin P (8.78 %) were recognized as moderately abundant ones. Other compounds such as 7-methyl-Z-tetradecan-1-ol acetate (6.69 %), and oleic acid (6.10 %) were comparatively less abundant.

Table 1 Compounds identified from n-hexane sub-fraction of methanolic leaf extract of Chenopodium album through GC–MS analysis.
Comp. No. Names of compounds Molecular Formula Molecular weight Retention time (min) Peak area (%)
1 1H-2-Indenone,2,4,5,6,7,7a-hexahydro-3-(1-methylethyl)-7a-methyl C13H20O 192 11.231 6.50
2 9,12,15-Octadecatrienoic acid,2,3-dihydroxypropyl ester, (Z,Z,Z)- C21H36O4 352 15.692 7.97
3 7-Methyl-Z-tetradecan-1-ol acetate C17H32O2 268 16.286 6.69
4 9,10-Dimethyltricyclo[4.2.1.1(2,5)]decane-9,10-diol C12H20O2 196 17.314 44.65
5 5,6,6-Trimethyl-5-(3-oxobut-1-enyl)-1-oxaspiro[2.5]octan-4-one C14H20O3 236 17.747 8.89
6 Kitazin P C13H21O3 288 18.053 8.78
7 Estra-1,3,5(10)-trien-17.beta-ol C18H24O 256 19.200 10.42
8 Oleic acid C18H34O2 282 20.874 6.10

Table 2 shows the details of compounds present in ethyl acetate sub-fraction. There were 9 compounds in this sub-fraction with dl-arabinose (27.18 %) as the most abundant compound followed by 5,6,6-trimethyl-5-(3-oxobut-1-enyl)-1oxaspiro[2.5]octan-4-one (18.35 %). Three compounds namely 1,3-pentanediol,4-methyl-2-nitro- (13.23 %), imidazole-4-carboxylic acid, 2-fluoro-1-methoxymethyl-, ethyl ester (11.91 %) and dithiocarbamate, S-methyl-,N-(2-methyl-3-oxobutyl)- (9.18 %) were categorized as moderately abundant compounds. Other compounds such as pantoactone (5.69 %), 2(3H)-furanone, dihydro-4,4-dimethyl (4.55 %), N-(O-nitrophenylthio)-l-leucine (5.60 %), pregan-20-one, 2-hydroxy-5,6-epoxy-15-methyl- (4.27 %) were present in less concentrations.

Table 2 Compounds identified from ethyl acetate sub-fraction of methanolic leaf extract of Chenopodium album through GC–MS analysis.
Comp. No. Names of compounds Molecular Formula Molecular weight Retention time (min) Peak area (%)
1 Pantoactone C6H10O3 130 8.046 5.69
2 dl-Arabinose C5H10O5 150 9.711 27.18
3 2(3H)-Furanone,dihydro-4,4-dimethyl C6H10O2 114 10.195 4.55
4 1,3-Pentanediol,4-methyl-2-nitro- C6H13NO4 163 10.875 13.23
5 Imidazole-4-carboxylic acid, 2-fluoro-1-methoxymethyl-, ethyl ester C8H11FN2O3 202 12.149 11.91
6 N-(O-Nitrophenylthio)-l-leucine C12H16N20O4 284 12.370 5.60
7 Dithiocarbamate, S-methyl-, N-(2-methyl-3-oxobutyl)- C7H13NO2 191 12.863 9.18
8 5,6,6-Trimethyl-5-(3-oxobut-1-enyl)-1oxaspiro[2.5]octan-4-one C14H20O3 236 17.943 18.35
9 Pregan-20-one, 2-hydroxy-5,6-epoxy-15-methyl- C22H34O3 346 18.979 4.27

GC–MS analysis of C. album identified prominent antifungal compounds that might be responsible in inhibiting the growth of S. rolfsii. El-Din and Mohyeldin (2018) isolated 5,6,6-trimethyl-5-(3-oxobut-1-enyl)-1-oxaspiro[2.5]octan-4-one from the methanolic extracts of Cystoseira barbata with strong antifungal activities against Aspergillus niger, A. flavus and F. solani. Similarly, imidazole-4-carboxylic acid, 2-fluoro-1-methoxymethyl-, ethyl ester and dl-arabinose exhibited the excellent antifungal potential against Aspergillus terreus (Hussein et al., 2016; Mohammed et al., 2018). Aguiar et al. (2014) also reported the fungicidal potential of kitazin P against Colletotrichum musae, Aspergillus spp., Magnaporthe grisea and Pyricularia grisea. Likewise, 9,12,15-octadecatrienoic acid, 2,3-dihydroxypropyl ester, (Z,Z,Z)- and oleic acid were identified from the methanoilc leaf extracts of Mesembryanthemum edule and Sesuvium portulacastrum respectively, with potent activities against Candida albicans (Omoruyi et al., 2014; Adeyemi et al., 2017). Likewise, inhibitory potential of 7-methyl-Z-tetradecan-1-ol acetate and 2(3H)-furanone, dihydro-4,4-dimethyl was tested against A. niger and F. solani, respectively (Kokila et al., 2016; Petre et al., 2017) as shown in Table 3.

Table 3 Potential antifungal compounds in n-hexane and ethyl acetate sub-fractions of methanolic leaf extract of Chenopodium album.
Sr. No. Names of compounds Target fungal species Reference
1. 5,6,6-Trimethyl-5-(3-oxobut-1-enyl)-1-oxaspiro[2.5]octan-4-one Aspergillus niger, A. flavus and Fusarium solani El-Din and Mohyeldin (2018)
2. Kitazin P Colletotrichum musae, Aspergillus spp., Magnaporthe grisea and P. grisea Aguiar et al. (2014); Zhang et al. (2004)
3. 9,12,15-Octadecatrienoic acid,2,3-dihydroxypropyl ester, (Z,Z,Z)- Candida albicans Omoruyi et al. (2014)
4. 7-Methyl-Z-tetradecan-1-ol acetate A. niger Kokila et al. (2016)
5. Oleic acid C. albicans, A. fumigatus and A. niger Verma et al. (2014); Chandrasekaran et al. (2011)
6. dl-Arabinose Aspergillus terreus Mohammed et al. (2018)
7. Imidazole-4-carboxylic acid, 2-fluoro-1-methoxymethyl-, ethyl ester A. terreus Hussein et al. (2016)
8. 2(3H)-Furanone, dihydro-4,4-dimethyl F. solani Petre et al. (2017)

4

4 Conclusion

This study concludes that methanolic leaf extract is highly antifungal against S. rlfsii. The potential antifungal constituents were mostly present in n-hexane and ethyl acetate sub-fractions. Further studies are recommended to isolate the potential antifungal ingredients and use them for the preparation of natural fungicides to control S. rolfsii.

5

5 Author’s contribution

Amna Ali carried out experimental work. Arshad Javaid supervised the whole work, write a part of paper and also did statistical analysis. Iqra Haider Khan contributed in writing of the manuscript. Malik F. H. Ferdosi did final editing and proof reading of the paper.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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