Next Article in Journal
Farmers’ Knowledge, Attitudes, and Control Practices of Rodents in an Agricultural Area of Taiwan
Next Article in Special Issue
Effect of Potassium (K) Supply on Cannabinoids, Terpenoids and Plant Function in Medical Cannabis
Previous Article in Journal
Novel Assessment of Region-Based CNNs for Detecting Monocot/Dicot Weeds in Dense Field Environments
Previous Article in Special Issue
Chemical Profile, Elemental Composition, and Antimicrobial Activity of Plants of the Teucrium (Lamiaceae) Genus Growing in Moldova
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Biological Activities of Zingiber officinale Roscoe Essential Oil against Fusarium spp.: A Minireview of a Promising Tool for Biocontrol

1
Departamento Ciencias de la Tierra, Universidad Estatal Amazónica, Km 2 ½ Vía Puyo-Tena, Puyo 160101, Ecuador
2
SIROE—Società Italiana per la Ricerca sugli Oli Essenziali, Viale Regina Elena 299, 00161 Rome, Italy
3
Departamento de Ciencias Biológicas, Facultad de Ciencias de la Salud, Universidad Técnica de Manabí, Avenida Urbina, Portoviejo 130105, Ecuador
4
Instituto de Investigación, Universidad Técnica de Manabí, Avenida Urbina, Portoviejo 130105, Ecuador
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(5), 1168; https://doi.org/10.3390/agronomy12051168
Submission received: 13 April 2022 / Revised: 6 May 2022 / Accepted: 7 May 2022 / Published: 12 May 2022
(This article belongs to the Special Issue Feature Papers on Medicinal and Aromatic Plants)

Abstract

:
Zingiber officinale Roscoe is an herbal plant native to Asia that can be found in all tropical countries. It is used in folk medicine, food, and cosmetics. A chemical characterization and some agronomic experiments have been carried out on Z. officinale essential oil, showing promising findings for the biological control of fungal pathogens belonging to the genus Fusarium. The aim of this review is to collect and update the literature covering its phytochemistry and biological activities as a Fusarium spp. plant-based biocide. The present research was conducted using the following bibliographic databases: Scifinder, Pubmed, and Science Direct. Thirteen papers were selected based on the adopted criteria. Data were independently extracted by the three authors of this work, and the final article selections were completed in a manner that avoided the duplication of data. The main chemical compounds were α-zingiberene, geranial, and aryl-curcumene, but a remarkable difference was found concerning the chemical compositions. Z. officinale essential oil was shown to possess promising biological functions against Fusarium spp. These findings offer new research approaches and potential applications as a biocontrol ingredient for Z. officinale essential oil.

1. Introduction

Several fungal species belonging to the Fusarium genus are phytopathogens and cause severe yield and quality losses for cultivated cereal grains such as maize, wheat, and rice [1] as well as plants such as coriander, cumin, fennel, and fenugreek [2]. Fusarium members can also be found as contaminants in stored agricultural commodities. Globally, there are grave concerns related to economic losses due to decreases in field production and contamination with mycotoxins [1].
The most common phytopathogen species are F. oxysporum [3], F. graminearum [1,4], F. verticillioides [5], and F. moniliforme. Fusarium spores are usually found in soil, and they infect plants through their roots. Fusarium species are causative agents of vascular system diseases that lead to the deterioration of host soft tissues and, consequently, plant necrosis [1,3]. Concerns also include the contamination of agricultural commodities with mycotoxins, which are secondary toxic metabolites produced by some fungal species, especially those belonging to the Aspergillus, Penicillium, and Fusarium genera.
The Food and Agriculture Organization estimates that about 25% of the world’s food crops are contaminated with mycotoxins; this has been recognized as a major health and economic problem due to the acute and chronic diseases they cause in humans and animals. Mycotoxin ingestion may lead to several health problems, such as carcinogenesis, neurotoxicity, and immunosuppressive effects; their toxicity may vary according to fungal species, human age, nutrition, and length of exposure. Hundreds of mycotoxins have been characterized, but the most relevant in terms of toxicity and occurrence are aflatoxins (AFs), ochratoxins (OTs), fumonisins (FMs), and trichothecenes (TRCs) [6].
The conventional treatment of infectious plant diseases caused by Fusarium involves the use of synthetic fungicides, but the adverse effects on the environment and human health require the development of safer solutions. Essential oils (EOs) have received attention from the research community due to their potential for developing biodegradable and plant-based fungicides [7,8].
EOs have been extensively investigated in many research fields, including pharmacology, food flavoring, soaps, cosmetics, and natural insecticides [9,10,11,12]. A large number of applications have been developed, and the scientific interest in EOs has increased in the last few decades. With respect to food science, the efficacy of EOs as antioxidant and antimicrobial food additives has been reported by several authors [13,14], and some interesting findings have been reported regarding the reduction in lipid oxidation in extra-virgin olive oil (EVOO) [15], antimicrobial and antioxidant activity in meat [16], the extension of shelf-life in vacuum-packaged fish fillets [17], and the preservation of unpasteurized fruit juice [18]. Additionally, EOs have been studied as additives for nanoemulsions [19] and edible films for food preservation [20]. All of these findings encourage new research concerning the use of EOs in food science.
EOs are oily liquids with a typical aromatic fragrance that are derived from a large number of plants; they can be obtained from different anatomical parts, such as leaves, flowers, bark, seeds, twigs, fruits, and roots. As reported by Sadgrove and Jones (2015), at the beginning of the 16th century, the concept of Eos was conceived by a Swiss medical pioneer who was studying a drug called “Quinta essentia” [21]. Essential oils have been identified as complex mixtures of several volatile compounds, including monoterpenes, sesquiterpenes, esters, ketones, aldehydes, and alcohols. A complete definition of EOs must include the extraction method because only steam distillation, dry distillation, and mechanical extraction from the epicarp of citrus fruits are acceptable methods that distinguish an EO from similar vegetal extracts, such as absolutes, concretes, alcoholates, and oleoresins [22].
Zingiber officinale Roscoe is a perennial herb belonging to the Zingiberaceae family and native to Southeast Asia and the Pacific Islands (Figure 1). Rhizomes are very popular in Asian folk medicine, and their traditional uses are widespread all over the world, mainly as flavoring agents for foods and beverages and as herbal remedies. Several authors have summarized the chemical composition of these plants [23,24], and some modern research articles have revealed new findings concerning their potential to ameliorate memory dysfunctions [25], metabolic syndromes [26], obesity management [27], and vascular diseases [28].
Additionally, the antimicrobial activities of Z. officinale derivatives have been investigated [29,30]; however, a specific focus on their potential as bio-microbicides is needed. The present study aimed to investigate the antifungal effect of Z. officinale EO against Fusarium spp. in order to describe the “state of the art” of a potential new plant-based treatment. The results may be useful for identifying novel strategies for the control of fungal pathogens belonging to the genus Fusarium.

2. Materials and Methods

Based on the PRISMA guidelines [31], the present review article was developed by selecting articles from the following scientific databases: PubMed (https://pubmed.ncbi.nlm.nih.gov/, accessed on 8 December 2021), SciELO (https://scielo.org/, accessed on 8 December 2021), ScienceDirect (https://www.sciencedirect.com/, accessed on 3 December 2021), SciFinder (https://scifinder.cas.org, accessed on 7 December 2021), and Wiley (https://onlinelibrary.wiley.com/, accessed on 6 December 2021). Mendeley software (https://www.mendeley.com/, accessed on 6 December 2021) was used to manage all bibliography references, and the search for and selection of the articles were independently performed by three researchers (i.e., LS, NRM, and MR) in a manner that avoided the duplication of data. The following keywords were used: “Zingiber officinale essential oil” and “Fusarium”. Both keywords were searched individually and in combination. Although we considered the literature of the past 20 years, we also included some key data in the Introduction and Discussion sections. Tables were prepared to represent the following criteria: the country where the research was performed, the main compounds found in the oil, the assay, the pathogen species, the results concerning antimicrobial activity, and the positive and negative controls. As reported in Figure 2, the above-mentioned criteria allowed the selection of 13 eligible articles, excluding 45 articles that did not meet the selection methodology either due to incomplete information or because they simply mentioned data concerning Fusarium infection without focusing on the topic of the present study.

3. Results

3.1. Geography and Focus of the Studies

As reported in the Materials and Methods section, the selection criteria allowed us to collect 13 articles covering a period between 2004 and 2020. India was the country in which the greatest number of studies was performed (4), followed by Brazil and China (2) and finally Cameroon, Egypt, Mexico, Nigeria, Romania, and Thailand (1).
Several Fusarium species were investigated, and we counted nine, four, three, one, and one experiments concerning the species F. oxysporum, F. moniliforme, F. graminearum, F. nivale, and F. verticillioides, respectively.

3.2. Z. officinale EO Composition

All of the selected experiments were performed on the Z. officinale rhizome without evidence concerning specific pretreatments; the preferred extraction method was found to be hydro-distillation by a Clevenger-type apparatus. Regarding the essential oil composition, α-zingiberene, geranial, and ar-curcumene were reported seven, four, and three times, respectively, in the top three compounds of the essential oil (Table 1). In accordance with [32], α-zingiberene and ar-curcumene were the major components of Z. officinale EO; these two compounds represented a percentage of the total EO content that ranged from 17.4% to 25.4% and from 14.1% to 16.4%, respectively. Even if the biological activity of essential oils may be attributed to the chemotype and the synergy between different components, these particular molecules nevertheless deserve attention in further research. However, the amount and the composition of the bioactive substances may vary according to different factors such as the harvest time; the climatic, geographic, and growing conditions; the extraction methods; etc. [32]. A research study from Sri Lanka [33] performed in 2021 reported α-zingiberene and ar-curcumene among the main compounds of Z. officinale EO. The study investigated the effect of maturity stage on the weight yield of two local varieties, Rangoon and Siddha, in comparison with a Chinese variety. The authors found that the highest quantity of essential oils was evident five months after sowing and decreased in the following months. This result seems to be related to a progressive increase in the fibrous matter of the rhizome after five months, at which point the amount of essential oil begins to decrease. Concerning the chemical composition, α-zingiberene was identified in EO obtained from both varieties, but with very different results. The Rangoon variety showed data regarding α-zingiberene content levels that ranged from 9.7% to 14.2% at five and eight months, respectively. In the same post-harvest period, the amount of α-zingiberene in the Siddha variety was between 0.0% and 1.6%. Z. officinale EO samples obtained from Ecuador [34] showed the presence of α-zingiberene at 17.4% of total composition and geranial at 10.5%. Another study from India (Sikkim) [35] detected the presence of α-zingiberene at 16.3% and 19.8% and geranial at 8.2% and 16.5% of the total composition of two local cultivars, named Bhaisa and Majulay, respectively. In 2001, an analysis of samples of Z. officinale EO from S. Tomé y Príncipe [36] revealed that geranial represented 13.4–16.0% of total composition, α-zingiberene was 8.3–15.1%, and ar-curcumene was 1.5–3.4%. All of these data confirm that EO composition can be affected by several factors, such as agricultural practices, the variety cultivated, and climatic conditions. Additionally, storage conditions and pretreatments can also influence the yield and composition of EOs [34]. According to ISO 16928:2014 [37], quality standards regarding chromatographic profile have been developed that take into account three different origin areas, namely China, India, and West Africa, and the values for α-zingiberene, geranial, and ar-curcumene ranged from 29% to 45%, 5.0% to 11.0% and 0.0% to 3.5%, respectively, with some minimal differences based on the area of origin. Data related to Table 1 showed great variability, and only a few samples can be compared with the ISO standard.
Zingiberene is the molecule that is responsible for the distinctive flavor and aroma of ginger. It is a sesquiterpene hydrocarbon, and it belongs to the mevalonate pathway [38]. It has been investigated for its biological properties showing antibacterial, antifungal, and antioxidant activities [39], and there are some preliminary results on its potential as a cytotoxic agent against some cancer cell lines [40]. Currently, there are very few data concerning its potential against fungal pathogens belonging to the genus Fusarium. Geranial and neral, often in a ratio of 2:1, represent a mixture of two double-bond monoterpen isomers that comprise citral. According to the scientific literature [38], geranial belongs to the methyl-erithrytol pathway, and this occurs by the oxidation of geraniol. The isolated molecule and the mixture (citral) have been widely studied because they are commonly used as fragrance, food additive, and flavor ingredients and have been associated with potential allergenic reactions [41]. Additionally, several investigations revealed their potential as anticonvulsants [42], estrogen modulators [43], and anti-adhesion and antibiofilm compounds [44]. Finally, ar-curcumene is also a sesquiterpene hydrocarbon that participates in the typical ginger “bouquet” and has been investigated for its antibacterial properties [32,45], apoptotic effects on SiHa cells [46], and its larvicidal and oviposition deterrence activity [47]. Therefore, our findings revealed a lack of studies relating to the activity of the above-mentioned compounds against Fusarium spp., even though they are widely present in many essential oils.
Table 1. Antifungal activity of Z. officinale essential oil against Fusarium spp.
Table 1. Antifungal activity of Z. officinale essential oil against Fusarium spp.
CountryExtraction Method/Distillation Time (h)Main CompoundsMIC/% Inhibition Rate/Zone InhibitionAssayFusarium SpeciesPositive ControlNegative ControlRefs.
BrazilHD/2α-Zingiberene (22.94%), α-citral (13.58%), geranial (10.39%)>2000 μg/mL Broth dilution methodF. graminearumn.r.Fungal inoculum with no essential oil[1]
BrazilHD/2α-zingiberene (23.85%), geranial (14.16%), (E,E)-a-farnesene (9.98%)2500 μg/mL Broth dilution methodF. verticillioidesn.r.Fungal inoculum with no essential oil[5]
CameroonHD/n.r.n.r.500 ppmAgar dilution techniqueF. moniliformen.r.Fungal inoculum with no essential oil[48]
Chinan.r.α-Zingiberene (31.47%), Beta-sesquiphellandrene (13.76%), alfa-curcumene (10.41%)61.4%
(280 μL)
Puncture inoculation methodF. oxysporumn.r.Fungal inoculum with no essential oil[49]
EgyptHD/3β-sesquiphellandrene (27.16%), caryophyllene (15.29%), zingiberene (13.97%)75 μg/mLBroth dilution methodF. oxysporumAmphotericin BFungal inoculum with no essential oil [50]
IndiaHD/n.r.Geranial (25.9%), α-Zingiberene (9.5%), (E,E)-alpha-farnesene (7.6%)100%
6 μL)
Inverted Petri plate technique/Poison food techniqueF. moniliformen.r.Water[51]
IndiaHD/6α-Zingiberene (28.62%), camphene (9.32%), ar-curcumene (9.09%)62.5% (10 μL)
87.5% (10 μL)
75.0% (10 μL)
Poison food techniqueF. graminearum
F. oxysporum
F. moniliforme
n.r.Medium without EO [52]
42.8% (10 μL)
50.0% (10 μL)
85.7% (10 μL)
Inverted Petri plate techniqueF. graminearum
F. oxysporum
F. moniliforme
IndiaHD/61,8-cineol (27.0%)79.5%
(20% oil concentration)
Poison food TechniqueF. oxysporumn.r.Medium without essential oil[53]
IndiaHD/3n.r.
(Z. officinale EO and combination of EO
Z. officinale + C. longa)
100%
(2.5 μL/mL)
Broth dilution methodF. oxysporum, F. nivalen.r.Medium without essential oil[54]
MexicoHD/4Eudesmol (8.19%), γ-terpinene (7.88%), α-curcumene (7.28%)FC50
(0.10 mg/mL)
Inhibition of radial growthF. moniliformeKetoconazole (60 μg)Olive oil
(4 μL)
[55]
NigeriaHD/5α-Zingiberene (18.6%), Geranial (13.9%), Neral (10.7%)100%
(5 μL/mL)
Poison food techniqueF. oxysporum60 μL/mL of Azoxystrobin/
Difenoconazole
Medium without essential oil[39]
RomaniaHD/n.r.n.r.F. oxysporum (DL50 = 1139 μL/L, DL80 = 1822 μL/L, DL90 = 2050, and DL95 = 2164 μL/L) Agar dilution methodF. oxysporumn.r.Medium without essential oil[56]
F. graminearum (DL50 = 1199 μL/L, DL80 = 1919 μL/L, DL90 = 2158, and DL95 = 2278 μL/L)F. graminearum
ThainlandHD/24Camphene, 1,8-cineol, and α-pinene10.0 mg/LMinimum inhibition concentrationF. oxysporumn.r.n.r.[57]
n.r.—not reported. HD—hydro-distillation.

3.3. Z. officinale EO Antifungal Activity

F. oxysporum has been the most investigated species, but some preliminary results are also available for F. graminearum and F. moniliforme. Data concerning antifungal activity may be strongly influenced by assay methods, and there is wide variability in the expression of the results. Indeed, MIC values for broth dilution methods ranged from 75 to 2500 μg/mL. In addition, several studies that applied the food poison technique showed a range of inhibition zones from 62.5% to 100% using EO concentrations between 5% and 10%. The antibacterial activity of EOs has been correlated to the destabilization of the cellular architecture, mainly due to the breakdown of the membrane. Membrane rupture is linked to the leakage of cellular components that involve the inhibition of membrane transport and energy production [58]. Due to the lipophilic nature and the small size of EO molecules, EOs are able to penetrate lipid barriers; this changes the permeability of the cell membrane, and the main effect is the outflow of ions and cellular constituents [59]. A study performed by the authors of [60] against Aspergillus flavus reported an MIC of 0.6 μL/mL. The authors proposed as a possible antifungal mechanism the depolarization of the mitochondrial membrane and the interference of the EO with carbohydrate catabolism. Additionally, there are few studies regarding the antifungal activities of Z. officinale EO (Figure 3a–c); some preliminary results have been reported on fluconazole-susceptible and fluconazole-resistant Candida albicans strains, showing an MIC of 2500 μg/mL [61].
There are several reports on the antifungal activities of Z. officinale against different fungal species. The minimum inhibitory concentration (MIC, μg/mL) and the minimum fungicidal concentration (MFC, μg/mL) of EO of Z. officinale were found to be 1898 ± 33.41, 2621 ± 37.72 for Aspergillus ochraceus and 1255 ± 18.30, 1442 ± 37.81 for Penicillium verrucosum, respectively [62]. Comparatively, in the same investigation, it was found that the EOs of Z. officinale showed less antifungal activity than the EOs of Cinnamomum zeylanicum and Cymbopogon martini, but similar levels of antifungal activity to Curcuma longa and Ocimum basilicum. Even though the results were not consistent, increasing concentrations of ginger EO (0.5–5 × 103 μg/mL) decreased ergosterol production from 200–350 μg/mL to ~5 μg/mL in Fusarium verticillioides [5]. The antifungal activity of ginger EOs is highly species-dependent; certain fungal species are highly sensitive and some species are less sensitive to the EOs of ginger. The LC50 values (μL/mL) of ginger EOs against different fungal phytopathogens are as follows: Fusarium oxysporum (1.3), Colletotrichum falcatum (1.5), Ganoderma boninense (2.5), Pyricularia oryzae (2.8), Rigidoporus microporus (3.5), Xanthomonas oryzae pv. oryzae strain A (300), and Ralstonia solanacearum (400) [39]. Surprisingly, the rhizosphere microbiome of Z. officinale has also shown antifungal activity, which implies an indirect antifungal role for ginger plants. For instance, Bacillus vietnamensis, isolated from the rhizosphere of Z. officinale, was shown to inhibit Pythium myriotylum, which is a causative agent of Pythium rot in ginger [63]. Thus, the above insights clearly suggest that Z. officinale and its EO have antifungal properties that could be useful in the control of potential fungal phytopathogens.
Ultimately, even if all research confirms that Z. officinale EO displays promising antifungal activity against Fusarium species, additional studies are needed in order to investigate the above-mentioned results in the context of pre- and post-harvest activities.

3.4. Effect of Z. officinale EO on Ergosterol Production Anti-Mycotoxigenic Activity

Ergosterol determination by HPLC-UV is a widespread analytical technique used in order to quantify antifungal activity in food. Ergosterol is an indicator of fungal contamination due to its natural role as a specific constituent of mycelium cell membranes, and for this reason, ergosterol can be used as a biological marker. Moreover, ergosterol has been used as an easily detectable and accurate indicator of potential mycotoxin presence in foods [64]. The main roles of ergosterol in yeast cells are related to structural and hormonal functions, which are crucial in order to maintain and regulate the physiological development of cell membranes in microorganisms. The mode of action of some synthetic and natural antifungal agents may be explained as the inhibition of cell growth by elective interference with ergosterol biosynthesis [39].
As reported in Table 2, Z. officinale EO also seems to be able to inhibit the production of deoxynivalenol (DON) (Figure 4), a low-molecular-weight trichothecenes belonging to a group of sesquiterpenoids produced by Fusarium spp. [65]. This mycotoxin is quite widespread in crops such as corn, wheat, barley, and potatoes; it is responsible for gastrointestinal inflammation, emesis, and diarrhea in animals. In addition, humans can be affected by DON and may show similar symptoms, but chronic effects as carcinogenic, teratogenic, and immune-suppressive diseases have also been reported as the principal danger. Indeed, the World Health Organization and the Food and Agriculture Organization have recognized DON as a very critical food contaminant [66,67]. As reported by Ferreira et al. (2018) [1], significant to total inhibition of DON production may be achieved by levels of Z. officinale EO ranging between 500 and 2000 μg/mL, respectively.
Research performed by Cai et al. (2021) [59] reported preliminary results concerning the effectiveness of EOs and herbal extracts in the reduction in mycotoxins, including AFB1, AFB2, AFG1, AFG2, DON, FB1, and OTA. Despite the fact that the degradation mechanism of mycotoxins by EOs and their components has not been clearly elucidated, this field of research deserves additional investigation. Moreover, as reported in [68] by Mirza Alizadeh et al. (2021), EOs are able to inhibit mycotoxin synthesis due to their interference with metabolic pathways and gene expression patterns in fungi.

4. Discussion

As reflected in the above-mentioned research, Z. officinale EO may be suggested as a potential plant-based treatment for Fusarium infections even if further investigations are needed. EOs are gaining more attention as promising plant-based biocontrol agents in food crop protection due to their synergic potential as anti-phytopathogenic, weed, and pest control treatments. Several studies revealed these findings in the previous decade, but the development and application of commercial products based on EOs or their components are still a long way off [7,69,70].
The application of EOs in crop protection presents advantages due to their wide-spectrum activities, their low toxicity, their lower persistence in soils and groundwater, and the reasonably low risk for non-target species, such as mammals and aquatic organisms [69,71].
Additionally, EOs are a good candidate for organic management strategies [72,73] due to the existence of several certified organic brands.
On the other hand, disadvantages have been pointed out concerning the use of EOs in crop protection, such as limited effectiveness, the need for frequent and higher application rates compared to conventional pesticides, high costs for authorization and regulatory processes, and decreased impact due to biodegradability in the field [69].
EO activity may be enhanced by nanotechnology. As reported by Kutawa et al. (2021) [74] and Adamu et al. (2021) [75], encapsulation and nanotechnology approaches seem to be able to enhance the antifungal and antibacterial activities of Z. officinale EOs in different crops. Abdullahi et al. (2020) [39] reported the potential application of Z. officinale EO in the control of tropical plant diseases, focusing on the idea that nanoemulsion may be able to improve its efficiency and bioavailability by allowing the controlled release of the EO in order to obtain a more stable and soluble biopesticide prototype. The same authors reiterated that foliar spray and irrigation techniques may enhance the activity of encapsulated EOs.
Moreover, in order to reduce Fusarium infections and mycotoxin contaminations, EOs may be proposed as an alternative approach to conventional fungicides, also taking into account some findings that highlighted the utility of appropriate crop rotation [76], pretreatment with salicylic acid [77], and the use of biological control agents, such as Clonostachys rosea [78] and lactic acid bacteria [79]; these methods have shown promising results against infection and mycotoxin spread. Finally, a research study performed by Madege et al. (2018) [80] determined that insecticide treatment is able to reduce Fusarium symptoms in maize, possibly due to an easier diffusion of Fusarium infection where significant insect damage is present. All of these findings, though they represent preliminary results, suggest the need for a synergistic approach to crop protection, and further investigations may reveal a new fungicide treatment or enable a reduction in conventional/synthetic fungicides.
Finally, Zingiber officinale represents one of the major spice crops produced in several Asian countries, such as China, India, Nepal, and Thailand, with an estimation of 1.683 thousand tons per year [81]. These data may be crucial in order to develop a commercial biofungicide and to plan adequate EO production, because a large quantity of rhizomes and organized crop production may encourage the industrial scale-up process.
With this vision, Z. officinale EO could play a role in a new pivot for how anti-Fusarium control is handled.

5. Conclusions

The present review article investigated some promising preliminary findings concerning the anti-Fusarium potential of Z. officinale EO. Z. officinale EO deserves a wider in-depth analysis in order to complete these discoveries, propose alternative research trends, and enable potential industrial developments. New research approaches should be adopted for the purpose of completing a general understanding of Z. officinale EO with respect to its anti-Fusarium activity and promoting innovative crop-protection strategies. In particular, further studies should be encouraged regarding (1) emerging nanotechnology formulations that may enhance EO activity (nanoemulsion, nanoparticles, etc.); (2) additional research about anti-mycotoxigenic activity; (3) synergistic anti-Fusarium activity with conventional biocontrol agents; (4) synergistic anti-Fusarium activity with other certified-organic compounds in order to investigate alternative organic management strategies; (5) investigations that relate phytochemistry with bioactivity (e.g., bioautographic investigations); and (6) new toxicological evaluations of long-term and acute toxicity in mammals and aquatic organisms, as well as evaluations of environmental impact and biodegradability.

Author Contributions

Conceptualization, M.R. and L.S.; methodology, M.R.; validation, N.R.M.; writing—original draft preparation, L.S.; writing—review and editing, L.S.; supervision, M.R. and N.R.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

This research was supported by the Universidad Estatal Amazónica, Departamento de Ciencias de la Tierra (Republic of Ecuador).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ferreira, F.M.D.; Hirooka, E.Y.; Ferreira, F.D.; Silva, M.V.; Mossini, S.A.G.; Machinski, M., Jr. Effect of zingiber officinale roscoe essential oil in fungus control and deoxynivalenol production of Fusarium graminearum schwabe in vitro. Food Addit. Contam. Part A Chem. Anal. Control. Expo. Risk Assess 2018, 35, 2168–2174. [Google Scholar] [CrossRef] [PubMed]
  2. Bokhari, F.M. Spices Mycobiota and Mycotoxins Available in Saudi Arabia and Their Abilities to Inhibit Growth of Some Toxigenic Fungi. Mycobiology 2007, 35, 47–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Athawale, V.; Paralikar, P.; Ingle, A.P.; Rai, M. Biogenically engineered nanoparticles inhibit Fusarium oxysporum causing soft-rot of ginger. IET Nanobiotechnol. 2018, 12, 1084–1089. [Google Scholar] [CrossRef] [PubMed]
  4. Sudakin, D.L. Trichothecenes in the environment: Relevance to human health. Toxicol. Lett. 2003, 143, 97–107. [Google Scholar] [CrossRef]
  5. Garcia Yamamoto-Ribeiro, M.M.; Grespan, R.; Kohiyama, C.Y.; Ferreira, F.D.; Mossini, S.A.G.; Silva, E.L.; de Abreu Filho, B.A.; Mikcha, J.M.G.; Junior, M.M. Effect of Zingiber officinale essential oil on Fusarium verticillioides and fumonisin production. Food Chem. 2013, 141, 3147–3152. [Google Scholar] [CrossRef] [Green Version]
  6. Pereira, V.; Fernandes, J.; Cunha, S. Mycotoxins in cereals and related foodstuffs: A review on occurrence and recent methods of analysis. Trends Food Sci. Technol. 2014, 36, 96–136. [Google Scholar] [CrossRef]
  7. Seepe, H.A.; Nxumalo, W.; Amoo, S.O. Natural products from medicinal plants against phytopathogenic fusarium species: Current research endeavours, challenges and prospects. Molecules 2021, 26, 6539. [Google Scholar] [CrossRef]
  8. Yasin, M.; Younis, A.; Javed, T.; Akram, A.; Ahsan, M.; Shabbir, R.; Ali, M.M.; Tahir, A.; El-Ballat, E.M.; Sheteiwy, M.S.; et al. River Tea Tree Oil: Composition, Antimicrobial and Antioxidant Activities, and Potential Applications in Agriculture. Plants 2021, 10, 2105. [Google Scholar] [CrossRef]
  9. Ramsey, J.T.; Shropshire, B.C.; Nagy, T.R.; Chambers, K.D.; Li, Y.; Korach, K.S. Essential oils and health. Yale J. Biol. Med. 2020, 93, 291–305. [Google Scholar]
  10. Zhang, N.; Yao, L. Anxiolytic Effect of Essential Oils and Their Constituents: A Review. J. Agric. Food Chem. 2019, 67, 13790–13808. [Google Scholar] [CrossRef]
  11. Sharmeen, J.; Mahomoodally, F.; Zengin, G.; Maggi, F. Essential Oils as Natural Sources of Fragrance Compounds for Cosmetics and Cosmeceuticals. Molecules 2021, 26, 666. [Google Scholar] [CrossRef] [PubMed]
  12. Durofil, A.; Radice, M.; Blanco-Salas, J.; Ruiz-Téllez, T. Piper aduncum essential oil: A promising insecticide, acaricide and antiparasitic. A review. Parasite 2021, 28, 42. [Google Scholar] [CrossRef] [PubMed]
  13. Rodriguez-Garcia, I.; Silva-Espinoza, B.; Ortega-Ramirez, L.; Leyva, J.; Siddiqui, M.W.; Valenzuela, M.R.C.; Gonzalez-Aguilar, G.; Zavala, J.F.A. Oregano Essential Oil as an Antimicrobial and Antioxidant Additive in Food Products. Crit. Rev. Food Sci. Nutr. 2015, 56, 1717–1727. [Google Scholar] [CrossRef] [PubMed]
  14. Sakkas, H.; Papadopoulou, C. Antimicrobial Activity of Basil, Oregano, and Thyme Essential Oils. J. Microbiol. Biotechnol. 2017, 27, 429–438. [Google Scholar] [CrossRef] [Green Version]
  15. Barreca, S.; La Bella, S.; Maggio, A.; Licata, M.; Buscemi, S.; Leto, C.; Pace, A.; Tuttolomondo, T. Flavouring Extra-Virgin Olive Oil with Aromatic and Medicinal Plants Essential Oils Stabilizes Oleic Acid Composition during Photo-Oxidative Stress. Agriculture 2021, 11, 266. [Google Scholar] [CrossRef]
  16. Ben Hsouna, A.; Ben Halima, N.; Smaoui, S.; Hamdi, N. Citrus lemon essential oil: Chemical composition, antioxidant and antimicrobial activities with its preservative effect against Listeria monocytogenes inoculated in minced beef meat. Lipids Heal. Dis. 2017, 16, 146. [Google Scholar] [CrossRef] [Green Version]
  17. Zhang, Y.; Li, D.; Lv, J.; Li, Q.; Kong, C.; Luo, Y. Effect of cinnamon essential oil on bacterial diversity and shelf-life in vacuum-packaged common carp (Cyprinus carpio) during refrigerated storage. Int. J. Food Microbiol. 2017, 249, 1–8. [Google Scholar] [CrossRef]
  18. Yen, P.P.L.; Kitts, D.D.; Pratap Singh, A. Natural Acidification with Low-pH Fruits and Incorporation of Essential Oil Constituents for Organic Preservation of Unpasteurized Juices. J. Food Sci. 2018, 83, 2039–2046. [Google Scholar] [CrossRef]
  19. Maurya, A.; Singh, V.K.; Das, S.; Prasad, J.; Kedia, A.; Upadhyay, N.; Dubey, N.K.; Dwivedy, A.K. Essential Oil Nanoemulsion as Eco-Friendly and Safe Preservative: Bioefficacy Against Microbial Food Deterioration and Toxin Secretion, Mode of Action, and Future Opportunities. Front. Microbiol. 2021, 12, 751062. [Google Scholar] [CrossRef]
  20. Kong, I.; Degraeve, P.; Pui, L.P. Polysaccharide-Based Edible Films Incorporated with Essential Oil Nanoemulsions: Physico-Chemical, Mechanical Properties and Its Application in Food Preservation—A Review. Foods 2022, 11, 555. [Google Scholar] [CrossRef]
  21. Sadgrove, N.; Jones, G. A Contemporary Introduction to Essential Oils: Chemistry, Bioactivity and Prospects for Australian Agriculture. Agriculture 2015, 5, 48–102. [Google Scholar] [CrossRef] [Green Version]
  22. ISO 9235:2013; Aromatic Natural Raw Materials-Vocabulary. International Organization for Standardization: Geneva, Switzerland, 2013. Available online: https://www.iso.org/standard/51017.html (accessed on 22 March 2022).
  23. Zhang, L.; Xu, Q.; Zhan, D.; Zhang, H.; Xia, G.; Zhu, J.; Zang, H. Chemical Composition and Biological Activities of Essential Oil from Roots of Aralia continentalis. Chem. Nat. Compd. 2020, 56, 548–550. [Google Scholar] [CrossRef]
  24. Liu, Y.; Liu, J.; Zhang, Y. Research Progress on Chemical Constituents of Zingiber officinale Roscoe. BioMed Res. Int. 2019, 1–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Talebi, M.; Ilgün, S.; Ebrahimi, V.; Talebi, M.; Farkhondeh, T.; Ebrahimi, H.; Samarghandian, S. Zingiber officinale ameliorates Alzheimer’s disease and Cognitive Impairments: Lessons from preclinical studies. Biomed. Pharmacother. 2021, 133, 111088. [Google Scholar] [CrossRef]
  26. Wang, J.; Ke, W.; Bao, R.; Hu, X.; Chen, F. Beneficial effects of ginger Zingiber officinale Roscoe on obesity and metabolic syndrome: A review. Ann. N. Y. Acad. Sci. 2017, 1398, 83–98. [Google Scholar] [CrossRef]
  27. Attari, V.E.; Mahdavi, A.M.; Javadivala, Z.; Mahluji, S.; Vahed, S.Z.; Ostadrahimi, A. A systematic review of the anti-obesity and weight lowering effect of ginger (Zingiber officinale Roscoe) and its mechanisms of action. Phytotherapy Res. 2017, 32, 577–585. [Google Scholar] [CrossRef]
  28. Li, C.; Li, J.; Jiang, F.; Tzvetkov, N.T.; Horbanczuk, J.O.; Li, Y.; Atanasov, A.G.; Wang, D. Vasculoprotective effects of ginger (Zingiber officinale Roscoe) and underlying molecular mechanisms. Food Funct. 2021, 12, 1897–1913. [Google Scholar] [CrossRef]
  29. Mao, Q.-Q.; Xu, X.-Y.; Cao, S.-Y.; Gan, R.-Y.; Corke, H.; Beta, T.; Li, H.-B. Bioactive Compounds and Bioactivities of Ginger (Zingiber officinale Roscoe). Foods 2019, 8, 185. [Google Scholar] [CrossRef] [Green Version]
  30. Raafat, M.; El-Sayed, A.S.A.; El-Sayed, M.T. Biosynthesis and anti-mycotoxigenic activity of Zingiber officinale roscoe-derived metal nanoparticles. Molecules 2021, 26, 2290. [Google Scholar] [CrossRef]
  31. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The prisma 2020 statement: An updated guideline for reporting systematic reviews. Med. Flum. 2021, 57, 444–465. [Google Scholar] [CrossRef]
  32. Sharifi-Rad, M.; Varoni, E.M.; Salehi, B.; Sharifi-Rad, J.; Matthews, K.R.; Ayatollahi, S.A.; Kobarfard, F.; Ibrahim, S.A.; Mnayer, D.; Zakaria, Z.A.; et al. Plants of the genus Zingiber as a source of bioactive phytochemicals: From tradition to pharmacy. Molecules 2017, 22, 2145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Jayasundara, N.D.B.; Arampath, P. Effect of variety, location & maturity stage at harvesting, on essential oil chemical composition, and weight yield of Zingiber officinale roscoe grown in Sri Lanka. Heliyon 2021, 7, e06560. [Google Scholar] [PubMed]
  34. Höferl, M.; Stoilova, I.; Wanner, J.; Schmidt, E.; Jirovetz, L.; Trifonova, D.; Stanchev, V.; Krastanov, A. Composition and Comprehensive Antioxidant Activity of Ginger (Zingiber officinale) Essential Oil from Ecuador. Nat. Prod. Commun. 2015, 10, 1085–1090. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Sasidharan, I.; Venugopal, V.; Menon, A.N. Essential oil composition of two unique ginger (Zingiber officinale Roscoe) cultivars from Sikkim. Nat. Prod. Res. 2012, 26, 1759–1764. [Google Scholar] [CrossRef]
  36. Martins, A.; Salgueiro, L.; Gonçalves, M.; Cunha, A.; Vila, R.; Cañigueral, S.; Mazzoni, V.; Tomi, F.; Casanova, J. Essential Oil Composition and Antimicrobial Activity of Three Zingiberaceae from S.Tomé e Príncipe. Planta Medica 2001, 67, 580–584. [Google Scholar] [CrossRef]
  37. ISO 16928:2014; Essential Oil of Ginger [Zingiber officinale Roscoe]. International Organization for Standardization: Geneva, Switzerland, 2014. Available online: https://www.iso.org/standard/57978.html (accessed on 22 March 2022).
  38. Baser, K.H.C.; Buchbauer, G. Handbook of Essential Oils: Science, Technology and Applications; CRC Press: Boca Raton, FL, USA, 2016. [Google Scholar]
  39. Abdullahi, A.; Khairulmazmi, A.; Yasmeen, S.; Ismail, I.; Norhayu, A.; Sulaiman, M.; Ahmed, O.; Ismail, M. Phytochemical profiling and antimicrobial activity of ginger (Zingiber officinale) essential oils against important phytopathogens. Arab. J. Chem. 2020, 13, 8012–8025. [Google Scholar] [CrossRef]
  40. Mahomoodally, M.F.; Aumeeruddy, M.; Rengasamy, K.R.; Roshan, S.; Hammad, S.; Pandohee, J.; Hu, X.; Zengin, G. Ginger and its active compounds in cancer therapy: From folk uses to nano-therapeutic applications. Semin. Cancer Biol. 2021, 69, 140–149. [Google Scholar] [CrossRef]
  41. Hagvall, L.; Bruze, M.; Engfeldt, M.; Isaksson, M.; Lindberg, M.; Ryberg, K.; Stenberg, B.; Svedman, C.; Karlberg, A.; Christensson, J.B.; et al. Contact allergy to citral and its constituents geranial and neral, coupled with reactions to the prehapten and prohapten geraniol. Contact Dermat. 2019, 82, 31–38. [Google Scholar] [CrossRef]
  42. Bahr, T.A.; Rodriguez, D.; Beaumont, C.; Allred, K. The Effects of Various Essential Oils on Epilepsy and Acute Seizure: A Systematic Review. Evid. Based Complement. Altern. Med. 2019, 2019, 6216745. [Google Scholar] [CrossRef] [Green Version]
  43. Kiyama, R. Nutritional implications of ginger: Chemistry, biological activities and signaling pathways. J. Nutr. Biochem. 2020, 86, 108486. [Google Scholar] [CrossRef]
  44. Galiè, S.; García-Gutiérrez, C.; Miguélez, E.M.; Villar, C.J.; Lombó, F. Biofilms in the Food Industry: Health Aspects and Control Methods. Front. Microbiol. 2018, 9, 898. [Google Scholar] [CrossRef] [PubMed]
  45. Wang, X.; Shen, Y.; Thakur, K.; Han, J.; Zhang, J.-G.; Hu, F.; Wei, Z.-J. Antibacterial Activity and Mechanism of Ginger Essential Oil against Escherichia coli and Staphylococcus aureus. Molecules 2020, 25, 3955. [Google Scholar] [CrossRef] [PubMed]
  46. Shin, Y.; Lee, Y. Cytotoxic Activity from Curcuma zedoaria Through Mitochondrial Activation on Ovarian Cancer Cells. Toxicol. Res. 2013, 29, 257–261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. AlShebly, M.M.; AlQahtani, F.S.; Govindarajan, M.; Gopinath, K.; Vijayan, P.; Benelli, G. Toxicity of ar-curcumene and epi-β-bisabolol from Hedychium larsenii (Zingiberaceae) essential oil on malaria, chikungunya and Japanese encephalitis mosquito vectors. Ecotoxicol. Environ. Saf. 2017, 137, 149–157. [Google Scholar] [CrossRef]
  48. Nguefack, J.; Leth, V.; Zollo, P.A.; Mathur, S. Evaluation of five essential oils from aromatic plants of Cameroon for controlling food spoilage and mycotoxin producing fungi. Int. J. Food Microbiol. 2004, 94, 329–334. [Google Scholar] [CrossRef]
  49. Deleanu, M.; Popa, E.E.; Popa, M.E. Chemical Composition and Active Properties Evaluation of Wild Oregano (Origanum Vulgare) and Ginger (Zingiber Officinale-Roscoe) Essential Oils. Rev. Chim. 2018, 69, 1927–1933. [Google Scholar] [CrossRef]
  50. El-Baroty, G.S.; Abd El-Baky, H.H.; Farag, R.S.; Saleh, M.A. Characterization of antioxidant and antimicrobial compounds of cinnamon and ginger essential oils. Afr. J. Biochem. Res. 2010, 4, 167–174. [Google Scholar]
  51. Singh, G.; Kapoor, I.; Singh, P.; de Heluani, C.S.; de Lampasona, M.P.; Catalan, C.A. Chemistry, antioxidant and antimicrobial investigations on essential oil and oleoresins of Zingiber officinale. Food Chem. Toxicol. 2008, 46, 3295–3302. [Google Scholar] [CrossRef]
  52. Singh, G.; Maurya, S.; Catalan, C.; de Lampasona, M.P. Studies on essential oils, Part 42: Chemical, antifungal, antioxidant and sprout suppressant studies on ginger essential oil and its oleoresin. Flavour Fragr. J. 2004, 20, 1–6. [Google Scholar] [CrossRef]
  53. Mir, S.A.; Qureshi, A.H. Antifungal activity of oil against plant pathogenic fungi isolated Zingiber officinale from solanaceous vegetable fruits. Asian J. Pharm. Pharmacol. 2017, 3, 121–124. [Google Scholar]
  54. Prakash, B.; Singh, P.; Kedia, A.; Singh, A.; Dubey, N.K. Efficacy of essential oil combination of curcuma longa l. and zingiber officinale rosc. As a postharvest fungitoxicant, aflatoxin inhibitor and antioxidant agent. J. Food Saf. 2012, 32, 279–288. [Google Scholar] [CrossRef]
  55. López, E.I.C.; Balcázar, M.F.H.; Mendoza, J.M.R.; Ortiz, A.D.R.; Melo, M.T.O.; Parrales, R.S.; Delgado, T.H.; de Farmacognosia, L. Antimicrobial Activity of Essential Oil of Zingiber officinale Roscoe (Zingiberaceae). Am. J. Plant Sci. 2017, 8, 1511–1524. [Google Scholar]
  56. Radu, N.; Voicescu, M.; Radu, E.; Tanasescu, C. Zingiber officinale based bioproduct. Properties and influence on some cellulolytic and keratinolytic fungi. Mol. Cryst. Liq. Cryst. 2017, 655, 103–113. [Google Scholar] [CrossRef]
  57. Sa-Nguanpuag, K.; Kanlayanarat, S.; Srilaong, V.; Tanprasert, K.; Techavuthiporn, C. Ginger (Zingiber officinale) oil as an antimicrobial agent for minimally processed produce: A case study in shredded green papaya. Int. J. Agric. Biol. 2011, 13, 895–901. [Google Scholar]
  58. Tariq, S.; Wani, S.; Rasool, W.; Shafi, K.; Bhat, M.A.; Prabhakar, A.; Shalla, A.H.; Rather, M.A. A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microb. Pathog. 2019, 134, 103580. [Google Scholar] [CrossRef]
  59. Cai, J.; Yan, R.; Shi, J.; Chen, J.; Long, M.; Wu, W.; Kuca, K. Antifungal and mycotoxin detoxification ability of essential oils: A review. Phytotherapy Res. 2021, 36, 62–72. [Google Scholar] [CrossRef]
  60. Singh, P.P.; Jaiswal, A.K.; Kumar, A.; Gupta, V.; Prakash, B. Untangling the multi-regime molecular mechanism of verbenol-chemotype Zingiber officinale essential oil against Aspergillus flavus and aflatoxin B1. Sci. Rep. 2021, 11, 6832. [Google Scholar] [CrossRef]
  61. Sharifzadeh, A.; Shokri, H. Antifungal activity of essential oils from Iranian plants against fluconazole-resistant and fluconazole-susceptible Candida albicans. Avicenna J. Phytomed. 2016, 6, 215–222. [Google Scholar]
  62. Kalagatur, N.K.; Gurunathan, S.; Kamasani, J.R.; Gunti, L.; Kadirvelu, K.; Mohan, C.D.; Rangappa, S.; Prasad, R.; Almeida, F.; Mudili, V.; et al. Inhibitory effect of C. zeylanicum, C. longa, O. basilicum, Z. officinale, and C. martini essential oils on growth and ochratoxin A content of A. ochraceous and P. verrucosum in maize grains. Biotechnol. Rep. 2020, 27, e00490. [Google Scholar] [CrossRef]
  63. John, J.C.; Ge, M.; Noushad, N. Probiotic rhizospheric Bacillus sp. from Zingiber officinale Rosc. displays antifungal activity against soft rot pathogen Pythium sp. Curr. Plant Biol. 2021, 27, 100217. [Google Scholar] [CrossRef]
  64. Kadakal, Ç.; Nizamoğlu, N.M.; Tepe, T.K.; Arısoy, S.; Tepe, B.; Batu, S. Relation between Ergosterol and Various Mycotoxins in Different Cheeses. Turk. J. Agric.-Food Sci. Technol. 2020, 8, 895–900. [Google Scholar] [CrossRef] [Green Version]
  65. Pinto, A.C.S.M.; De Pierri, C.R.; Evangelista, A.G.; Gomes, A.S.d.L.P.B.; Luciano, F.B. Deoxynivalenol: Toxicology, Degradation by Bacteria, and Phylogenetic Analysis. Toxins 2022, 14, 90. [Google Scholar] [CrossRef] [PubMed]
  66. FAO & WHO. Conference on Food Additive and Contaminants Agenda Item; FAO & WHO: Rome, Italy, 1973. [Google Scholar]
  67. Yao, Y.; Long, M. The biological detoxification of deoxynivalenol: A review. Food Chem. Toxicol. 2020, 145, 111649. [Google Scholar] [CrossRef] [PubMed]
  68. Alizadeh, A.M.; Golzan, S.A.; Mahdavi, A.; Dakhili, S.; Torki, Z.; Hosseini, H. Recent advances on the efficacy of essential oils on mycotoxin secretion and their mode of action. Crit. Rev. Food Sci. Nutr. 2021, 2021, 1–26. [Google Scholar] [CrossRef]
  69. Alonso-Gato, M.; Astray, G.; Mejuto, J.; Simal-Gandara, J. Essential Oils as Antimicrobials in Crop Protection. Antibiotics 2021, 10, 34. [Google Scholar] [CrossRef] [PubMed]
  70. Raveau, R.; Fontaine, J.; Sahraoui, A.L.-H. Essential Oils as Potential Alternative Biocontrol Products against Plant Pathogens and Weeds: A Review. Foods 2020, 9, 365. [Google Scholar] [CrossRef] [Green Version]
  71. Conti, B.; Flamini, G.; Cioni, P.L.; Ceccarini, L.; Macchia, M.; Benelli, G. Mosquitocidal essential oils: Are they safe against non-target aquatic organisms? Parasitol. Res. 2014, 113, 251–259. [Google Scholar] [CrossRef]
  72. Chang, Y.; Harmon, P.F.; Treadwell, D.D.; Carrillo, D.; Sarkhosh, A.; Brecht, J.K. Biocontrol Potential of Essential Oils in Organic Horticulture Systems: From Farm to Fork. Front. Nutr. 2022, 8, 1–26. [Google Scholar] [CrossRef]
  73. Gullickson, M.; Hodge, C.F.; Hegeman, A.; Rogers, M. Deterrent Effects of Essential Oils on Spotted-Wing Drosophila (Drosophila suzukii): Implications for Organic Management in Berry Crops. Insects 2020, 11, 536. [Google Scholar] [CrossRef]
  74. Kutawa, A.B.; Ahmad, K.; Ali, A.; Hussein, M.Z.; Wahab, M.A.A.; Adamu, A.; Ismaila, A.A.; Gunasena, M.T.; Rahman, M.Z.; Hossain, I. Trends in Nanotechnology and Its Potentialities to Control Plant Pathogenic Fungi: A Review. Biology 2021, 10, 881. [Google Scholar] [CrossRef]
  75. Adamu, A.; Ahmad, K.; Siddiqui, Y.; Ismail, I.S.; Asib, N.; Bashir Kutawa, A.; Adzmi, F.; Ismail, M.R.; Berahim, Z. Ginger Essential Oils-Loaded Nanoemulsions: Potential Strategy to Manage Bacterial Leaf Blight Disease and Enhanced Rice Yield. Molecules 2021, 26, 3902. [Google Scholar] [CrossRef] [PubMed]
  76. Qiu, J.; Dong, F.; Yu, M.; Xu, J.; Shi, J. Effect of preceding crop on Fusarium species and mycotoxin contamination of wheat grains. J. Sci. Food Agric. 2016, 96, 4536–4541. [Google Scholar] [CrossRef] [PubMed]
  77. Bawa, G.; Feng, L.; Yan, L.; Du, Y.; Shang, J.; Sun, X.; Wang, X.; Yu, L.; Liu, C.; Yang, W.; et al. Pre-treatment of salicylic acid enhances resistance of soybean seedlings to Fusarium solani. Plant Mol. Biol. 2019, 101, 315–323. [Google Scholar] [CrossRef]
  78. Gimeno, A.; Kägi, A.; Drakopoulos, D.; Bänziger, I.; Lehmann, E.; Forrer, H.; Keller, B.; Vogelgsang, S. From laboratory to the field: Biological control of Fusarium graminearum on infected maize crop residues. J. Appl. Microbiol. 2020, 129, 680–694. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Oliveira, P.M.; Zannini, E.; Arendt, E.K. Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: From crop farming to cereal products. Food Microbiol. 2014, 37, 78–95. [Google Scholar] [CrossRef] [PubMed]
  80. Madege, R.R.; Audenaert, K.; Kimanya, M.; Tiisekwa, B.; De Meulenaer, B.; Bekaert, B.; Landschoot, S.; Haesaert, G. Control of Fusarium verticillioides (Sacc.) Nirenberg and Fumonisins by Using a Combination of Crop Protection Products and Fertilization. Toxins 2018, 10, 67. [Google Scholar] [CrossRef] [Green Version]
  81. APEDA Agri Exchange. Ginger. 2014. Available online: http://apeda.in/agriexchange/Market%20Profile/one/GINGER.aspx#:~:text=The%20total%20production%20of%20ginger,and%20172.68%20thousand%20tons%20respectively (accessed on 22 March 2022).
Figure 1. Root of Zingiber officinale Roscoe.
Figure 1. Root of Zingiber officinale Roscoe.
Agronomy 12 01168 g001
Figure 2. Flowchart showing the methodology and selection process used in the present review.
Figure 2. Flowchart showing the methodology and selection process used in the present review.
Agronomy 12 01168 g002
Figure 3. Microbiological effects of EOs of Z. officinale. (a) Effect of Z. officinale EO on growth (top) and ochratoxin A (OTA) production (bottom) in fungi in maize grains [62]; (b) effectiveness; and (c) inhibitory effect of Z. officinale EOs on the growth of F. oxysporum [39].
Figure 3. Microbiological effects of EOs of Z. officinale. (a) Effect of Z. officinale EO on growth (top) and ochratoxin A (OTA) production (bottom) in fungi in maize grains [62]; (b) effectiveness; and (c) inhibitory effect of Z. officinale EOs on the growth of F. oxysporum [39].
Agronomy 12 01168 g003
Figure 4. Relationship between Z. officinale EO and mycotoxin deoxynivalenol (DON) synthesis [1].
Figure 4. Relationship between Z. officinale EO and mycotoxin deoxynivalenol (DON) synthesis [1].
Agronomy 12 01168 g004
Table 2. Ergosterol quantification and anti-mycotoxigenic activity of several Z. officinale EOs.
Table 2. Ergosterol quantification and anti-mycotoxigenic activity of several Z. officinale EOs.
CountryEffects of EO upon Ergosterol Production (Determined by HPLC)Anti-Mycotoxigenic ActivityFusarium SpeciesPositive ControlNegative ControlRefs.
BrazilConcentrations higher than 1000 μg/mL of EO caused significant inhibitionSignificant reduction in DON levels by 47.3% (p < 0.05) at a concentration of 500 μg/mL
Total inhibition: 2000 μg/mL
F. graminearumn.r.Fungal inoculum with no essential oil[1]
BrazilConcentrations ranging from 4000 to 5000 μg/mL caused inhibition ranging from 57% to 100%Significant inhibition of FB1 production (p < 0.05) at a concentration of 4000 μg/mL and complete inhibition at 5000 μg/mL
Significant inhibition of FB2 production at 2000 μg/mL and complete inhibition at 3000 μg/mL
F. verticillioidesSuspension of 4 × 105 CFU/mL (F. verticillioides)n.r.[5]
n.r.—not reported.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Radice, M.; Maddela, N.R.; Scalvenzi, L. Biological Activities of Zingiber officinale Roscoe Essential Oil against Fusarium spp.: A Minireview of a Promising Tool for Biocontrol. Agronomy 2022, 12, 1168. https://doi.org/10.3390/agronomy12051168

AMA Style

Radice M, Maddela NR, Scalvenzi L. Biological Activities of Zingiber officinale Roscoe Essential Oil against Fusarium spp.: A Minireview of a Promising Tool for Biocontrol. Agronomy. 2022; 12(5):1168. https://doi.org/10.3390/agronomy12051168

Chicago/Turabian Style

Radice, Matteo, Naga Raju Maddela, and Laura Scalvenzi. 2022. "Biological Activities of Zingiber officinale Roscoe Essential Oil against Fusarium spp.: A Minireview of a Promising Tool for Biocontrol" Agronomy 12, no. 5: 1168. https://doi.org/10.3390/agronomy12051168

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop