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Article

The Preventive and Curative Potential of Morinda citrifolia Essential Oil for Controlling Anthracnose in Cassava Plants: Fungitoxicity, Phytotoxicity and Target Site

by
Jossimara F. Damascena
1,
Luis O. Viteri
1,2,3,*,
Matheus H. P. Souza
4,
Raimundo W. Aguiar
1,
Marcos P. Camara
5,
Wellington S. Moura
1,
Eugênio E. Oliveira
1,6 and
Gil R. Santos
1,2,7,*
1
Programa de Pós-Graduação em Biotecnologia, Universidade Federal do Tocantins, Gurupi 77402-970, Brazil
2
Programa de Pós-Graduação em Ciências Florestais e Ambientais, Universidade Federal do Tocantins, Gurupi 77402-970, Brazil
3
Programa de Pós-Graduação em Biologia Animal, Universidade Federal de Viçosa, Viçosa 36570-900, Brazil
4
Curso de Engenharia Florestal, Universidade Federal do Tocantins, Gurupi 77402-970, Brazil
5
Departamento de Fitopatologia, Universidade Federal Rural de Pernambuco, Recife 52171-900, Brazil
6
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa 36570-900, Brazil
7
Programa de Pós-Graduação em Produção Vegetal, Universidade Federal do Tocantins, Gurupi 77402-970, Brazil
*
Authors to whom correspondence should be addressed.
Stresses 2024, 4(4), 663-675; https://doi.org/10.3390/stresses4040042
Submission received: 22 September 2024 / Revised: 12 October 2024 / Accepted: 14 October 2024 / Published: 17 October 2024
(This article belongs to the Collection Feature Papers in Plant and Photoautotrophic Stresses)
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Abstract

:
Controlling anthracnose in crops usually depends on synthetic chemicals, but essential oils offer a promising alternative with a potentially lower risk to human health and the environment. This study examines the use of noni (Morinda citrifolia L.) essential oil for preventive and curative control of anthracnose in cassava plants. Extracted from ripe noni fruit, the oil was tested at concentrations of 0.1, 0.5, 1.0, 1.5, 2.0, 2.5, and 5.0 µL/mL for its antifungal properties against Colletotrichum species isolated from cassava. We applied the oil both preventively and curatively, monitoring for phytotoxic effects. Phytochemical analysis revealed that the main compounds were octanoic acid (64.03%), hexanoic acid (10.16%), and butanoic acid (8.64%). The oil effectively inhibited C. chrysophillum and C. musicola at 2.0 µL/mL, while C. truncatum required 5.0 µL/mL for significant inhibition. Higher concentrations reduced disease progression but showed phytotoxicity at only 5 µL/mL. Molecular docking suggested that octanoic acid interacts with the fungi’s tyrosine-tRNA ligase enzyme, hinting at its mechanism of action. Collectively, our findings reinforce the potential of noni essential oil as an alternative agent against Colletotrichum spp. in cassava crops.

Graphical Abstract

1. Introduction

Cassava, Manihot esculenta L., is a crop of great importance to countries with an emerging economy and is the staple food for thousands of people in several countries, including Brazil [1,2]. It ranks as the sixth most important food source in Africa, Asia, Latin America, and the Caribbean [3,4,5], having major importance in tropical and subtropical regions. Under optimal conditions, cassava has a high yield; however, due to its inherent tolerance to stressful environments and its minimal care requirements, this crop is a secure food source against famine where other food crop species would fail [6,7,8].
In our hemisphere, Brazil is the largest producer of cassava and it is the third largest producer in the world [4]. Despite its importance, cassava remains under-researched, and as a result, significant losses occur due to diseases. One of the most serious diseases is cassava anthracnose caused by Colletotrichum spp., which is considered one of the most destructive leaf diseases of cassava in Brazil, particularly in the hot and humid climate [9,10,11,12]. Symptoms include irregular necrotic lesions distributed on stems, branches, fruit, and leaves, as well as the dieback of aerial parts [13,14,15]. The disease leads to progressive defoliation, damage to the apical meristem, and death of the apices [16], which adversely affect cassava yield and production.
To manage diseases in cassava, various methods are used, with twice synthetic fungicides being the most common. However, the indiscriminate use of pesticides can lead to environmental pollution that affects the soil, plants, animals, water, and food supply [17]. Additionally, it can foster the development of resistance in phytopathogens and pests [18,19]. In this context, new alternatives are being sought and the use of plant compounds has emerged as a possible alternative for controlling fungal diseases in plants. These compounds have shown promise in controlling fungal diseases [20,21,22] and have shown potential in controlling Colletotrichum spp. [23,24,25].
The essential oil of Morinda citrifolia L. is known for its richness in phenolic compounds, which have shown a potential effect in controlling phytopathogens. Barros, et al. [26] reported a 100% inhibitory effect against the pathogen Rhizoctonia solani, which causes anthracnose in soybeans, and effective control of leaf spots caused by Exserohilum turcicum and Bipolaris maydis in maize [27,28]. In another study, the efficacy of noni essential oil in the control of the pathogen Didymella bryoniae was observed in vitro, as well as in vivo, in the preventive control of gum blight disease in melon trees [29]. While there are reports on the biological activity of M. citrifolia essential oil and its antifungal effects against post-harvest anthracnose in fruits, its potential for controlling field diseases remains under-explored. Cassava, a hardy plant often cultivated by small- and medium-sized farmers with minimal inputs, faces significant challenges from anthracnose, which is currently the primary disease affecting the crop. This study aims to evaluate the effectiveness of noni essential oil in controlling cassava anthracnose under both in vitro and in vivo conditions, while also considering its potential phytotoxic effects and identifying its main target site.

2. Results

The pathogenicity test revealed that all isolates inoculated into the Água morma cassava cultivar were pathogenic. They caused necrotic lesions on the leaves within 48 h of inoculation, consistent with Koch’s postulates.

2.1. Chemical Composition of Morinda citrifolia Essential Oil

Our chromatographic analysis revealed that octanoic acid (64.03%) and hexanoic acid (10.16%) are the main compounds of M. citrifolia essential oil; both arecarboxylic acids (Table 1). Additionally, butanoic acid (8.64%), methyl octanoate (5.35%), and 4-pentyl hexanoate (4.3%), along with other minor compounds (<4%), were also identified.

2.2. In Vitro Sensitivity of Colletotrichum spp. to Morinda citrifolia Essential Oil

The mycelial growth of the three species of Colletotrichum was dependent on the applied concentrations of the noni essential oil. The growth of fungi C. chrysophilum was severely inhibited at concentrations above 1.0 µL/mL (Figure 1A), while C. musicola was affected at concentrations above 2.0 µL/mL (Figure 1B). C. truncatum was only affected with 5.0 µL/mL (Figure 1A–C), Table S1. Additionally, C. truncatum was the most susceptible in vitro when exposed to M. citrifolia essential oil.

2.3. Phytotoxity of Morinda citrifolia Essential Oil in Cassava Plants

We observed that concentrations of noni essential oil below 2.5 µL/mL did not cause phytotoxicity in cassava plants. However, a concentration of 5.0 µL/mL resulted in phytotoxicity, with initial symptoms of chlorosis on the leaves, followed by necrosis, primarily at the edges, veins, and tips (Table 2). Therefore, considering both its fungitoxicity and phytotoxicity, noni essential oil can be deemed safe for preventive and curative control of Colletotrichum chrysophilum in cassava plants.

2.4. In Vivo Control of Cassava Anthracnose

The assay results evaluating the preventive effect of M. citrifolia essential oil against anthracnose are shown in Figure 2. The results indicate that the preventive effect was concentration dependent for both the Vasourinha and Lagoão cultivars. In contrast, for the Água morma cultivar, intermediate concentrations increased the area under the progress curve of anthracnose, whereas higher concentrations reduced this effect (Figure 2A; Table S2). When the essential oil was applied as a curative method, the control of anthracnose also depended on the concentration, with a higher concentration providing better control (Figure 2B; Table S2).

2.5. Identification of the Interaction Between the Target Receptor and the Morinda citrifolia Essential Oil

The model selected through homology modeling that highlighted the identities and validation results with the corresponding Ramachandran favored QMEAN values is shown in Table 3. The octanoic acid complexed with the receptor and formed various types of interactions, as indicated by the molecular docking tests that were carried out. These tests showed an affinity energy with the protein tyrosine-tRNA ligase of the Glomerella cingulata target of −4.8 kcal/mol.
The complex formed between the octanoic acid ligand and the target receptor, tyrosine-tRNA ligase, showed a close interaction with the amino acids of the active site of the organism Glomerella cingulata (Figure 3A). This complex showed the following interactions between the amino acids of the target protein’s active site and the ligand: a conventional hydrogen bridge with GLY56 and SER215; alkyl interactions with LEU257 e LYS265; and van der Waals interactions with LEU59, PRO60, GLY214, ASP216, VAL255, PRO256, LEU258, and PHE266 (Figure 3B).

3. Discussion

We found that the fresh, ripe fruit of Morinda citrifolia can produce 3% essential oil through hydrodistillation, with five compounds accounting for 92.48% of the total. The major constituents are short-chain fatty acids, specifically octanoic acid (64.03%) and hexanoic acid (10.16%), which likely contribute to the fungitoxicity against Colletotrichum chrysophilum and C. truncatum. This is supported by the observation that octanoic acid has an affinity for the enzyme tyrosine-tRNA ligase. Although noni essential oil causes phytotoxicity in cassava plants at the highest concentration tested (5 μL/mL), lower concentrations (<2.5 μL/mL) are also effective in the preventive or curative control of Colletotrichum species without adversely affecting the cassava plants.
Our results showed that fresh, ripe Morinda citrifolia fruit produces 3% essential oil, a relatively high yield compared with the typical 1–2% found in most plants, which often limits their use [30]. Additionally, as a perennial bush that continuously bears fruit at a mean of 78 kg of fruit/plant/year [31], M. citrifolia provides a consistent source for essential oil extraction. Here we found that noni essential oil is mostly composed of octanoic, hexanoic, and butanoic acids, a finding that is consistent with previous studies identifying these compounds as the main constituents [32,33,34]. However, it is known that its composition can vary, particularly in the proportions of these compounds. For instance, Piaru et al. [35] reported that these compounds constituted only 13% of the total composition of noni essential oil from fresh, ripe fruit. This variation could affect the biological activity of the essential oil. We demonstrated that noni essential oil effectively inhibited the mycelial growth of three species of Colletotrichum, with C. chrysophilum and C. musicola being the most susceptible. The antimicrobial and fungicide activity of noni essential oil has been reported in other studies [27,32,33,34,36,37]. The susceptibility of Colletotrichum spp. to essential oils, including those from M. citrifolia, has also been documented [38,39,40,41,42]. Specifically, octanoic, hexanoic, and butanoic acids have been investigated [43,44,45]. These same compounds also showed fungicidal effects against the phytopathogen Botrytis cinerea and Fusarium oxysporum under laboratory and greenhouse conditions [46,47]. Thus, the antifungal activity against Colletotrichum spp. can be primarily attributed to these three compounds.
The bioactivities of essential oils are generally attributed to their main components, while also considering the possible synergistic effects of minority compounds [48,49]. Fatty acids with antifungal characteristics are known to naturally insert themselves into the lipid bilayer of fungal membranes and physically disrupt the membrane, resulting in increased membrane fluidity, and consequently, a generalized disorganization of the cell membrane [50]. Similarly, our results found that octanoic acid showed affinity for the tyrosine-tRNA ligase enzyme, which suggests a possible interference of this compound on the ligand of the enzyme. In other studies, the toxicity of M. citrifolia was also attributed to octanoic acid’s affinity for the tyrosine-tRNA ligase enzyme [33,34,51]. These crucial enzymes, aminoacyl-tRNA ligases or aminoacyl-tRNA, have key functions including participation in amino acid biosynthesis, cell cycle control, RNA splicing, and the export of tRNAs from the nucleus to the cytoplasm in eukaryotic cells [52]. The fungicidal and bactericidal activity of essential oils and plant extracts can be attributed to the interaction of these compounds with tyrosine-tRNA ligase [53,54,55]. Additionally, in one recent study was showed that compounds from M. citrifolia activate plants’ latent defense mechanisms and antioxidant systems such as superoxide dismutase, phenol peroxidase, and chitinase [34]. These enzymes could be responsible for preventing infestation in the plants (preventive treatment) by inducing their defenses [56,57]. Thus, this essential oil shows promise for fungal control, although the potential phytotoxic effects in plants should also be considered.
We found that noni essential oil as a preventive significantly reduces the colonization of C. chrysophilum. As a curative treatment, it also controls the expansion of fungi in the leaves of cassava plants, which was reflected in the area under the progress curve (AUPC). Although these effects are dependent on the cultivar, our results showed that the M. citrifolia essential oil did not have toxic effects in cassava plants when applied in fungitoxic concentrations (<2.5 µL/mL) to C. chrysophilum and C. musicola, making this essential oil a safe fungicidal for this crop. An interesting feature of this essential oil is that it can be used in different plants. For example, a study [28] reported similar results when applying noni essential oil to corn plants in the same concentrations. Noni essential oil has also been tested in Cucumis melo plants [29,33] and Oryza sativa plants [58]. This finding is relevant because biomolecules with phytotoxic effects interfere with normal physiologic activities in plants, reinforcing the potential of this essential oil as a preventive and curative tool.

4. Materials and Methods

4.1. Sampling, Isolation, Species Identification, and Pathogenicity

Leaf samples showing symptoms of anthracnose were collected from 20 municipalities in Pará and Tocantins states. In each municipality, five properties with cassava (Manihot esculenta) at various growth stages (ranging from six months to one year) and managed by family labor were sampled. From each property, ten leaves from the upper third of plants with typical anthracnose symptoms were collected. Fragments from the lesion margins, between necrotic and healthy tissue, were disinfected in 70% ethanol for 30 s and 1% sodium hypochlorite for 1 min. The fragments were then plated on potato dextrose agar (PDA) and incubated for five days at 25 °C with a 12-h photoperiod and 75 ± 5% relative humidity. Isolates characteristic of the genus Colletotrichum were purified and stored in cryogenic tubes with sterile distilled water [59,60]. These isolates were deposited in the fungal collection of the Laboratório de Micologia at the Universidade Federal Rural de Pernambuco. Morphological characteristics (such as colony color, spore size, and shape) were used to randomly select isolates for further identification through phylogenetic analysis. DNA was extracted following the cetyltrimethylammonium bromide (CTAB) protocol and the DNA concentration was visually estimated on a 0.8% agarose gel. The PCR amplification was performed, and sequencing was carried out following the methods described by Doyle Doyle [61] and Machado, et al. [62]. Species identification and recognition were conducted using the phylogenetic analysis techniques outlined [12].
The pathogenicity of Colletotrichum musicola, Colletotrichum truncatum, and Colletotrichum chrysophilum was tested in cassava plants. Initially, the pathogenicity assay was performed on cassava leaves (Var. Formosa) that were close to 90 days old. Fungal inoculum was produced in Petri dishes containing PDA culture medium, under a 12-h photoperiod and at 27 °C until sporulation was confirmed. The recovered conidial suspension was adjusted to 2 × 106 conidia mL−1 and sprayed on the leaves until run-off. The inoculated plants were kept in a humid chamber at 27 °C for 36 h. Then, the plants were kept in the greenhouse for 10 days, after which the evaluations were completed. Three replicates were used for each isolate, with one plant considered a replicate. The presence of typical anthracnose symptoms confirmed the pathogenicity of the isolates. The fungal pathogen was reisolated, fulfilling Koch’s postulates. After, healthy, disinfected cassava seedlings of the “Água morma” cultivar (susceptible to anthracnose) from Pará, Brazil, were planted in three-liter polyethylene pots containing sterile substrate and 10 g of commercial NPK fertilizer (5 nitrogen 25 phosphorus 15 potassium) per pot and maintained in controlled conditions (25 ± 2 °C, 65% relative humidity, 12-h photoperiod). When the plants reached 30 cm in height, they were inoculated using a hand sprayer with a spore suspension of either C. musicola, C. truncatum, or C. chrysophilum at a concentration of 1 × 106 conidia/mL [63,64]. Subsequently, the plants were transferred to the biochemical oxygen demand (BOD) chamber in humid (75 ± 5%) conditions for 48 h. After this incubation period, the first symptoms of anthracnose appeared. The fungus was reisolated on PDA medium as previously described. The cultures and structures of the pathogen were then compared to fulfill all the stages of Koch’s postulates. Each fungus was tested on five different plants, and the treatment control was sprayed with distilled water.

4.2. Noni Essential Oil Extraction

Ripe noni fruit (M. citrifolia) was harvested in the region of Gurupi, a municipality in the State of Tocantins, Brazil. The essential oil was extracted using steam distillation with a modified clevenger apparatus for 2 h [65]. The harvested fruit was washed in distilled water and cut into small cubes. In total, 200 g of fruit was placed in a 2-L round-bottom flask with 1 L of distilled water. The essential oil was collected in dark, airtight screw-capped vials, dried over anhydrous sodium sulfate, and stored at −4 °C until needed.

4.3. Gas Chromatography (GC) Analysis

The identification and quantification of the noni essential oil components were carried out using gas chromatography coupled with mass spectrometry (GC-MS). The analysis was performed on a Shimadzu GC-210 chromatograph equipped with a QP2010 Plus mass detector. The system used an RTX-5MS fused silica capillary column (30 m × 0.25 mm × 0.25 μm film thickness) under the following conditions: temperature programming from 60 to 240 °C at 3 °C/min; injector temperature set at 220 °C; helium as the carrier gas; and splitless injection with a 1 μL sample of a 1:1000 solution in hexane. The mass spectrometer operated with an impact energy of 70 eV and had an ion source and interface temperature of 200 °C [35]. The components of the noni oil were identified by comparing their mass spectra with those in the NIST and Wiley 229 library databases. Some compound identities were further confirmed by comparing their retention times with values in the NIST webbook and relevant literature [66].

4.4. In Vitro Fungitoxicity of Morinda citrifolia Essential Oil in Colletotrichum spp.

Solutions of noni essential oil (M. citrifolia) were prepared at concentrations of 0.0, 0.5, 1.0, 1.5, 2.0, 2.5, and 5.0 µL/mL, diluted in 1% Tween 80 using distilled, autoclaved water in a laminar flow chamber. After, 200 μL of each concentration was spread over the surface of the culture medium using a Drigalsky loop. A 6 mm diameter disc of BDA (batata dexrose agar) containing the mycelium and hyphae of Colletotrichum truncatum, Colletotrichum musicola, and Colletotrichum chrysophilum was then placed in the center of each Petri dish. The Petri dishes were sealed with PVC film, labeled, and incubated in a BOD incubator at 25 °C for ten days. During this period, the mycelial diameter was measured every 48 h, with five evaluations made using a digital caliper to obtain the average of two opposite measurements. Each concentration was tested in triplicate, with sterilized distilled water as the negative control and thiophanate methyl (2 µL/mL) as the positive control.

4.5. Phytotoxity of Morinda citrifolia Essential oil in Cassava Plants

Phytotoxicity was assessed in the Lagoão, Vassourinha, and Água morma cassava cultivars, with seedlings grown under greenhouse conditions. The same concentrations used for fungitoxicity testing (0.5, 1.0, 1.5, 2.0, 2.5, and 5.0 µL/mL) were applied to the plants. The control group was treated with distillate water and 1% Tween 80. After 24 h, the plants were evaluated for phytotoxic effects based on the criteria described by Freitas, et al. [67]. Phytotoxicity was classified as the following: no symptoms (0%), slight chlorosis or necrosis on the leaves (1–25%), moderate chlorosis or necrosis (26–50%), high chlorosis or necrosis (51–75%), and wilting and drying out of the plant (76–100%).

4.6. Preventive and Curative Disease Control of Noni Essential Oil

Preventive bioassays were conducted using Colletotrichum chrysophilum, the most frequent and aggressive pathogen in cassava-producing areas of Pará and Tocantins [62]. Additionally, this species was the most susceptible when exposed to the essential oil M. citrifolia during in vitro assays. Three cassava cultivars were selected (i.e., Água morma, Lagoão, and Vassourinha). Each cultivar was treated with seven concentrations of M. citrifolia essential oil (0.0, 0.5, 1.0, 1.5, 2.0, 2.5 µL/mL) that had not caused phytotoxicity in a previous assay [67]. In the preventive trials, selected leaves of the plants were sprayed with 5 mL of each essential oil concentration using a hand sprayer. Two hours later, the treated leaves were sprayed with 5 mL of a spore suspension of C. chrysophilum (1 × 106 conidia/mL) and transferred to a humid chamber for 48 h. Negative and positive controls were treated with distilled water and a 2000 ppm thiophanate methyl solution, respectively. Disease severity was evaluated over ten days, with assessments every 48 h post-inoculation. For the curative control trials, the same methodology was used, except that the cassava plants were initially inoculated with C. chrysophilum spores (1 × 106 conidia/mL) and kept in a humid chamber for 48 h. As soon as the first anthracnose symptoms appeared (after 48 h), the plants were treated with the same increasing concentrations of noni essential oil as in the preventive control. In both treatments, the area under the disease progress curve (AACPD) was determined and calculated using the expression AACPD = Σ (yi + yi+1)/(ti+1 − ti), where yi and yi+1 are the severity values observed in two consecutive evaluations and ti is the interval between evaluations [68,69].

4.7. In Silico Analysis

4.7.1. Ligand Modeling

The main compound in noni essential oil, octanoic acid, was selected for the molecular docking study. The 3D structure of the analyzed compound was constructed in its neutral form using Marvin Sketch 18.10, ChemAxon (accessed on 4 March 2023 at http://www.chemaxon.com).

4.7.2. Preparing the Molecular Target

The amino acid sequences of tyrosine-tRNA ligase from Colletotrichum teleomorph and Glomerella cingulata were obtained from the UniProt database (accessed on 4 March 2023 at http://uniprot.org). The 3D structures of these proteins were constructed using homology modeling in the Swiss Model Workspace (accessed on 4 March 2023 at https://swissmodel.expasy.org/), with model selection guided by the BLASTp tool. Models were downloaded from the Protein Data Bank (accessed on 4 March 2023 at https://www.rcsb.org/), considering quality parameters such as experimental method, resolution, R-value, and ligand complexation. To examine potential structural issues and amino acid positioning in the active site, we used the Swiss Model [70]. The generated models were validated using Ramachandran plots [71,72], which analyze the distribution of skeletal torsion angles Φ and ψ that are responsible for the stereochemical quality of the protein studied, as well as the QMEAN factor [73].

4.7.3. Molecular Docking Calculations

Targets and ligands were prepared for the molecular docking using Autodock Tools 1.5.7 (CCRB, La Jolla, CA, USA) [74], according to the methodology proposed by Souza Moura, et al. [75]. The grid size was set to 60 × 60 × 60 xyz points with grid spacing of 0.375 Å. The grid center was designated at dimensions (x, y, and z) 33.154, 23.604, and 13.890. Docking calculations were performed with AutoDock Vina (CCSB, La Jolla, CA, USA) [76], which generated nine docking positions for ligands interacting with the targets and provided affinity energy values (kcal/mol). The docking results were analyzed and visualized using PyMOL 2.0 (Schrodinger, New York, NY, USA) [77] and Discovery Studio 4.5 (Dassault Systèmes, Waltham, MA, USA) [78].

4.8. Statistics Analysis

The growth values for the three Colletotrichum species exposed to noni essential oil, as well as the area under the progress curve (AAPC) values, were analyzed using linear and non-linear regression with SigmaPlot 12.0 (Systat Software Inc, Palo Alto, CA, USA).

5. Conclusions

Our results provide new evidence supporting the fungicidal properties of M. citrifolia essential oil. Although cassava is considered to be a very hardy plant that usually adapts well to cultivation with few chemical inputs, it is not immune to fungal attacks that cause anthracnose. Fresh, ripe M. citrifolia fruit produces 3% essential oil through hydrodistillation, with five compounds, namely, octanoic, hexanoic, butanoic acid, methyl octanoate, and octanoate acetate, accounting for 91% of the total. The M. citriflora essential oil contributes to the fungitoxicity against Colletotrichum chrysophilum and C. truncatum and can be used to prevent or treat anthracnose in cassava crops, without causing unwanted effects on the plant. These characteristics make this product a tool that can be implemented in integrated pest management programs for cassava crops.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/stresses4040042/s1.

Author Contributions

Conceptualization, J.F.D., G.R.S. and R.W.A.; methodology, J.F.D., G.R.S. and R.W.A.; software, M.H.P.S., J.F.D., W.S.M. and M.P.C.; validation, G.R.S., W.S.M. and M.P.C.; formal analysis, L.O.V., M.P.C., G.R.S. and E.E.O.; investigation, J.F.D. and M.H.P.S.; resources, R.W.A., G.R.S. and M.P.C.; data curation, J.F.D., M.H.P.S., M.P.C. and W.S.M.; writing—original draft, L.O.V., G.R.S. and E.E.O.; writing—review & editing, L.O.V., G.R.S. and E.E.O.; visualization, L.O.V.; W.S.M., E.E.O. and G.R.S.; supervision, G.R.S. and R.W.A.; project administration, G.R.S. and R.W.A.; funding acquisition, G.R.S. and R.W.A. All authors have read and agreed to the published version of the manuscript.

Funding

The authors express their gratitude to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) in Brazil (Finance Code 001). Further thanks are directed to CNPq for their support (project number 408598/2023-9). Furthermore, the authors thank the Federal University of Tocantins for the availability of facilities.

Data Availability Statement

All data generated and/or analyzed during the present study are available in the manuscript, and the corresponding author has no objection to the availability of data and materials upon reasonable request.

Acknowledgments

This work was supported by the Coordination for the Improvement of Higher Education Personnel—Brazil (CAPES)—Finance Code 001, the National Council of Scientific and Technological Development (CNPq), the Tocantins State Foundation for Research Aid (FAPTO), the Federal University of Tocantins (CTC-UFT/PROPESQ), and the Minas Gerais State Foundation for Research Aid (FAPEMIG) for funding.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Mycelial growth over time of Colletotrichum chrysophilum (A), Colletotrichum musicola (B), and Colletotrichum truncatum (C) in response to varying concentrations of Morinda citrifolia essential oil.
Figure 1. Mycelial growth over time of Colletotrichum chrysophilum (A), Colletotrichum musicola (B), and Colletotrichum truncatum (C) in response to varying concentrations of Morinda citrifolia essential oil.
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Stresses 04 00042 g002
Figure 2. Area under the progress curve (AACPD) of cassava anthracnose, caused by Colletotrichum chrysophilum, using different concentrations of Morinda citrifolia essential oil in preventive (A) and curative (B) applications.
Figure 2. Area under the progress curve (AACPD) of cassava anthracnose, caused by Colletotrichum chrysophilum, using different concentrations of Morinda citrifolia essential oil in preventive (A) and curative (B) applications.
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Stresses 04 00042 g003
Figure 3. Octanoic acid (red) complexed with tyrosine-tRNA ligase (A) and a 2D map of molecular interactions with amino acids in target active sites (yellow) (B) of Glomerella cingulata.
Figure 3. Octanoic acid (red) complexed with tyrosine-tRNA ligase (A) and a 2D map of molecular interactions with amino acids in target active sites (yellow) (B) of Glomerella cingulata.
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Table 1. Composition of Morinda citrifolia essential oil obtained by chromatographic analysis (GC-MS).
Table 1. Composition of Morinda citrifolia essential oil obtained by chromatographic analysis (GC-MS).
CompoundsRetention Time (min)RI (Calculated Retention Index)%
2-Heptanone5.019270.14
Methyl hexanoate5.789441.08
Ethyl-hexanoate7.999910.50
Hexanoic acid8.68100610.16
Butanoic, 4-pentenyl ester10.3910430.19
Methyl octanoate12.7510945.35
Octanoate acetate15.8411633.58
Octanoic acid17.41119864.03
4-pentyl hexanoate18.6012254.30
Decanoic acid, methyl ester21.3912880.19
Butanoic acid26.9914208.64
Hexyl caprylate31.9315400.37
1-Octanoyl-1H-imidazole28.3014510.90
Others 0.57
Total 100
Table 2. Phytotoxicity in cassava plants when exposed to different concentrations of Morinda citrifolia essential oil.
Table 2. Phytotoxicity in cassava plants when exposed to different concentrations of Morinda citrifolia essential oil.
Treatment (µL/mL)ScaleObserved in Cassava Plants
Control (sterilized H2O + Tween 80)0No phytotoxicity
Control (sterilized H2O)0No phytotoxicity
0.50No phytotoxicity
1.00No phytotoxicity
1.50No phytotoxicity
2.00No phytotoxicity
2.50No phytotoxicity
5.075High chlorosis and necrosis
Table 3. Fungal target models used to analyze molecular docking with the key Morinda citrifolia essential oil compound.
Table 3. Fungal target models used to analyze molecular docking with the key Morinda citrifolia essential oil compound.
OrganismTarget
(Unipot Database)		IdentityModel Identity (%)Ramachandran Favored (%)Q
Medium
Glomerella cingulataTyrosine-tRNA ligase
(T0L8P8)		4OJM61.6297.460.78
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Damascena, J.F.; Viteri, L.O.; Souza, M.H.P.; Aguiar, R.W.; Camara, M.P.; Moura, W.S.; Oliveira, E.E.; Santos, G.R. The Preventive and Curative Potential of Morinda citrifolia Essential Oil for Controlling Anthracnose in Cassava Plants: Fungitoxicity, Phytotoxicity and Target Site. Stresses 2024, 4, 663-675. https://doi.org/10.3390/stresses4040042

AMA Style

Damascena JF, Viteri LO, Souza MHP, Aguiar RW, Camara MP, Moura WS, Oliveira EE, Santos GR. The Preventive and Curative Potential of Morinda citrifolia Essential Oil for Controlling Anthracnose in Cassava Plants: Fungitoxicity, Phytotoxicity and Target Site. Stresses. 2024; 4(4):663-675. https://doi.org/10.3390/stresses4040042

Chicago/Turabian Style

Damascena, Jossimara F., Luis O. Viteri, Matheus H. P. Souza, Raimundo W. Aguiar, Marcos P. Camara, Wellington S. Moura, Eugênio E. Oliveira, and Gil R. Santos. 2024. "The Preventive and Curative Potential of Morinda citrifolia Essential Oil for Controlling Anthracnose in Cassava Plants: Fungitoxicity, Phytotoxicity and Target Site" Stresses 4, no. 4: 663-675. https://doi.org/10.3390/stresses4040042

APA Style

Damascena, J. F., Viteri, L. O., Souza, M. H. P., Aguiar, R. W., Camara, M. P., Moura, W. S., Oliveira, E. E., & Santos, G. R. (2024). The Preventive and Curative Potential of Morinda citrifolia Essential Oil for Controlling Anthracnose in Cassava Plants: Fungitoxicity, Phytotoxicity and Target Site. Stresses, 4(4), 663-675. https://doi.org/10.3390/stresses4040042

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