Biological Control of Citrus Postharvest Phytopathogens
Abstract
:1. Introduction
2. Alternative Control Methods
2.1. Microrganisms
2.2. Natural Products
2.3. Commercial Biofungicides
3. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Antagonist | Agent | Mechanism | Target Pathogen | References |
---|---|---|---|---|
Yeast | Wickerhamomyces anomalus (or Pichia anomala) | Antibiosis, competition for nutrients, fruit resistance induction and ‘killer’ activity | P. digitatum P. italicum | [39,40,41,52] |
Saccharomyces cerevisiae | Competition for nutrients or space and ‘killer’ activity | P. digitatum P. italicum | [40,41,43,44] | |
Candida oleophila | Resistance induction. Increase phenylalanine ammonia lyase activity and accumulation of the phytoalexins such as scoparone, scopoletin, and umbelliferone | P. digitatum P. italicum | [33,53] | |
Saccharomycopsis crataegensis + sodium bicarbonate | Not specified | P. digitatum | [54] | |
Kluyveromyces marxianus + sodium bicarbonate | Competition for nutrient and space. The salt stimulates K. marxianus growth and it inhibits fungal spore germination | P. digitatum | [55] | |
Rhodosporidium paludigenum | Fruit resistance induction. Increase in ethylene production and expression of defensive genes | P. digitatum | [56] | |
Pichia membranifaciens | Competition for nutrients or space | P. digitatum | [57] | |
Metschnikowia pulcherrima, and Aureobasidium pullulans | Competition for nutrients and fruit resistance induction by influencing peroxidase and superoxide dismutase activities | P. digitatum P. italicum | [52] | |
Candida stellimalicola | ‘Killer’ activity, production of chitinase, and inhibition of conidial germination | P. italicum | [44] | |
Cryptococcus laurentii associated with cinnamic acid | Different influence of cinnamic acid on the antagonistic yeast and the pathogen, leading to synergistic effect | P. italicum | [58] | |
Metschnikowia citriensis | Biofilm formation, adhesion to mycelia, and iron depletion | P. digitatum P. italicum | [53] | |
Pseudozyma antarctica | Direct parasitism | P. digitatum P. italicum | [53] | |
Rhodotorula minuta, Candida azyma, and Aureobasidium pullulans | ‘Killer’ activity and hydrolytic enzyme production | G. citri-aurantii | [11] | |
Debaryomyces hansenii | Competition for space and nutrients | P. digitatum P. italicum | [32,59,60] | |
Kazachstania exígua and Pichia fermentans | ‘Killer’ activity | P. digitatum P. italicum | [41] | |
Bacillus subtilis | Water soluble antibiotics, proteins, enzymes, and VOC production | P. digitatum | [43,45] | |
Bacteria | Bacillus amyloliquefaciens | Great amounts of antibiotics produced in vitro, however, still not effective for green mold control in vivo | P. digitatum | [46] |
Lactobacillus plantarum | Metabolites 3-phenyllactic acid and benzeneacetic acid, 2-propenyl ester with antifungal activity | P. digitatum | [47,48] | |
Streptomyces sp. | Metabolites with higher mass than 2000 and fungicidal effect | P. digitatum G. citri-aurantii | [49,50] | |
Streptomyces violascens | Extracellular antifungal compounds that inhibits fungal spore germination and antibiosis | G. citri-aurantii | [61] |
Plant/Fruit | Pathogen (s) | Extract/Method | Natural Products | Details | References |
---|---|---|---|---|---|
Chinese propolis | P. italicum | 1) Ethyl acetate (3 times); 2) chloroform; 3) ethanol and water; 4) methanol | Pinocembrin | Pinocembrin acts against P. italicum through inhibition on respiration and interference of energy homeostasis | [72] |
Citrus aurantium | P. digitatum P. italicum | Hydrodistillation (peels, leaves, and flowers) | α-terpineol, terpinen-4-ol, linalool, and limonene | Essential oils (EOs) of flowers and leaves reduced the growth of pathogen, while EO of peels was inactive | [73] |
Citrus eticulate Blanco | P. digitatum | - | Citral | Antifungal activity of citral was tested in vitro and in vivo and combined with the wax showed potential for control applications | [68] |
Citrus fruits | P. italicum P. digitatum | Commercial product | Octanal | Octanal inhibits the fungal mycelial growth | [74] |
Citrus fruits | P. italicum | Commercial product | Citral | Citral inhibits the mycelial growth of P. italicum causing disruption of cell membrane integrity | [75] |
Citrus paradise Macf. (Grapefruit fruit) | P. digitatum | - | Chitosan and salicylic acid | Chitosan combined with salicylic acid had better treatment of green mold than these isolated compounds, without compromising the quality of fruit. | [26] |
Citrus sinensis Osbeck | P. digitatum | Commercial product | Citronellal | Citronellal was able to inhibit spores germination and mycelial growth. Just as citral, the compound combined with wax reduced the incidence rate | [69] |
Laminaceae spp. | P. digitatum P. italicum | - | Carvacrol and thymol | The mechanisms that have been proposed for these compounds are: 1) morphological deformation and deterioration of the conidia and hyphae; 2) hydroxyl group and systems with delocalized electrons has important role for antimicrobial effect | [69] |
Peganum harmala L. (harmal seeds) | P. italicum | Ethanol | Harmine, harmaline, and tetrahydroharmine (THH) | Harmal extracts showed strong antifungal activity against P. italicum and its activity is related to alkaloids harmine, harmaline e THH | [76] |
Peganum harmala L. | P. digitatum | Commercial product | Harmol, harmaline, harmalol, harmane, and norharmane | It was tested the antifungal activity of β-carbolines against P. digitatum and Botrytis cinerea. Harmol showed highest antifungal activity after 24 h. | [63] |
Pimpinella anisum and Carum carvi | P. digitatum | Hydrodistillation (seeds) | trans-anethole, estragole (anise oil), cuminaldehyde, and perillaldehyde (black caraway) | EO were able in vitro of reduce the germination, the mycelial growth of pathogen and the incidence of disease symptoms | [77] |
Populus × euramericana cv. ‘Neva’ (poplar buds) | P. italicum | Dichloromethane | Flavonoids of pinocembrin, chrysin, and galangin | Antifungal compounds from poplar buds active fraction, identified by HPLC–MS, had antifungal effect in the fungal hyphae analyzed by scanning electron microscopy and transmission electron microscopy images | [78] |
Punica Granatum | P. digitatum | Ethanol/water (4:1) | Phenolic compounds with a prevalence of punicalagins | Pomegranate peel extract has a broad range of antifungal activity | [13] |
Ramulus cinnamomi | P. digitatum P. italicum G. citri-aurantii | Ethyl acetate and n-buthanol | Cinnamic acid and cinnamaldehyde | Through 1H-NMR-based metabolomics it was identified the extracts related to antifungal activity of Ramulus cinnamomi after 4, 8, and 12 h. The antifungal mechanism of cinnamaldehyde it was also analyzed by 1H-NMR | [79] |
Rosmarinus officinalis L. | P. digitatum | Hydrodistillation (for EO) and methanol | Flavonoids, polyphenols, and essential oils | EO act in the fungal cells by disrupting the membrane permeability and the osmotic balance | [80] |
Salvia fruticosa Mill. | P. digitatum | Ethyl acetate | Carnosic acid, carnosol, and hispidulin | Compounds that have antifungal properties, according to its compositions, structures/activity, and literature | [81] |
Sapium baccatum | P. digitatum | Commercial product | Tannic acid | In vitro antifungal activity to P. digitatum was verified between 400 and 1000 µg mL−1 of tannic acid inoculated in Ponkan fruit was sufficient to inhibit the mycelial growth of 45% to 100% | [82] |
Solanum nigrum | P. digitatum | Aqueous extract (leaves) | Alkaloids, flavonoids, saponins, steroids, glycosides, terpenoids, and tannins | Bioactive compounds that has pharmacological prospects for development of drugs | [83] |
Thymus species (T. leptobotris, T. riatarum, T. broussonnetii subsp. hannonis, and T. satureioides subsp. pseudomastichina) | P. digitatum P. italicum G. citri-aurantii | Hydrodistillation | Thymol, carvacrol, geraniol, eugenol, octanal, and citral | EO of four Thymus species showed antifungal activity. Through GC–MS, MIC, and previous studies determined the principal active compounds | [84] |
Thymus leptobotris | P. digitatum P. italicum G. citri-aurantii | Methanol, chloroform | Thymol and carvacrol | The antifungal screening from EO obtained from 21 plants showed that the EO from Thymus leptobotris had the highest fungistatic effect. The active compounds were identified in previous studies. | [85] |
Thymus vulgaris L. | P. italicum P. digitatum | - | Thymol | EO of thyme inhibited the mycelium growth (MIC 0.13 µL mL−1) and spore germination (MIC 0.50 µL mL−1) in vitro and in vivo | [86] |
Withania somnifera + Acacia seyal | P. digitatum | Methanol/acetone/water—7:7:1, v/v (dried plant powder—1:20 w/v) | Insoluble and soluble phenolic compounds | Application of plants extract (W. somnifera and A. seyal) in the sick host, induced plant resistance through change of phenolic concentration (phenylpropanoid pathway) | [87] |
Microorganism | Product | Targeted Pathogens | References |
---|---|---|---|
Candida oleophila | Aspire | Botrytis, Penicillium | [117] |
Metschnikowia fructicola | Shemer | Botrytis, Penicillium, Rhizopus, Aspergillus | [124] |
Pantoea agglomerans | Pantovital | Penicillium, Botrytis, Monilinia | [125] |
Pseudomonas syringae | Biosave | Penicillium, Botrytis, Mucor | [126] |
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Moraes Bazioli, J.; Belinato, J.R.; Costa, J.H.; Akiyama, D.Y.; Pontes, J.G.d.M.; Kupper, K.C.; Augusto, F.; de Carvalho, J.E.; Fill, T.P. Biological Control of Citrus Postharvest Phytopathogens. Toxins 2019, 11, 460. https://doi.org/10.3390/toxins11080460
Moraes Bazioli J, Belinato JR, Costa JH, Akiyama DY, Pontes JGdM, Kupper KC, Augusto F, de Carvalho JE, Fill TP. Biological Control of Citrus Postharvest Phytopathogens. Toxins. 2019; 11(8):460. https://doi.org/10.3390/toxins11080460
Chicago/Turabian StyleMoraes Bazioli, Jaqueline, João Raul Belinato, Jonas Henrique Costa, Daniel Yuri Akiyama, João Guilherme de Moraes Pontes, Katia Cristina Kupper, Fabio Augusto, João Ernesto de Carvalho, and Taícia Pacheco Fill. 2019. "Biological Control of Citrus Postharvest Phytopathogens" Toxins 11, no. 8: 460. https://doi.org/10.3390/toxins11080460