Agricultural Uses of Juglone: Opportunities and Challenges
Abstract
:1. Introduction
2. Prospects of Juglone as a Natural Product-Based Pesticide
2.1. Insecticidal Properties
2.2. Bactericidal Properties
2.3. Fungicidal Properties
2.4. Algacidal Properties
2.5. Phytotoxic (Herbicidal) Properties
3. Juglone as a Biostimulant
4. Juglone as a Urease Inhibitor
5. Knowledge Gaps and Future Prospects
- Juglone concentration may vary with species, age of the plant, seasons, and locations. For example, de Scisciolo et al. [27], recorded up to 10-fold variation in juglone concentrations in soils under different walnut trees, while Coder [159], recorded higher juglone levels in the lower parts of the leaf crown. The concentration of juglone appears to be highest during the leaf opening period of walnut and during fruit formation, but it may vary depending on walnut species [3].
- Batch-to-batch variation and post-harvest effects on juglone content. Carnat et al. [160], found no juglone in extracted J. regia dried leaves, while Girzu et al. [161], extracted fresh leaves of the same species and determined juglone accounts for 0.5% of the fresh weight. Juglone concentration also varies across different parts of walnut trees [162], which can lead to unpredictable potencies of mulches derived from litter or unused portions of walnut industry byproducts, for example.
- The general phytotoxicity of juglone to a variety of specialty crops, like asparagus, cabbage, eggplant, pepper, potato, tomato, apple, blackberry, blueberry, pear, and tobacco limits its use in horticultural production. Nonetheless, there are a number of species that appear to be more juglone tolerant [14].
- Oxidized juglone is semi-volatile. While juglone was not detected in headspace collections from intact green husks, it could be detected in collections from blended husks [168]. Thus, while juglone may have low volatility when reduced or in aqueous solution, or be bound as a glycoside in intact tissues, free juglone in pure form or in disrupted tissues (e.g., mulches) has the potential to volatilze which could lead to off-target movement and effects on nearby insects, vertebrates, plants, and microorganisms.
- Juglone is light sensitive and begins to photodegrade within a few days [28]. Surface or foliar applications of juglone therefore may be subject to shortened environmental half-lives that reduce its efficacy.
- Investigating the biostimulatory (hormetic) and inhibitory activity of juglone on different crops and weeds at various stages of growth. While most research has focused on studying the phytotoxicity of juglone (Table 1), identifying application rates leading to hormetic doses of juglone at early stages in crops may also contribute to suppressing weed growth by enhancing crop growth [130,169].
- Understanding the activity of juglone in natural field settings. Most research on juglone has been conducted under strictly controlled environmental conditions, either in laboratory or greenhouse settings [170]. The accumulation of any allelochemical, however, is heavily influenced by environmental conditions [171,172,173,174]. In the case of juglone, this further depends on the route by which juglone reaches the environment (Figure 2).
- Identifying ways to reduce production costs. The cost of chemically synthesizing a natural product, producing it through metabolic engineering in a heterologous system, or of cultivating the producing species and extracting and purifying the target compound must be economically competitive in order to become a practical substitute to conventional synthetic pesticides and agrochemicals. While efficient methods for synthesizing juglone have been reported (e.g., [175]), identifying the remaining unknown genes in juglone biosynthesis [12] should be prioritized to enable biotechnological platforms for producing juglone in engineered biological systems in the field. Moreover, juglone is synthesized in most organs of black and English walnut trees, including the husks, hulls, and leaves [23], which become waste products of the hardwood and food industries. Millions of tons of English walnut shells from walnut kernel processing are generated worldwide but generally end up as waste [176]. Thus, together with other underutilized parts of walnut trees, there is an abundance of inexpensive juglone-containing source material that could be directly used in agricultural applications or for extraction of pure juglone.
- Exploring the design of novel juglone derivatives [125] that balance alteration of lipophilicity with aqueous solubility [177] and which do not compromise Lipinski’s “Rule of 5” set for physicochemical parameters of pharmaceuticals and fitted for agrochemicals by Tice [178]. Nanoparticle encapsulation is another revolutionary technique that has been shown to increase antimicrobial activity and duration of juglone [179]. Its application in agricultural settings could help reduce off-target movement and toxicity of juglone and improve water solubility of more lipophilic juglone derivatives.
- Improving basic knowledge about juglone’s mode(s) of action and molecular target sites in insects, vertebrates, plants, and microorganisms, the molecular mechanisms involved in deploying juglone into the environment, the uptake of juglone in target organisms, and the metabolism-based mechanisms that allow juglone-producing plants and other types of juglone-tolerant organisms to counter or resist the effects of juglone.
6. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Species | Growth Effect (Solution Tested) | Parts or Processes Affected | Ref. |
---|---|---|---|
Lonicera maackii, Lespedeza cuneata, Trifolium incarnatum, Alnus glutinosa, Elaeagnus umbellata | Decreased (0.01–1 mM juglone) | Shoot elongation and dry weight accumulation | [1] |
Cucumis melo cv. Kiş Kavunu | Increased (1 mM juglone) | Elongation, fresh and dry weights, and polyphenol oxidase enzyme | [107] |
Cucumis sativus cv. Beith Alpha | Decreased (1 mM juglone) | Elongation, fresh and dry weights, and protein content of cotyledons | [103] |
Increased (1 mM juglone) | Polyphenol oxidase enzyme activity | ||
Solanum lycopersicum cv. Rio Grande, Cucumis sativus cv. Çengelköy, Lepidium sativum cv. Bandirma, Medicago sativa cv. Yerli | Decreased (1 mM juglone; 10% (w/v) J. regia leaf aqueous extract) | Seed germination and seedling growth | [104] |
Cucumis melo | Increased (1 mM juglone; 1/8 of 10% (w/v) J. regia leaf aqueous extract) | Seedling growth | |
Cucumis sativus cv. Beith Alpha | Decreased (0.01–1 mM juglone) | Germination | [108] |
Brassica rapa L. | Decreased (2% (w/v) ethyl acetate extract of J. regia rhizosphere and adjacent soil) | Seed germination, shoot and root length, peroxidase and malondialdehyde (MDA) activity | [109] |
Day-neutral Strawberry (Fragaria × ananassa L.) cultivar Fern | Decreased (1 mM juglone; 10% (w/v) J. regia leaf aqueous extract) | Fruit yield per plant, number of fruits per plant, average fruit weight, crowns per plant, number of leaves, leaf area, fresh root weight, total soluble solid, vitamin C, and acidity | [110] |
Nicotiana tabacum | Decreased (10–50 µM juglone) | Seedling growth | [111] |
Increased (10–50 µM juglone) | Reactive oxygen species and proline concentration | ||
Triticum aestivum | Decreased (J. nigra leaf aqueous extract) | Plant height and number of leaves | [105] |
Oryza sativa | Increased (J. nigra leaf aqueous extract) | ||
Zea mays and Glycine max | Decreased (10–100 µM juglone) | Root shoot dry weight and length, and H+-ATPase activity | [96] |
Zea mays and Glycine max | Decreased (100 µM juglone) | Shoot and root relative growth rates, leaf photosynthesis, transpiration, stomatal conductance, and leaf and root respiration | [112] |
Raphanus sativus, | Decreased (J. nigra leaf aqueous extract) | Germination rate radical and plumule length, and seedling dry weight | [113] |
Cucumis sativus cv. Beith Alpha, | Decreased (1 mM juglone) | Seedling elongation, fresh and dry weights, catalase and superoxide dismutase activities | [114] |
C. melo cv. Ananas | |||
C. melo cv. Kis Kavunu | Increased (1 mM juglone) | ||
Cucumis sativus cv. Beith Alpha, | Increased (1 mM juglone) | Malondialdehyde (MDA) levels | [114] |
C. melo cv. Ananas | |||
C. melo cv. Kis Kavunu | Decreased (1 mM juglone) | ||
Medicago polymorpha, | Increased (100 µM juglone) | Leaf chlorosis | [115] |
Medicago polymorpha and M. lupulina | Reduce glutathione (GSH), GSH and oxidized glutathione ratios, and antioxidant activity | ||
Purshia tridentata (Pursh.) D.C. | Decreased (100 µM juglone) | Plant growth and total protein content | [116] |
Lactuca sativa var. angustata | Decreased (180 g J. regia leaf litter per pot with 15 kg soil) | Growth and physiological processes | [117] |
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Islam, A.K.M.M.; Widhalm, J.R. Agricultural Uses of Juglone: Opportunities and Challenges. Agronomy 2020, 10, 1500. https://doi.org/10.3390/agronomy10101500
Islam AKMM, Widhalm JR. Agricultural Uses of Juglone: Opportunities and Challenges. Agronomy. 2020; 10(10):1500. https://doi.org/10.3390/agronomy10101500
Chicago/Turabian StyleIslam, A. K. M. Mominul, and Joshua R. Widhalm. 2020. "Agricultural Uses of Juglone: Opportunities and Challenges" Agronomy 10, no. 10: 1500. https://doi.org/10.3390/agronomy10101500
APA StyleIslam, A. K. M. M., & Widhalm, J. R. (2020). Agricultural Uses of Juglone: Opportunities and Challenges. Agronomy, 10(10), 1500. https://doi.org/10.3390/agronomy10101500