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Agricultural Uses of Juglone: Opportunities and Challenges

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Agricultural Uses of Juglone: Opportunities and Challenges agronomy Review Agricultural Uses of Juglone: Opportunities and Challenges A. K. M. Mominul Islam 1,2,* and Joshua R. Widhalm 1,3,* 1 Department of Horticulture and Landscape Architecture, Purdue University, 625 Agriculture Mall Dr, West Lafayette, IN 47907, USA 2 Department of Agronomy, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh 3 Purdue Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA * Correspondence: [email protected] (A.K.M.M.I.); [email protected] (J.R.W.); Tel.: +1-765-496-3891 (J.R.W.) Received: 4 September 2020; Accepted: 28 September 2020; Published: 1 October 2020 Abstract: Application of conventional synthetic pesticides and agrochemicals has boosted the yield and productivity of crops by reducing pest infestation and promoting crop growth yet increasing reliance on many of these products poses serious environmental threats. This has led to growing interest in obtaining more environmentally friendly alternatives to conventional pesticides and agrochemicals. Allelochemicals produced by plants, fungi, and microbes offer options for developing novel natural product-based pesticides and agrochemicals that are effective but with lower environmental half-lives. Here, we review the current state of knowledge about the potential use of juglone (5-hydroxy-1,4-naphthoquinone), the allelochemical produced by black walnut trees (Juglans nigra), which has been investigated for applications across a range of different agricultural purposes. We then offer our perspective on what opportunities and challenges exist for harnessing juglone as a component of sustainable agriculture. Keywords: allelochemical; agrochemical; biostimulant; Juglans; juglone; natural product; pesticide; sustainable agriculture; urease inhibitor 1. Introduction Juglone, 5-hydroxy-1,4-napthoquinone (Figure1), is a quinoid compound that functions as an allelochemical when released from trees in the walnut family (Juglandaceae) into the rhizosphere. Juglone has been isolated from several Juglandaceae members, including Juglans nigra L. (black walnut), J. regia L. (English walnut), J. cinerea L., J. ailantifolia Carr., J. mandshurica Maxim., Carya tomentosa Nutt., C. ovata (Mill.) K. Koch, C. illinoensis (Wangenh.) K. Koch (pecan), Ptero-carya fraxinifolia (Lam.) Spach, and Platycarya strobilacea Siebold & Zucc. [1,2]. Juglone is excreted from roots and exuded from litterfall in its reduced form, hydrojuglone [3–6]. Hydrojuglone is colorless, nontoxic, and is abundant in leaves, roots, husks, and bark [7]. Upon release, hydrojuglone is oxidized in air to its toxic form, juglone [8–10]. Juglone taken up by sensitive plants has general inhibitory effects on growth and development [4]. Moreover, juglone is the bioactive compound in certain plant parts used in traditional medicines for treating ailments including allergies, gastrointestinal abnormalities, cancer, and different fungal, bacterial, and viral infections [9]. Due to its general toxicity, juglone itself is unlikely to ever become a clinically significant drug. However, efforts are ongoing to synthesize juglone analogs with enhanced bioavailability, lower toxicity, and improved selectivity [11]. Agronomy 2020, 10, 1500; doi:10.3390/agronomy10101500 www.mdpi.com/journal/agronomy Agronomy 2020, 10, 1500 2 of 19 Agronomy 2020, 10, x FOR PEER REVIEW 1 of 19 Figure 1. TheFigure chemical 1. The chemical structure structure of of juglone juglone (5-hydroxy-1,4-naphthoquinone). (5-hydroxy-1,4-naphthoquinone). The allelopathic effects of black walnut on neighboring plants have been reported for centuries The allelopathicand remain eaff concernects of for black home walnut gardeners on today neighboring [8,12–14]. Plinius plants Secundus have (Pliny been the reported Elder) is for centuries and remaincredited a concern with being for the home first to gardeners report the phytotoxic today effects [8,12 of– 14black]. walnut. Plinius It was Secundus not until the (Pliny1850s, the Elder) however, that juglone, previously known as nucin, was first isolated [15]. By 1887, juglone could be is credited withsynthesized being [16], the and first in 1881 to the report first scientific the phytotoxic article related etoff itsects allelopathy of black was published walnut. [17]. It In was not until the 1850s, however,1928, juglone that was determined juglone, to previously be the compound known responsible as nucin, for the phytotoxicity was first of isolated walnut trees [15 ]. By 1887, juglone could[18]. be Today, synthesized natural products [16], and like in juglone 1881 theare firsttouted scientific as promising article alternatives related to to synthetic its allelopathy was agrochemicals due to their reported pesticidal properties and other biochemical activities of published [17agricultural]. In 1928, interest. juglone Perhaps was most determined notably, juglone to beexhibits the compoundinhibitory effects responsible on several weed for species the phytotoxicity of walnut trees[19], [as18 characterized]. Today, naturalby effects productslike leaf wilting like and juglone yellowing are or touted damaging as the promising roots through alternatives to synthetic agrochemicalsinduction of reactive due oxygen to their species reported (ROS) together pesticidal with calcium properties accumulation and other resulting biochemical to death activities [20,21]. Juglone is also reported as being lethal to larval development and insect flight muscle of agriculturalmitochondria, interest. to Perhaps have sedative most effects notably, on fish and juglone other animals, exhibits to have inhibitory mutagenic, e ffcarcinogenic,ects on several weed species [19], asand characterized lethal effects on animal by eff cells,ects and like to leaf have wilting repellent, and antifeedant, yellowing antimicrobial, or damaging antifungal, the and roots through induction of reactiveantiparasitic oxygen properties species [19,22– (ROS)26]. However, together toxicity with of calciumjuglone varies accumulation depending on resultingseveral factors, to death [20,21]. such as the donor plant species, quantity released and amount accumulated, soil pH, texture, and Juglone is alsoorganic reported matter ascontent being [27,28]. lethal Therefore, to larval it is worth development investigating and the use insect of juglone flight in muscleagricultural mitochondria, to have sedativeapplications effects and onto study fish the and factors other precluding animals, it from being to have implemented mutagenic, as a chemical carcinogenic, tool. In this and lethal effects on animalreview, cells, we provide and to an haveoverview repellent, of the current antifeedant, state of knowledge antimicrobial, on juglone, antifungal,which encompasses and antiparasitic nearly 100 years of research and observations. We also address the challenges and prospects to properties [19harnessing,22–26]. it However, as a natural product-based toxicity of juglonepesticide and/or varies agrochemical. depending Finally, on several we identify factors, areas such as the donor plant species,where further quantity research released is needed to and implement amount juglone accumulated, across areas of soil sustainable pH, texture, agriculture. and organic matter content [27,28]. Therefore, it is worth investigating the use of juglone in agricultural applications and to 2. Prospects of Juglone as a Natural Product-Based Pesticide study the factors precluding it from being implemented as a chemical tool. In this review, we provide Since the dawn of agriculture, pests have posed threats to crops, fish, livestock, and non-target an overviewinsects. of the When current it comes state to food of crops, knowledge for example, on it juglone, is estimated which that over encompasses 140,000 species of nearly insects, 100 years of research andweeds, observations. nematodes, Weand microorganisms, also address including the challenges pathogenic and fungi, prospects viruses, and to bacteria harnessing contribute it as a natural product-basedto agricultural pesticide losses and [29]./or On agrochemical. average, 26–50% of Finally, crop losses we have identify been reported areas in rice, where potato, further coffee, research is maize, cotton, wheat, soybean, barley, and sugar beet [30]. In total, around one-third of the total needed to implementproduction of juglone major crops across is damaged areas ofdue sustainable to pests worldwide agriculture. [31]. More recently, the Food and Agriculture Organization (FAO) of the United Nations estimated that 19–30% of cereals, 33–60% of 2. Prospectsroots of Juglone and tubers, as and aNatural 37–55% of Product-Basedfruits and vegetables Pesticide are damaged globally by crop pests [32]. To meet the demand for the agricultural output needed to sustain an increasing global Since thepopulation, dawn of 3.5 agriculture, billion kg of active pests ingredient have posedis used in threats the form toof synthetic crops, fish,pesticides livestock, each year andby non-target insects. Whenfarmers it comes [33]. While to food pesticides crops, are for regulated example, in certain it is countries, estimated farmers that and over their 140,000environments species in of insects, developing countries are often exposed to toxic chemicals that are banned or restricted in other weeds, nematodes,countries. and This microorganisms,exposure is further exacerbated including when pathogenic inappropriate fungi, dosages, viruses, application and techniques, bacteria contribute to agriculturalequipment, losses [ 29and/or]. On storage
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