Convergent evolution of plant specialized 1,4-naphthoquinones: metabolism, trafficking, and resistance to their allelopathic effects

Meyer, George W.; Naranjo, Maria A Bahamon; Widhalm, Joshua R.

doi:10.1093/jxb/eraa462

Cited by 22 publications

(26 citation statements)

References 78 publications

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“…One way of reducing the cost of producing novel allelochemicals,

, is to harness existing metabolic frameworks. Many species producing naphthoquinone‐based compounds, for example, have independently evolved to do so from 1,4‐dihydroxy‐2‐naphthoic acid (DHNA), an intermediate of the phylloquinone (vitamin K 1 ) pathway (Meyer et al, 2020 ; Widhalm & Rhodes, 2016 ). Examples include juglone in black walnut trees (McCoy et al, 2018 ), lawsone and 2‐MNQ in the Balsaminaceae (e.g., Impatiens species) (Zenk & Leistner, 1967 ), lawsone and lapachol in the Bignoniaceae (Hussain et al, 2007 ), anthraquinones like alizarin made by Rubiaceae species (Yamazaki et al, 2013 ), and anthrasesamones produced by sesame ( Sesamum indicum , Pedaliaceae) (Furumoto & Hoshikuma, 2011 ).…”

Section: Discussionmentioning

confidence: 99%

“…Heterologous overexpression AmGSTF1 in Arabidopsis thaliana was shown to be sufficient to confer resistance to multiple herbicides (Cummins et al, 2013 ). Moreover, Arabidopsis seedlings grown in vitro in the presence of GSH in juglone‐containing media were found to display root growth phenotypes indistinguishable from wild type (Meyer et al, 2020 ). Beyond conjugation with GSH, glycosylation appears to be a major mechanism of detoxification of specialized metabolites (le Roy et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

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Allelopathy as an evolutionary game

2022

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In plants, most competition is resource competition, where one plant simply preempts the resources away from its neighbors. Interference competition, as the name implies, is a form of direct interference to prevent resource access. Interference competition is common among animals that can physically fight, but in plants, one of the main mechanisms of interference competition is allelopathy. Allelopathic plants release cytotoxic chemicals into the environment which can increase their ability to compete with surrounding organisms for limited resources. The circumstances and conditions favoring the development and maintenance of allelochemicals, however, are not well understood. Particularly, despite the obvious benefits of allelopathy, current data suggest it seems to have only rarely evolved. To gain insight into the cost and benefit of allelopathy, we have developed a 2 2 matrix game to model the interaction between plants that produce allelochemicals and plants that do not. Production of an allelochemical introduces novel cost associated with both synthesis and detoxifying a toxic chemical but may also convey a competitive advantage. A plant that does not produce an allelochemical will suffer the cost of encountering one. Our model predicts three cases in which the evolutionarily stable strategies are different. In the first, the nonallelopathic plant is a stronger competitor, and not producing allelochemicals is the evolutionarily stable strategy. In the second, the allelopathic plant is the better competitor, and production of allelochemicals is the more beneficial strategy. In the last case, neither is the evolutionarily stable strategy. Instead, there are alternating stable states, depending on whether the allelopathic or nonallelopathic plant arrived first. The generated model reveals circumstances leading to the evolution of allelochemicals and sheds light on utilizing allelochemicals as part of weed management strategies. In particular, the wide region of alternative stable states in most parameterizations, combined with the fact that the absence of allelopathy is likely the ancestral state, provides an elegant answer to the question of why allelopathy seems to rarely evolve despite its obvious benefits. Allelopathic plants can indeed outcompete nonallelopathic plants, but this benefit is simply not great enough to allow them to go to fixation and spread through the population. Thus, most populations would remain purely nonallelopathic.

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“…One way of reducing the cost of producing novel allelochemicals,

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Allelopathy as an evolutionary game

2022

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“…One way of reducing the cost of producing novel allelochemicals, C , is to harness existing metabolic frameworks. Many species producing naphthoquinone-based compounds, for example, have independently evolved to do so from 1,4-dihydroxy-2-naphthoic acid (DHNA), an intermediate of the phylloquinone (vitamin K1) pathway 32,33 . Examples include juglone in black walnut trees 34 , lawsone and 2-MNQ in the Balsaminaceae (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Heterologous overexpression AmGSTF1 in Arabidopsis thaliana was shown to be sufficient to confer resistance to multiple herbicides 46 . Moreover, Arabidopsis seedlings grown in vitro in the presence of GSH in juglone-containing media were found to display root growth phenotypes indistinguishable from wild type (Meyer et al 2020). Beyond conjugation with GSH, glycosylation appears to be a major mechanism of detoxification of specialized metabolites 47 .…”

Section: Discussionmentioning

confidence: 99%

Allelopathy as an evolutionarily stable strategy

McCoy

Widhalm

McNickle

2021

Preprint

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In plants, most competition is resource competition, where one plant simply pre-empts the resources away from its neighbours. Interference competition, as the name implies, is a form of direct interference to prevent resource access. Interference competition is common among animals who can physically fight, but in plants, one of the main mechanisms of interference competition is Allelopathy. allelopathic plants release of cytotoxic chemicals into the environment which can increase their ability to compete with surrounding organisms for limited resources. The circumstances and conditions favoring the development and maintenance of allelochemicals, however, is not well understood. Particularly, it seems strange that, despite the obvious benefits of allelopathy, it seems to have only rarely evolved. To gain insight into the cost and benefit of allelopathy, we have developed a 2x2 matrix game to model the interaction between plants that produce allelochemicals and plants that do not. Production of an allelochemical introduces novel cost associated with synthesis and detoxifying a toxic chemical but may also convey a competitive advantage. A plant that does not produce an allelochemical will suffer the cost of encountering one. Our model predicts three cases in which the evolutionarily stable strategies are different. In the first, the non-allelopathic plant is a stronger competitor, and not producing allelochemicals is the evolutionarily stable strategy. In the second, the allelopathic plant is the better competitor and production of allelochemicals is the more beneficial strategy. In the last case, neither is the evolutionarily stable strategy. Instead, there are alternating stable states, depending on whether the allelopathic or non-allelopathic plant arrived first. The generated model reveals circumstances leading to the evolution of allelochemicals and sheds light on utilizing allelochemicals as part of weed management strategies. In particular, the wide region of alternative stable states in most parameterizations, combined with the fact that the absence of allelopathy is likely the ancestral state, provides an elegant answer to the question of why allelopathy rarely evolves despite its obvious benefits. Allelopathic plants can indeed outcompete non-allelopathic plants, but this benefit is simply not great enough to allow them to go to fixation and spread through the population. Thus, most populations would remain purely non-allelopathic.

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“…Researchers have been widely concerned about walnut blight (Meyer et al, 2021;Motmainna et al, 2021). However, with the extraction and isolation of different walnut parts, the allelopathic effects of juglone have been widely reported and gradually developed into green pesticides (Soderquist 1973;Rietveld 1983;Rietveld et al, 1983).…”

Section: Juglone As a Natural Pesticidementioning

confidence: 99%

Resource efficiency and environmental impact of juglone in Pericarpium Juglandis: A review

Liu

Cheng

Jia

et al. 2022

Front. Environ. Sci.

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Black walnut (Juglans nigra) is considered one of the most valuable plants, with a global production of 3.5 million tons of dried fruit yearly. Throughout the past two millennia, its allelopathic effects have been widely recognized. Black walnuts produce a natural naphthoquinone called juglone, which occurs naturally in all parts of the tree, particularly the green husk, and contributes significantly to the allelopathic effects of black walnut. Except for the fruit’s edible nature, the walnut green husk (Pericarpium Juglandis) has been used for centuries to make wine, natural dyes, and traditional medicines to cure certain diseases. Within the extracts of walnut green husk, 1,4-naphthoquinones, gallic acid, caffeic acid, and quercitrin were separated and characterized. Among these compounds, the major active ingredient with a good application prospect is juglone, which has proven to be a natural chemical compound with anticancer, antitumor, antibacterial, and antiviral activities, especially the strong anticancer activity. Juglone is also an environmentally friendly biological pesticide and herbicide. Certainly, the environmental impact of juglone also needs to be considered. Significant quantities of walnut green husk are currently produced as a byproduct of walnut production; however, its value has not been fully utilized and explored, which raises environmental concerns. This review attempts to: 1) summarize the origin and historical use of walnut and walnut green husk; 2) introduce the structure, biosynthesis pathway, extraction method, biological activity, and potential applications of juglone, as well as its environmental impact assessment.

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Convergent evolution of plant specialized 1,4-naphthoquinones: metabolism, trafficking, and resistance to their allelopathic effects

Cited by 22 publications

References 78 publications

Allelopathy as an evolutionary game

Allelopathy as an evolutionary game

Allelopathy as an evolutionarily stable strategy

Resource efficiency and environmental impact of juglone in Pericarpium Juglandis: A review

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