Exploring the metabolic intersection of juglone and phylloquinone biosynthesis

Abstract

Juglone is a 1,4-naphthoquinone (1,4-NQ) and the allelochemical responsible for the well-known toxic effects of black walnut (Juglans nigra) and other members of the Juglandaceae. Juglone affects a variety of weed species via a mode of action unlike any commercially available herbicides, and thus has the potential to be used as a new natural product-based herbicide. However, lack of knowledge about its metabolism precludes introducing juglone biosynthesis traits into resistant crops through biotechnology. Herein, we established that juglone is derived from the phylloquinone pathway at the level of the intermediate 1,4-dihydroxy-2-naphthoic acid (DHNA). Phylloquinone is a primary 1,4-NQ made by all plants for photosynthetic electron transport. Despite the fundamental importance of phylloquinone, there are still unanswered questions about the subcellular architecture of the phylloquinone pathway. In chapter 3, we show that o-succinylbenzoate CoA-ligase is localized to both chloroplasts and peroxisomes and that its activity is vital in both organelles. The required dual localization of CoA ligase activity is a theme common to other plant pathways with CoA metabolic steps occurring in peroxisomes and thus leads us to propose a revised model of the phylloquinone pathway. Lastly, given the potential of introducing juglone biosynthesis as part of novel weed management strategies, we investigated the circumstances, costs, and benefits of producing allelochemicals in crops using an evolutionary game theory model. Together, this work (i) shows that the phylloquinone pathway provides crops with the biosynthetic framework to produce juglone, (ii) sheds new light on the phylloquinone pathway architecture, and (iii) reveals the circumstances in which producing an allelochemical will be an evolutionarily stable strategy. We envision these results will assist biotechnological efforts to utilize juglone as a novel, natural product-based herbicide.