Abstract

Naphthoquinones are secondary metabolites widely distributed in nature and produced by bacteria, fungi and higher plants. Their biological activity may result from induction of oxidative stress, caused by redox cycling or direct interaction with cellular macromolecules, in which quinones act as electrophiles. The redox homeostasis is known as one of factors involved in auxin-mediated plant growth regulation. To date, however, little is known about the crosstalk between reactive oxygen species (ROS) produced by quinones and the plant growth hormone auxin (IAA). In this study, redox cycling properties of two naphthoquinones, juglone (5-hydroxy-1,4-naphthoquinone) and lawsone (2-hydroxy-1,4-naphthoquinone), were compared in experiments performed on maize coleoptile segments incubated with or without the addition of IAA. It was found that lawsone was much more effective than juglone in increasing both H2O2 production and the activity of antioxidative enzymes (SOD, POX and CAT) in coleoptile cells, regardless of the presence of IAA. An increase in the activity of Cu/Zn-SOD isoenzymes induced by both naphthoquinones suggests that juglone- and lawsone-generated H2O2 was primarily produced in the cytosolic and cell wall spaces. The cell potential to neutralize hydrogen peroxide, determined by POX and CAT activity, pointed to activity of catalase as the main enzymatic mechanism responsible for degradation of H2O2 Therefore, we assumed that generation of H2O2, induced more efficiently by LW than JG, was the major factor accounting for differences in the toxicity of naphthoquinones in maize coleoptiles. The role of auxin in the process appeared negligible. Moreover, the results suggested that oxidative stress imposed by JG and LW was one of mechanisms of allelopathic action of the studied quinones in plants.

Highlights

  • Juglone (JG) (5-hydroxy-1,4-naphthoquinone) and lawsone (LW) (2-hydroxy-1,4-naphthoquinone) are naturally occurring naphthoquinones that are widespread in nature

  • The application of either juglone or lawsone after 2 h of the pre-incubation of a segment in the control medium resulted in an increase in H2O2 production, which was significantly higher in the presence of lawsone (F10,42 1⁄4 115, P 1⁄4 0.0023) than in juglone (F10,44 1⁄4 67, P 1⁄4 0.0021), regardless of the time of incubation [see Supporting Information—Table S1] (F12,44 1⁄4 3.496, P 1⁄4 0.03 and F12,44 1⁄4 5.928, P 1⁄4 0.008, respectively)

  • We found that LW was a more effective oxidative stress inducer in maize coleoptile segments than JG

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Summary

Introduction

Juglone (JG) (5-hydroxy-1,4-naphthoquinone) and lawsone (LW) (2-hydroxy-1,4-naphthoquinone) are naturally occurring naphthoquinones that are widespread in nature. They have been identified as secondary metabolites that can be isolated from the leaves, roots, husks and bark of plants of the Juglandaceae family, black walnut (Juglans nigra) in case of JG, and from. Kurtyka et al.—Naphthoquinone-induced oxidative stress in maize the leaves of the henna plant (Lawsonia inermis) and water hyacinth (Eichhornia crassipes) in case of LW (Solar et al 2006; Babula et al 2009; Ashnagar and Shiri 2011; Nour et al 2013). JG and LW display a related chemical structure (Kumagai et al 2012), knowledge about the effects of LW in plants is limited and the main area of LW research has been its interaction with animal and human tissues (O€llinger and Brunmark 1991; Kumbhar et al 1996; Dasgupta et al 2003)

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