Inhibitory Potential of Naphthoquinones Leached from Leaves and Exuded from Roots of the Invasive Plant Impatiens glandulifera

Abstract

Exploring the effects of allelopathic plant chemicals on the growth of native vegetation is essential to understand their ecological roles and importance in exotic plant invasion. Naphthoquinones have been identified as potential growth inhibitors produced by Impatiens glandulifera, an exotic annual plant that recently invaded temperate forests in Europe. However, naphthoquinone release and inhibitory potential have not been examined. We quantified the naphthoquinone content in cotyledons, leaves, stems, and roots from plants of different ages of both the invasive I. glandulifera and native Impatiens noli-tangere as well as in soil extracts and rainwater rinsed from leaves of either plant species by using ultra-high pressure liquid chromatography-mass spectrometry (UHPLC-MS). We identified the compound 2-methoxy-1,4-naphthoquinone (2-MNQ) exclusively in plant organs of I. glandulifera, in resin bags buried into the soil of patches invaded by I. glandulifera, and in rainwater rinsed from its leaves. This indicates that 2-MNQ is released from the roots of I. glandulifera and leached from its leaves by rain. Specific bioassays using aqueous shoot and root extracts revealed a strong inhibitory effect on the germination of two native forest herbs and on the mycelium growth of three ectomycorrhiza fungi. These findings suggest that the release of 2-MNQ may contribute to the invasion success of I. glandulifera and support the novel weapons hypothesis.

Differential influence of four invasive plant species on soil physicochemical properties in a pot experiment

“…Similarly, soil total phenolics, N, and P did not differ between the groups of invasive forbs, including I. glandulifera, R. japonica, and S. gigantea, native forbs and native graminoids (Scharfy et al 2011). Overall, it seems that increases or no changes in soil nutrient concentrations due to the invasion of these species prevail over decreases (Güsewell et al 2005;Vanderhoeven et al 2005Vanderhoeven et al , 2006Chapuis-Lardy et al 2006;Dassonville et al 2007;Aguilera et al 2010;Mincheva et al 2014;Ruckli et al 2014a;Scharfy et al 2009Scharfy et al , 2010Scharfy et al , 2011Stefanowicz et al 2017).…”

“…The variability in the soil response to plant invasion revealed by different studies may be caused by a number of reasons, among which the most important are functional traits of invasive species and native vegetation, properties of recipient soil, season, and length of invasion history (Dassonville et al 2008;Liao et al 2008;Scharfy et al 2011;Tharayil et al 2013). Plants affect the soil environment through deposition of litter, exudation of chemical compounds via roots, or their leaching from plants by rain, as well as through nutrient uptake (Hobbie 1992;Orwin et al 2010;Haichar et al 2014;Ruckli et al 2014a). It is known that invasive plant species often produce huge amounts of biomass which differs considerably from that of native vegetation in chemical quality, for example lignin and element content, C/N and lignin/N ratios, and/or secondary metabolite concentrations (Dassonville et al 2007(Dassonville et al , 2008Tharayil et al 2013;Mincheva et al 2014).…”

“…While the tissues or litter of I. glandulifera, R. japonica, R. laciniata, and S. gigantea have been assessed in respect of element and/or secondary metabolite concentrations and some authors tried to link their tissue quality with the soil environment (Kalemba et al 2001;Dassonville et al 2008;Fan et al 2009;Aguilera et al 2010;Tharayil et al 2013;Bardon et al 2014;Ruckli et al 2014a;Stefanowicz et al 2017), much less is known on the quality of root exudates of these species or their effects on physicochemical and biological soil properties (Scharfy et al 2010;Ruckli et al 2014a). Ruckli et al (2014a) found that I. glandulifera is able to inhibit mycelium growth by naphthoquinones-phenolics released from roots or leached from leaves by rain.…”

“…Ruckli et al (2014a) found that I. glandulifera is able to inhibit mycelium growth by naphthoquinones-phenolics released from roots or leached from leaves by rain. On the other hand, 3-year growth of S. gigantea in experimental wetland plant communities influenced neither N nor P availability in soil (Scharfy et al 2010).…”

Experimental evidence for a delayed response of the above-ground vegetation and the seed bank to the invasion of an annual exotic plant in deciduous forests

“…Furthermore, invasive plants may indirectly modify abiotic habitat characteristics such as physical and chemical soil properties (e.g., soil moisture and/or soil nutrients), important factors determining the survival of seeds in the soil seed bank (Bewley & Black 1994). The exudation of allelochemical compounds released from invasive plants into the soil can also reduce the germination of native seeds (Greer, Wilson, Hickman, & Wilson 2014;Ruckli, Hesse, Glauser, Rusterholz, & Baur 2014).…”