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August 2021 Safety Update: Borage contains pyrrolizidine alkaloids (PAs), which can be harmful to the liver over time when ingested internally. Recent research <anchor>shows</anchor> that the PAs found in borage (and other PA-containing plants) can be taken up by other plants when grown in close proximity or when comfrey is used in the garden as mulch or fertilizer. In light of this, we are recommending that borage should not be interplanted with herbs or food plants in the garden that will be ingested or used as mulch or fertilizer to err on the side of caution. However, mature compost that includes borage does not seem to contain PAs once it has been fully composted according to this study.
Transfer of pyrrolizidine alkaloids between living plants: A disregarded source of contaminations - ScienceDirect
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## Environmental Pollution

# Transfer of pyrrolizidine alkaloids between living plants: A disregarded source of contaminations ☆

Author links open overlay panelDirkSelmara, CarinaWittkea, IrisBeck-von Wolffersdorffb, BernhardKlierb, LauraLewerenza, MaikKleinwächterc, MelanieNowaka

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## Highlights

- •
  Pyrrolizidine alkaloids are released from living alkaloidal plants into the soil.

- •
  The alkaloids are taken up by acceptor plants growing in the vicinity.

- •
  In the acceptor plants, the alkaloids are modified.

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  This transfer could explain the contaminations of many plant-derived commodities.

## Abstract

To elucidate the origin of the wide-spread contaminations of plant derived commodities with various alkaloids, we employed co-cultures of pyrrolizidine alkaloid (PA) containing Senecio jacobaea plants with various alkaloid free acceptor plants. Our analyses revealed that all plants grown in the vicinity of the Senecio donor plants indeed contain significant amounts of the PAs, which previously had been synthesized in the Senecio plants. These findings illustrate that typical secondary metabolites, such as pyrrolizidine alkaloids, are commonly transferred and exchanged between living plants. In contrast to the broad spectrum of alkaloids in Senecio, in the acceptor plants nearly exclusively jacobine is accumulated. This indicates that this alkaloid is exuded specifically by the Senecio roots. Although the path of alkaloid transfer from living donor plants is not yet fully elucidated, these novel insights will extend and change our understanding of plant-plant interactions and reveal a high relevance with respect to the widespread alkaloidal contaminations of plant-derived commodities. Moreover, they could be the basis for the understanding of various so far not fully understood phenomena in cultivation of various crops, e.g. the beneficial effects of crop rotations or the co-cultivation of certain vegetables.

## Graphical abstract

Image 1

## Introduction

Toxic pyrrolizidine alkaloids (PAs) are widespread in plant kingdom, and PA containing plants are assumed to represent the most common poisonous plants affecting livestock, wildlife, and humans (Fu et al., 2004; Wiedenfeld and Edgar, 2011). In the liver of vertebrates, PAs are oxidized to unstable dehydropyrrolizidine alkaloids, also denoted as PA pyrroles (Mattocks, 1986). PA pyrroles can be hydrolyzed to form necine pyrroles, i.e., 6,7-dihydro-7-hydroxy-1-hydroxymethyl-5H-pyrrolizine (DHP). Both the PA pyrroles and DHP are strong electrophiles, which are capable of alkylating cellular nucleophiles including DNA (Williams et al., 1989; Huxtable, 1990). This bioactivation is considered to be the main reason for the high carcinogenicity of the pyrrolizidine alkaloids (e.g. Williams et al., 1989; Fu et al., 2004).

In the recent past it was shown that a large number of plant-derived commodities such as herbal teas, spices, or phytopharmaceuticals, contain significant amounts of toxic PAs (Mulder et al., 2015). A precondition to reduce these pollution is the comprehensive knowledge of the paths of contaminations. It was initially assumed that the only source of the PA contaminations is accidental co-harvesting of PA-containing weeds. However, an alternate path of contamination that involves horizontal transfer of natural products was recently discovered (Selmar et al., 2015a; Selmar et al., 2015b). According to this phenomenon, alkaloids, such as nicotine or PAs, which have been leached out from decomposing plant materials, are taken up from the soil into acceptor plants (Nowak et al., 2016; Selmar et al., 2018a). The obvious question arose, whether - in analogy - such transfer also might occur from living donor plants. The objective of this paper is to answer the question, whether or not PAs are transferred from vital plants to crops cultivated in the vicinity, and thus to identify a further source of PA contaminations. Accordingly, we co-cultivated PA-containing ragwort (Senecio jacobaea) plants with parsley together in the same pots. Thereafter, corresponding co-cultivations under field conditions of S. jacobaea with various alkaloid free acceptor plants, i.e., Petroselinum crispum, Melissa officinalis, Matricaria recutita, Mentha x piperita, and Tropaeolum majus were conducted to expound the putative transfer of the PAs between living plants growing in the near vicinity.

## Section snippets

## Plant material

Parsley plants ( Petroselinum crispum) were grown together with ragwort ( Senecio jacobaea) during spring to early summer outdoors in plant containers (60 × 15 × 15 cm) filled with about 10 L of a soil-sand mixture (3:1). In each container 6 parsley plants were co-cultivated with 12 Senecio plants for 10 weeks.

Co-cultivation under field conditions was performed in plots in the Botanical Garden of the TU Braunschweig. Parsley, melissa ( Melissa officinalis), chamomile ( Matricaria recutita),

## Transfer of PAs from living acceptor plants

After ten weeks of co-cultivation with Senecio jacobaea in the same pots, the aerial part of parsley plants were harvested and analyzed for the occurrence of PAs. The average PA content of the Senecio plants was about 4,520 mg/kg d.w. Whereas all control plants (grown solely in different pots) were completely free of alkaloids, the content of PAs in the leaves of the co-cultivated parsley plants exceeded 230 μg/kg d.w. (Fig. 1). This clearly illustrates that the PAs originally synthesized and

## Uptake and modifications of alkaloids - basic coherences

As already outlined, a direct transfer from leaf to leaf, or from root to root, respectively, can be excluded. Thus, the transfer of PAs from donor to acceptor plants must involve an uptake of alkaloids from the soil. With respect to such process, several basic matters of fact have to be considered.

It is well established that the uptake of xenobiotics and alkaloids from the soil is due to their diffusion across the biomembranes and does not require any transporter or carrier systems (Trapp, 2000

## Conclusion

Our analyses revealed that pyrrolizidine alkaloids indeed are transferred and exchanged between living plants via the soil. In all plants growing in the vicinity of the Senecio donor plants PAs, which previously had been synthesized in the Senecio plants, are accumulated. Although the exact path of transfer is not yet known, these novel insights demonstrate that such transfer could be - at least in part - responsible for the observed PA contaminations of plant-derived commodities. Accordingly,

## Declaration on conflict of interest

The authors declare no conflict of interests.

## Funding sources

The project was funded by the German Federal Ministry of Food and Agriculture via the “Fachagentur für Nachwachsende Rohstoffe” (Project No.: 95667-002). The related financial support is greatly acknowledged.

## Acknowledgements

Financial support by the German Federal Ministry of Food and Agriculture via the “Fachagentur für Nachwachsende Rohstoffe” (Project No.: 95667-002) is greatly acknowledged. We wish to thank Prof. Dr. David Seigler for fruitful discussions and critical reading the manuscript.

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