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1 August 2016 A review of garlic mustard (Alliaria petiolata, Brassicaceae) as an allelopathic plant
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Alliaria petiolata is a widespread biennial herb from Eurasia that is one of the most recognizable invasive plants of forests in the eastern United States and southern Canada. After two decades of intensive study on its physiology, ecology, and impacts, this plant has come to be known in both the scientific and gray literature as an allelopathic plant capable of exerting negative, chemically mediated effects on plants and microbes in its environment. A critical review of the literature reveals that there is evidence both supporting and failing to support this assertion, and that conclusions can be affected greatly by the experimental approaches taken, the target species examined, the sources of allelopathic inputs, and environmental factors. The objective of this review is to provide a history of allelopathy research in A. petiolata, describing the various approaches that have been taken and conclusions drawn, and to summarize the current standing of A. petiolata as an allelopathic plant using the most ecologically relevant data on this phenomenon. Finally, we discuss the degree to which allelopathy, versus other mechanisms, may contribute to the invasive success of this plant.

Alliaria petiolata as a Model Invasive Plant

Alliaria petiolata (Cavara and Grande, Brassicaceae) “Alliaria” is a biennial herb from Eurasia that was first identified in North America in the 1860s (Nuzzo 1993). Alliaria has since become known as one of the most notorious invasive plants of forest understories and edges in the eastern United States and Canada, but it is also a common, but less intrusive, plant in its native range (Blossey et al. 2001). Studies of the ecology of this plant in North America first arose in the 1970s and many of the early studies were on the life history and reproductive ecology of this plant (e.g., Cavers et al. 1979). As Alliaria was increasingly viewed as a problematic plant, attention turned to mechanisms of impact, including its ability to compete for resources (e.g., Meekins and McCarthy 1999). Another mechanism of impact, for which Alliaria has become a “poster child,” is the production of secondary metabolites that can exert negative effects on native plants, insects, and microbes (e.g., Cipollini et al. 2012a), collectively referred to here as allelopathy. After two decades of intensive study on this phenomenon, support for the assertion that allelopathy is an important invasive mechanism in this plant remains mixed. In this review, we examine the history of allelopathy research in Alliaria, highlighting studies of its direct and indirect effects on plants and beneficial microbes, and summarize the current standing of this plant as an allelopathic plant using the most ecologically relevant data on this phenomenon.

Allelochemicals From Alliaria petiolata and Their Direct Effects on Plants

In order for a plant to exert allelopathic effects, it must produce compounds with bioactive effects that are capable of entering the environment around the plant and persisting long enough to have effects on neighboring organisms. Attesting to the bioactive properties of its tissues, Alliaria has long been used as a spice, having been found in 6,000-yr-old Neolithic cooking pots from northern Europe (Saul et al. 2013). It was likely originally brought to North America in the late 1800s for culinary or medicinal uses, but accidental introductions have likely occurred as well (Nuzzo 1993). Its utility as a spice is largely due to the presence of glucosinolates, a class of compounds characteristic of the Brassicaceae that provide the pungency to mustard and other food products from this family of plants (Drewnowski and Gomez-Carneros 2000). Glucosinolates and their derivatives have been long investigated for their weed-suppressive and antimicrobial activities (Shreiner and Koide 1993). By as early as 1845, the bioactive chemistry of roots and leaves of Alliaria was being investigated, revealing that Alliaria produced a “mustard oil” in its roots similar in nature to that of black mustard, Brassica nigra (Wertheim 1845). Interestingly, Wertheim indicated that Alliaria was a common weedy plant of gardens in Germany at the time. The chemical similarity between Alliaria and B. nigra is due to the presence of allyl isothiocyanate (AITC), a volatile compound that is liberated when the glucosinolate sinigrin is hydrolyzed by the enzyme myrosinase. Allyl isothiocyanate accounts for nearly half of the volatile content of fresh Alliaria leaves (Blazevic and Mastelic 2008). While present in many weedy mustards (Brassica spp., in particular) that have invaded open habitats in North America, sinigrin and AITC appear to be novel in the native North American flora (Agerbirk et al. 2010, Barto et al. 2010a). Later studies driven primarily by a desire to understand negative effects of this plant on some North American native insects have revealed a suite of other compounds in roots and leaves of Alliaria, including novel hydroxynitrile glucosides, such as alliarinoside, as well as a variety of flavonoids, flavones and their glycosidic derivatives, and cyanide and other volatile products (e.g., Haribal and Renwick 2001, Cipollini and Gruner 2007, Blazevic and Mastelic 2008, Frisch et al. 2014).

Despite its use as a spice, some understanding of its bioactive chemistry, and its recognition as a weedy plant, no studies of allelochemically mediated ecological impacts of Alliaria are found in the literature until the 1990s. The first published study on allelopathy of Alliaria examined the effects of aqueous extracts of leaf and root tissue that were macerated in a vegetable juicer on germination and seedling growth of four nonnative commercial plant species (McCarthy and Hanson 1998). Little evidence of allelopathic inhibition of germination or growth was found, but it was likely that the vigorous tissue disruption and mixing of plant enzymes with their substrates resulted in a loss of bioactive allelochemicals from extracts, including toxic and volatile degradation products of glucosinolates that result from the action of myrosinase on parent glucosinolates. Soon after, Vaughan and Berhow (1999) reported strong effects of organic solvent extracts of whole Alliaria tissues containing allyl isothiocyanate (AITC) and benzyl isothiocyanate (BzITC), toxic degradation products of the two major glucosinolates that Alliaria produces, sinigrin and glucotropaeolin. Both compounds significantly inhibited radicle elongation of wheat (Triticum aestivum) and garden cress (Lepidium sativum).

Effects of either extracts of Alliaria or the purified compounds it contains have been found to vary with experimental conditions and target species. In tests of purified AITC and BzITC and their parent glucosinolates, Lepidium sativum (a member of the Brassicaceae) was more susceptible than Triticum aestivum to the effects of the parent glucosinolates (Vaughan and Berhow 1999), which may have been due to the possession of endogenous myrosinase by L. sativum that yielded bioactive degradation products from the parent glucosinolates. A subsequent study with L. sativum revealed that it was more tolerant to aqueous extracts of dried and ground Alliaria leaves than was lettuce, but it was more negatively affected by extracts of Alliaria than by extracts from a weedy member of its own genus, Lepidium perfoliatum (Aminidehaghi et al. 2006). Later studies (Cipollini et al. 2008, Cipollini et al. 2012) showed that Arabidopsis thaliana (a member of the Brassicaceae) suffered no negative growth and/or fitness effects from exposure to aqueous extracts of fresh Alliaria leaves, although it did f