A novel impact of a novel weapon: allelochemicals in Alliaria petiolata disrupt the legume-rhizobia mutualism

Abstract

Some introduced species become invasive by releasing novel allelochemicals into the soil, directly harming nearby plants and soil microbes. Alliaria petiolata (garlic mustard) is an invasive plant, well known to excrete a suite of phytotoxic and antimicrobial allelochemicals, including allyl isothiocyanate (AITC) and benzyl isothiocyanate (BITC). While the effects of these chemicals on plant-mycorrhizae mutualisms are well documented, the effects on other plant-soil microbe interactions, such as the legume-rhizobia mutualism, have not yet been tested. Here, we performed laboratory and greenhouse experiments with both synthetic chemicals and leaf extracts to investigate the effects of allelochemicals in A.petiolata on a native leguminous plant, Amphicarpaea bracteata, and its rhizobia mutualists. We found that BITC reduced rhizobia growth rate in the lab, but had no effect on nodulation in the greenhouse when rhizobia were grown in the presence of plants. AITC did not directly harm either plants or rhizobia, though plants and rhizobia grown in the presence of AITC showed reduced nodulation, indicating that it disrupted the formation of the mutualism itself. We found no effects of A. petiolata allelochemical leaf extracts on plant performance or nodulation. Our data suggest that AITC causes mutualism disruption in this system by preventing the formation of nodules, which reduces plant growth and could threaten the long-term performance of rhizobia. Our study shows that the allelochemicals in A. petiolata disrupt the legume-rhizobia resource mutualism, adding another impact of these novel weapons in addition to their well-documented role in disrupting plant-mycorrhizae symbioses.

Effect of Allium sativum (garlic) extract on the growth and nodulation of cowpea (Vigna unguiculata) and groundnut (Arachis hypogea)

“…Interaction effect indicated that higher concentrations produced lower vigour index. The increased inhibitory effect at higher concentration of weed extract may be due to increase in the concentration of allelo chemicals like phenolic acids namely, P-hydroxy benzoic acid, p-coumaric acid, caffeic acid, o-coumaric acid and ferulic acid (Portales-Reyes, 2015). Similar results were noticed by Singh and Thapar (2003).…”

“…Allelopathy is the suppression of growth of one plant Adeleke 4305 species by another due to the release of toxic substances (Portales-Reyes et al, 2015;Cipollini et al, 2012). One of the studied aspects of allelopathy is the role of allelopathy in agriculture.…”

“…There are increasing evidences that the allelochemicals have significant effect on cell division, ion and water uptake, phytohormone metabolism, respiration, photosynthesis, enzyme function, as well as gene expression (Sadaqa et al, 2016;Portales-Reyes, 2015;Ian et al, 2014;Hale and Kalisz, 2012;Singh and Thapar 2003). This study was conducted to ascertain the effect of garlic extracts on the growth and nodulation of the legumes -cowpea and groundnut.…”

Comparison of the non‐native herbAlliaria petiolatawith dominant native herbs in microhabitats of a Midwestern forest

“…, Lankau , Portales‐Reyes et al. , Cipollini and Cipollini ), hypothetically providing non‐mycorrhizal Alliaria a competitive edge against native species. Woody seedlings appear to be particularly sensitive to allelopathic effects of Alliaria , likely due to their strong reliance on mycorrhizae during early development (Rodgers et al.…”

“…The possibility of allelopathy in Alliaria, in particular, has received a great deal of research attention and concern about potential ecological impacts (reviewed in Cipollini 2016, Rodgers et al 2008a). The secondary compounds in Alliaria tissues that are associated with herbivore defense are also released into Alliaria-associated soil, where they have been demonstrated to inhibit both fungal and bacterial plant symbioses (Wolfe et al 2008, Cantor et al 2011, Lankau 2011a, Portales-Reyes et al 2015, Cipollini and Cipollini 2016, hypothetically providing non-mycorrhizal Alliaria a competitive edge against native species. Woody seedlings appear to be particularly sensitive to allelopathic effects of Alliaria, likely due to their strong reliance on mycorrhizae during early development (Rodgers et al 2008a, Lankau 2011a.…”