Studies of allelopathy in terrestrial systems have experienced tremendous growth as interest has risen in describing biochemical mechanisms responsible for structuring plant communities, determining agricultural and forest productivity, and explaining invasive behaviors in introduced organisms. While early criticisms of allelopathy involved issues with allelochemical production, stability, and degradation in soils, an understanding of the chemical ecology of soils and its microbial inhabitants has been increasingly incorporated in studies of allelopathy, and recognized as an essential predictor of the outcome of allelopathic interactions between plants. Microbes can mediate interactions in a number of ways with both positive and negative outcomes for surrounding plants and plant communities. In this review, we examine cases where soil microbes are the target of allelopathic plants leading to indirect effects on competing plants, provide examples where microbes play either a protective effect on plants against allelopathic competitors or enhance allelopathic effects, and we provide examples where soil microbial communities have changed through time in response to allelopathic plants with known or potential effects on plant communities. We focus primarily on interactions involving wild plants in natural systems, using case studies of some of the world's most notorious invasive plants, but we also provide selected examples from agriculturally managed systems. Allelopathic interactions between plants cannot be fully understood without considering microbial participants, and we conclude with suggestions for future research. Allelopathy and Soil MicrobesAllelopathy, generally, is considered as a form of negative chemical communication between organisms, whereby one participant (the donor) in an interaction produces a compound(s) that is released in the environment in ecologically relevant quantities that negatively impacts the fitness of other participants (the receivers); the effect presumably benefits fitness of the donor. While the concept of allelopathy extends back to at least Theophrastus in the third century B.C., who invoked this phenomenon as an explanatory mechanism of plant growth, abundance, or community structure in natural systems, the concept has fluctuated in popularity over time (see Willis, 2007 for review). Allelopathy often has been subjected to criticisms of ecological relevance that other phenomena, such as resource competition, have not, thus explaining why it has fallen out of favor during certain time periods. However, studies of allelopathy in terrestrial systems have experienced a tremendous "rebirth" in the last 20 years as interest has risen in describing biochemical mechanisms responsible for structuring plant communities, determining agricultural and forest productivity, and explaining invasive behaviors in introduced organisms. More rigorous observational and experimental approaches, along with better analytical techniques, have
The emerald ash borer (EAB; Agrilus planipennis Fairmaire) is causing widespread mortality of ash (Fraxinus spp.) in North America. To date, no mechanisms of host resistance have been identified against this pest. Methyl jasmonate was applied to susceptible North American and resistant Asian ash species to determine if it can elicit induced responses in bark that enhance resistance to EAB. In particular, phenolic compounds, lignin, and defense-related proteins were quantified, and compounds associated with resistance were subsequently tested directly against EAB larvae in bioassays with artificial diet. MeJA application decreased adult emergence in susceptible ash species, comparable to levels achieved by insecticide application. Concentration of the phenolic compound verbascoside sharply increased after MeJA application to green and white ash. When incorporated in an artificial diet, verbascoside decreased survival and growth of EAB neonates in a dose-dependent fashion. Lignin and trypsin inhibitors were also induced by MeJA, and analogs of both compounds reduced growth of EAB larvae in artificial diets. We conclude that the application of MeJA prior to EAB attack has the ability to enhance resistance of susceptible ash trees by inducing endogenous plant defenses, and report evidence that induction of verbascoside is a mechanism of resistance to EAB.
Emerald ash borer (EAB) is an invasive beetle native to Asia that infests and kills ash (Fraxinus spp.) in North America. Previous experiments indicated that larvae feeding on co-evolved, resistant Manchurian ash (F. mandshurica) have increased antioxidant and quinone-protective enzyme activities compared to larvae feeding on susceptible North American species. Here, we examined mechanisms of host-generated oxidative and quinone-based stress and other putative defenses in Manchurian ash and the closely related and chemically similar, but susceptible, black ash (F. nigra), with and without exogenous application of methyl jasmonate (MeJA) to induce resistance mechanisms. Peroxidase activities were 4.6-13.3 times higher in Manchurian than black ash, although both species appeared to express the same three peroxidase isozymes. Additionally, peroxidase-mediated protein cross-linking activity was stronger in Manchurian ash. Polyphenol oxidase, β-glucosidase, chitinase, and lipoxygenase activities also were greater in Manchurian ash, but only lipoxygenase activity increased with MeJA application. Phloem HO levels were similar and were increased by MeJA application in both species. Lastly, trypsin inhibitor activity was detected in methanol and water extracts that were not allowed to oxidize, indicating the presence of phenolic-based trypsin inhibitors. However, no proteinaceous trypsin inhibitor activity was detected in either species. In response to MeJA application, Manchurian ash had higher trypsin inhibitor activity than black ash using the unoxidized water extracts, but no treatment effects were detected using methanol extracts. Based on these results we hypothesize that peroxidases, lignin polymerization, and quinone generation contribute to the greater resistance to EAB displayed by Manchurian ash.
The "mother knows best" hypothesis states that adults should choose hosts for ovipo sition on which their offspring will best perform, maximizing their own fitness. It has been hypoth esized that this preference-performance relationship for wood-boring insects is especially important because larvae are not able to switch hosts, although no study has examined oviposition choices for these insects. We examined oviposition preferences of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), in two common gardens, one on the campus of Wright State University in Dayton, OH, and the other at the Michigan State University Tollgate Research Farm in Novi, MI, by wrapping cheesecloth around ash trunks to assess passive oviposition patterns. We found that in both gardens, ash species native to North America, which are highly susceptible to the emerald ash borer, consistently received more ova than Manchurian ash, which is indigenous to Asia and more resistant to the emerald ash borer. Susceptible trees in the Novi garden received 93 times the number of ova and susceptible trees at the Wright State garden received up to 25 times the number of ova that were received by Manchurian ash in each of their respective gardens. Neither tree size nor vigor affected oviposition choice. There were also higher numbers of adult exit holes on North American than Manchurian ash in both common gardens. The observed oviposition preferences in this study align with patterns of adult feeding preference, ash host mortality, and exit hole numbers from other studies. These observations also suggest that oviposition preferences may contribute to interspecific patterns of host resistance and mortality. Collectively, our results demonstrate that the emerald ash borer prefers to oviposit on species on which its offspring will best perform, suggesting that there is strong selection for the ability to recognize host cues that predict better larval survival and perfor mance.KEY WORDS invasive wood borer, host selection, preference-performance, host plant resistance, antixenosisThe forces acting on female oviposition choice have long been an important topic in behavioral and evo lutionary biology and specifically in the context of plant-insect interactions (Gripenberg et al. 2010). The "mother knows best" hypothesis underlies key insect host-plant selection models (Jaenike 1978, Bernays and Graham 1988, Mayhew 2001, predicting that females will oviposit on hosts on which their progeny will optimally perform, which in turn will optimize
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