Fungal superhighways: do common mycorrhizal networks enhance below ground communication?

In many natural communities communication between plants and other organisms below ground drives community dynamics. This communication is primarily through the release and detection of infochemicals, which must traverse the soil matrix to be effective. In this opinion article, we propose the Network Enhanced Bioactive Zone (NEBaZ) model, which posits that common mycorrhizal networks (CMNs) increase the bioactive zones of infochemicals by serving as superhighways directly connecting plants below ground. Here we argue that infochemical transport via CMNs allows for systemic defense signaling across plant populations and directed allelochemical delivery to target plants. Plant-animal interactions may also be facilitated by CMNs, suggesting that these fungal networks may be crucial components of many natural ecosystems.

Microbes as targets and mediators of allelopathy in plants.

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.

The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils.

Allelopathy, a phenomenon where compounds produced by one plant limit the growth of surrounding plants, is a controversially discussed factor in plant-plant interactions with great significance for plant community structure. Common mycorrhizal networks (CMNs) form belowground networks that interconnect multiple plant species; yet these networks are typically ignored in studies of allelopathy. We tested the hypothesis that CMNs facilitate transport of allelochemicals from supplier to target plants, thereby affecting allelopathic interactions. We analyzed accumulation of a model allelopathic substance, the herbicide imazamox, and two allelopathic thiophenes released from Tagetes tenuifolia roots, by diffusion through soil and CMNs. We also conducted bioassays to determine how the accumulated substances affected plant growth. All compounds accumulated to greater levels in target soils with CMNs as opposed to soils without CMNs. This increased accumulation was associated with reduced growth of target plants in soils with CMNs. Our results show that CMNs support transfer of allelochemicals from supplier to target plants and thus lead to allelochemical accumulation at levels that could not be reached by diffusion through soil alone. We conclude that CMNs expand the bioactive zones of allelochemicals in natural environments, with significant implications for interspecies chemical interactions in plant communities.

Density-dependent phytotoxicity of impatiens pallida plants exposed to extracts of Alliaria petiolata.

Invasive plants are by definition excellent competitors, either indirectly through competition for resources or directly through allelopathic inhibition of neighboring plants. Although both forms of competition are commonly studied, attempts to explore the interactions between direct and indirect competition are rare. We monitored the effects of several doses of extracts of Alliaria petiolata, a Eurasian invader in North America, on the growth of Impatiens pallida, a North American native, at several planting densities. The density-dependent phytotoxicity model predicts that as plant density increases, individual plant size will decrease, unless a toxin is present in the soil. In this case, individual plant size is predicted to increase as plant density increases, as plants share a limited toxin dose. We tested this model using fractions of an A. petiolata extract enriched in flavonoids or glucosinolates, as well as a combined fraction. The flavonoid-enriched fraction and the combined fraction suppressed I. pallida growth but only when applied at a dose eight times higher than that expected in the field. When treated with a dose equivalent to estimated field exposure levels, I. pallida growth was not distinguishable from that of control plants that received no extract, showing that indirect competition for resources was more important for determining the growth of I. pallida than direct allelopathic inhibition by A. petiolata. This is an important reminder that, even though many plants have the demonstrated potential to exert strong allelopathic effects, those effects may not always be apparent when other forms of competition are considered as well.

Half-lives and field soil concentrations of Alliaria petiolata secondary metabolites.

The allelopathic potential of Alliaria petiolata is well established in the lab, but questions remain about the importance of these processes in natural settings, partly because we know so little about the stability of the purported allelopathic compounds. We determined the half-lives of several flavonoid glycosides produced by A. petiolata in sterile and non-sterile soil at two temperatures. We also attempted to quantify the levels of the glucosinolates and flavonoid glycosides produced by A. petiolata, in field soils. The flavonoid glycosides had half-lives in non-sterile soil ranging from 3 to 12 h. Even in sterile soil the longest half-life was only 45.5 h. None of the glucosinolates or flavonoid glycosides produced by A. petiolata were detected in bulk soil extracts. Only one compound, isovitexin-6''-O-beta-D-glucopyranoside, was detected during nine months of biomimetic soil extraction. These very low field levels and short half-lives suggest that the allelopathic effects of A. petiolata are likely either due to degradates of the compounds produced by the plant, or to other unknown mechanisms.

Testing the optimal defense theory and the growth-differentiation balance hypothesis in Arabidopsis thaliana.

Two prominent theories proposed to explain patterns of chemical defense expression in plants are the optimal defense theory (ODT) and the growth-differentiation balance hypothesis (GDBH). The ODT predicts that plant parts with high fitness value will be highly defended, and the GDBH predicts that slow growing plant parts will have more resources available for defense and thus will have higher defense levels than faster growing tissues. We examined growth rate, fitness value, and defense protein levels in leaves of a wild and lab ecotype of Arabidopsis thaliana to address whether patterns of defense protein expression in this plant conform to predictions of either the ODT or the GDBH. We divided leaves of A. thaliana into six leaf classes based on three developmental stages: vegetative, bolting, and flowering; with two leaf ages at each stage: young and old. We assessed the fitness value of leaves by determining the impact of the removal of each leaf class on total seed production and germination rates. Although A. thaliana was highly tolerant to defoliation, young leaves were more valuable than old in general, and young leaves on bolting plants were the most valuable leaf class in particular. Young leaves on vegetative plants grew fastest in both ecotypes, while old leaves on bolting and flowering plants grew slowest. Finally, defense levels were assessed in each leaf class by quantifying the constitutive and inducible expression of four defense-related proteins. Expression of guaiacol peroxidase and chitinase activity conformed largely to GDBH predictions. Expression of trypsin inhibitor and polyphenoloxidase activity varied by leaf class and treatment, but conformed to neither GDBH nor ODT predictions.