Background Plants sustain intimate relationships with diverse microbes. It is well-recognized that these plant-associated microbiota shape individual performance and fitness of host plants, but much remains to be explored regarding how they exert their function and maintain their homeostasis.Results Here, using pink lady (Heterotis rotundifolia) as a study plant, we investigated the phenomenon of microbiota-mediated nitrogen fixation and elucidated how this process is steadily maintained in the root mucilage microhabitat. Metabolite and microbiota profiling showed that the aerial root mucilage is enriched in carbohydrates and diazotrophic bacteria. Nitrogen isotope-labeling experiments, N-15 natural abundance, and gene expression analysis indicated that the aerial root-mucilage microbiota could fix atmospheric nitrogen to support plant growth. While the aerial root mucilage is a hotspot of nutrients, we did not observe high abundance of other environmental and pathogenic microbes inside. We further identified a fungus isolate in mucilage that has shown broad-spectrum antimicrobial activities, but solely allows the growth of diazotrophic bacteria. This "friendly" fungus may be the key driver to maintain nitrogen fixation function in the mucilage microhabitat.Conclusion The discovery of new biological function and mucilage-habitat friendly fungi provides insights into microbial homeostasis maintenance of microenvironmental function and rhizosphere ecology.

The response of soil microbes to heavy metal pollution provides a metric to evaluate the soil health and ecological risks associated with heavy metal contamination. However, a multitrophic level perspective of how soil microbial communities and their functions respond to long-term exposure of multiple heavy metals remains unclear. Herein, we examined variations in soil microbial (including protists and bacteria) diversity, functional guilds and interactions along a pronounced metal pollution gradient in a field surrounding an abandoned electroplating factory. Given the stressful soil environment resulting from extremely high heavy metal concentrations and low nutrients, beta diversity of protist increased, but that of bacteria decreased, at high versus low pollution sites. Additionally, the bacteria community showed low functional diversity and redundancy at the highly polluted sites. We further identified indicative genus and "generalists" in response to heavy metal pollution. Predatory protists in Cercozoa were the most sensitive protist taxa with respect to heavy metal pollution, whereas photosynthetic protists showed a tolerance for metal pollution and nutrient deficiency. The complexity of ecological networks increased, but the communication among the modules disappeared with increasing metal pollution levels. Subnetworks of tolerant bacteria displaying functional versatility (Blastococcus, Agromyces and Opitutus) and photosynthetic protists (microalgae) became more complex with increasing metal pollution levels, indicating their potential for use in bioremediation and restoration of abandoned industrial sites contaminated by heavy metals. © 2023 Elsevier Ltd

The ability to predict future risks is essential for many organisms, including plants. Plants can gather information about potential future herbivory by detecting volatiles that are emitted by herbivore-attacked neighbors. Several individual volatiles have been identified as active danger cues. Recent work has also shown that plants may integrate multiple volatiles into their defense responses. Here, I discuss how the integration of multiple volatiles can increase the capacity of plants to predict future herbivore attack. I propose that integration of multiple volatile cues does not occur at the perception stage, but may through downstream early defense signaling and then be further consolidated by hormonal crosstalk. Exploring plant volatile cue integration can facilitate our understanding and utilization of chemical information transfer.

Plant secondary (or specialized) metabolites mediate important interactions in both the rhizosphere and the phyllosphere. If and how such compartmentalized functions interact to determine plant-environment interactions is not well understood. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth when plants are grown in soils with very low available iron but enhance growth in soils with higher available iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions and in the presence of chelated iron but enhance herbivore growth in the presence of free iron in the growth medium. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with potential consequences for plant resistance in variable environments.

Plants release distinct blends of herbivore-induced plant volatiles (HIPVs) upon herbivore attack. HIPVs have long been known to influence the behavior of herbivores and natural enemies. In addition, HIPVs can act as physiological regulators that induce or prime plant defenses. Recent work indicates that the regulatory capacity of HIPVs may extend to herbivore immunity: herbivores that are exposed to HIPVs can become more resistant or susceptible to parasitoids and pathogens. While the mechanisms of HIPV-mediated plant defense regulation are being unraveled, the mechanisms underlying the regulation of herbivore immunity are unclear. Evidence so far suggests a high degree of context dependency. Here, we review the mechanisms by which HIPVs regulate plant defense and herbivore immunity. We address major gaps of knowledge and discuss directions for future mechanistic research to facilitate efforts to use the regulatory capacity of HIPVs for the biological control of insect pests.