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Most of Earths trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earths land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.IMPORTANCEUnderstanding how soil microbes interact with one another and their host plant will help us combat the negative effects that climate change has on terrestrial ecosystems. Unfortunately, we lack a clear understanding of how the presence of ectomycorrhizal fungi (EcMF)-one of the most dominant soil microbial groups on Earth-shapes belowground organic resources and the composition of bacterial communities. To address this knowledge gap, we profiled lipid and non-lipid metabolites in soils and plant roots, characterized soil bacterial communities, and compared soils amended either with or without EcMF. Our results show that the presence of EcMF changes soil organic resource availability, impacts the proliferation of different bacterial communities (in terms of both type and potential function), and primes plant root chemistry for pathogen suppression and energy conservation. Our findings therefore provide much-needed insight into how two of the most dominant soil microbial groups interact with one another and with their host plant.

BACKGROUND: Biological control of insect pests is encountering an unprecedented challenge in agricultural systems due to the ongoing rise in carbon dioxide (CO2) level. The use of entomopathogenic fungi (EPF) in these systems is gaining increased attention, and EPF as crop endophytes hold the potential for combining insect pest control and yield enhancement of crops, but the effects of increased CO2 concentration on this interaction are poorly understood. Here, the introduction of endophytic EPF was explored as an alternative sustainable management strategy benefiting crops under elevated CO2, using maize (Zea mays), Asian corn borer (Ostrinia furnacalis), and EPF (Beauveria bassiana) to test changes in damage to maize plants from O. furnacalis, and the nutritional status (content of carbon, nitrogen, phosphorus, potassium), biomass, and yield of maize. RESULTS: The results showed that endophytic B. bassiana could alleviate the damage caused by O. furnacalis larvae for maize plants under ambient CO2 concentration, and this effect was enhanced under higher CO2 concentration. Inoculation with B. bassiana effectively counteracted the adverse impact of elevated CO2 on maize plants by preserving the nitrogen content at its baseline level (comparable with ambient CO2 conditions without B. bassiana). Both simultaneous effects could explain the improvement of biomass and yield of maize under B. bassiana inoculation and elevated CO2. CONCLUSION: This finding provides key information about the multifaceted benefits of B. bassiana as a maize endophyte. Our results highlight the promising potential of incorporating EPF as endophytes into integrated pest management strategies, particularly under elevated CO2 concentrations. © 2024 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. [ABSTRACT FROM AUTHOR]

ABSTRACT Interactions between arbuscular mycorrhizal fungi (AMF), plants, and the soil microbial community have the potential to increase the availability and uptake of phosphorus (P) and nitrogen (N) in agricultural systems. Nutrient exchange between plant roots, AMF, and the adjacent soil microbes occurs at the interface between roots colonized by mycorrhizal fungi and soil, referred to as the mycorrhizosphere. Research on the P exchange focuses on plant–AMF or AMF–microbe interactions, lacking a holistic view of P exchange between the plants, AMF, and other microbes. Recently, N exchange at both interfaces revealed the synergistic role of AMF and bacterial community in N uptake by the host plant. Here, we highlight work carried out on each interface and build upon it by emphasizing research involving all members of the tripartite network. Both nutrient systems are challenging to study due to the complex chemical and biological nature of the mycorrhizosphere. We discuss some of the effective methods to identify important nutrient processes and the tripartite members involved in these processes. The extrapolation of in vitro studies into the field is often fraught with contradiction and noise. Therefore, we also suggest some approaches that can potentially bridge the gap between laboratory-generated data and their extrapolation to the field, improving the applicability and contextual relevance of data within the field of mycorrhizosphere interactions. Overall, we argue that the research community needs to adopt a holistic tripartite approach and that we have the means to increase the applicability and accuracy of in vitro data in the field.

ABSTRACT Most of Earth’s trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth’s land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.IMPORTANCEUnderstanding how soil microbes interact with one another and their host plant will help us combat the negative effects that climate change has on terrestrial ecosystems. Unfortunately, we lack a clear understanding of how the presence of ectomycorrhizal fungi (EcMF)—one of the most dominant soil microbial groups on Earth—shapes belowground organic resources and the composition of bacterial communities. To address this knowledge gap, we profiled lipid and non-lipid metabolites in soils and plant roots, characterized soil bacterial communities, and compared soils amended either with or without EcMF. Our results show that the presence of EcMF changes soil organic resource availability, impacts the proliferation of different bacterial communities (in terms of both type and potential function), and primes plant root chemistry for pathogen suppression and energy conservation. Our findings therefore provide much-needed insight into how two of the most dominant soil microbial groups interact with one another and with their host plant.

BACKGROUND: Plant volatile organic compounds (VOCs) modified by plant‐associated microbes can attract or repel the oviposition of herbivores. Here, we explored the effects of three different fungi on apples' VOCs and the cascading impacts on the oviposition preference of yellow peach moth [YPM, Conogethes punctiferalis (Guenée)]. RESULTS: Among Penicillium crustosum‐infected apples (PCA), Rhizopus oryzae‐infected apples (ROA), Colletotrichum gloeosporioides‐infected apples (CGA) and healthy apples (HA), mated YPM females preferred to oviposit eggs on ROA and CGA, and showed significant attractiveness to VOCs from PCA, ROA, and CGA under laboratory conditions. The VOCs analyses showed that there were significant differences between fungi‐infected apples (ROA, CGA) and control treatments (mechanically damaged apples (MDA), HA) in terms of the relative contents of 13 VOCs. The relative contents of ethyl 2‐methylbutyrate, ethyl caprylate, estragole, ethyl hexanoate in ROA and CGA were higher than those in MDA. The relative content of isopropyl 2‐methylbutyrate in ROA was significantly higher than those in HA and CGA. The relative contents of 2‐methylbutyl acetate, butyl 2‐methylbutyrate, hexyl 2‐methylbutyrate, amyl hexanoate, hexyl hexanoate, (E, E)‐α‐farnesene in ROA and CGA were lower than those in HA. The relative content of hexyl acetate in ROA and CGA was significantly higher than that in MDA, but lower than that in HA. Additionally, 10 fungi‐induced VOCs were detected in ROA and/or CGA. When 20 VOCs from ROA and/or CGA were tested as individuals or mixed blends in Y‐tube olfactometer assays, mated YPM females preferred amyl 2‐methylbutyrate, isoamyl 2‐methylbutyrate, isopropyl 2‐methylbutyrate, hexyl propionate (common VOCs in ROA, CGA, and HA), and heptacosane (a fungi‐induced VOC in ROA), but no significant preferences were observed between individual compounds and mixed blends, except for hexyl propionate. CONCLUSION: Different fungi infection increased the relative contents of common VOCs from healthy and fungi‐infected apples, which ultimately resulted in the significant attractiveness for the oviposition of mated YPM females. This study clarified why fungi‐infected apples were more attractive to YPMs than healthy apples and screened out the crucial VOCs for YPM oviposition. © 2023 Society of Chemical Industry. [ABSTRACT FROM AUTHOR]

Abstract Background Leptosphaeria maculans “brassicae” (Lmb) and Leptosphaeria biglobosa “brassicae” (Lbb) make up a species complex involved in the stem canker (blackleg) disease of rapeseed (Brassica napus). They coinfect rapeseed together, from the early stage of infection on leaves to the final necrotic stage at the stem base, and both perform sexual crossings on plant residues. L. biglobosa is suggested to be a potential biocontrol agent against Lmb, but there has been no mechanistic investigation of the different types of interactions that may occur between the plant and the two fungal species. Results We investigated the bi- or tripartite interaction mechanisms by (i) confronting Lmb and Lbb in culture conditions or during cotyledon infection, with different timing and/or spore concentration regimes, (ii) performing RNA-Seq experiments in vitro or on the kinetics of infection of cotyledons infected by Lmb and/or Lbb to evaluate the transcriptomic activity and the plant response when both fungal species are inoculated together. Lbb infection of B. napus cotyledons was typical of a necrotrophic behavior, with a very early setup of one pathogenicity program and very limited colonization of tissues. This contrasted with the complex succession of pathogenicity programs of the hemibiotroph Lmb. During simultaneous co-infection by both species, Lmb was strongly impacted in its growth and transcriptomic dynamics both in vitro and in planta, while Lbb was unaffected by the presence of Lmb. However, the drastic inhibition of Lmb growth by Lbb was ineffective in the case of delayed inoculation with Lbb or a lower amount of spores of Lbb compared to Lmb. Conclusions Our data suggest that Lmb growth inhibition by Lbb is the result of a combination of factors that may include competition for trophic resources, the generation by Lbb of an environment unsuitable for the lifecycle of Lmb or/and the effect on Lmb of plant defense responses induced by Lbb. It indicates that growth inhibition occurs in very specific conditions (i.e., co-inoculation at the same place of an equal amount of inoculum) that are unlikely to occur in the field where their coexistence does not prevent any species from completing their life cycle.

Background: Leptosphaeria maculans "brassicae" (Lmb) and Leptosphaeria biglobosa "brassicae" (Lbb) make up a species complex involved in the stem canker (blackleg) disease of rapeseed (Brassica napus). They coinfect rapeseed together, from the early stage of infection on leaves to the final necrotic stage at the stem base, and both perform sexual crossings on plant residues. L. biglobosa is suggested to be a potential biocontrol agent against Lmb, but there has been no mechanistic investigation of the different types of interactions that may occur between the plant and the two fungal species. Results: We investigated the bi- or tripartite interaction mechanisms by (i) confronting Lmb and Lbb in culture conditions or during cotyledon infection, with different timing and/or spore concentration regimes, (ii) performing RNA-Seq experiments in vitro or on the kinetics of infection of cotyledons infected by Lmb and/or Lbb to evaluate the transcriptomic activity and the plant response when both fungal species are inoculated together. Lbb infection of B. napus cotyledons was typical of a necrotrophic behavior, with a very early setup of one pathogenicity program and very limited colonization of tissues. This contrasted with the complex succession of pathogenicity programs of the hemibiotroph Lmb. During simultaneous co-infection by both species, Lmb was strongly impacted in its growth and transcriptomic dynamics both in vitro and in planta, while Lbb was unaffected by the presence of Lmb. However, the drastic inhibition of Lmb growth by Lbb was ineffective in the case of delayed inoculation with Lbb or a lower amount of spores of Lbb compared to Lmb. Conclusions: Our data suggest that Lmb growth inhibition by Lbb is the result of a combination of factors that may include competition for trophic resources, the generation by Lbb of an environment unsuitable for the lifecycle of Lmb or/and the effect on Lmb of plant defense responses induced by Lbb. It indicates that growth inhibition occurs in very specific conditions (i.e., co-inoculation at the same place of an equal amount of inoculum) that are unlikely to occur in the field where their coexistence does not prevent any species from completing their life cycle. [ABSTRACT FROM AUTHOR]

Global potato production is plagued by multiple pathogens, amongst which are Phytophthora infestans and Alternaria solani, the causal agents of potato late blight and early blight, respectively. Both these pathogens have different lifestyles and are successful pathogens of potato, but despite observations of both pathogens infecting potato simultaneously in field conditions, the tripartite interactions between potato and these two pathogens are so far poorly understood. Here we studied the interaction of A. solani and P. infestans first in vitro and subsequently in planta both in laboratory and field settings. We found that A. solani can inhibit P. infestans in terms of growth in vitro and also infection of potato in both laboratory experiments and in an agriculturally relevant field setting. A. solani had a direct inhibitory effect on P. infestans in vitro and compounds secreted by A. solani had both an inhibitory and disruptive effect on sporangia and mycelium of P. infestans in vitro. In planta infection bioassays revealed that simultaneous co‐inoculation of both pathogens resulted in larger necrotic lesions than single inoculations; however, consecutive inoculations only resulted in larger lesions when A. solani was inoculated after P. infestans. These results indicate that the order in which these pathogens attempt to colonize potato is important for the disease outcome and that the influence of plant pathogens on each other should be accounted for in the design of future disease control strategies in crops such as potato. [ABSTRACT FROM AUTHOR]

Arbuscular mycorrhizal fungi (AMF) are essential components of the plant root mycobiome and are found in approximately 80% of land plants. As obligate plant symbionts, AMF harbor their own microbiota, both inside and outside the plant root system. AMF-associated bacteria (AAB) possess various functional traits, including nitrogen fixation, organic and inorganic phosphate mobilization, growth hormone production, biofilm production, enzymatic capabilities, and biocontrol against pathogen attacks, which not only contribute to the health of the arbuscular mycorrhizal symbiosis but also promote plant growth. Because of this, there is increasing interest in the diversity, functioning, and mechanisms that underlie the complex interactions between AMF, AAB, and plant hosts. This review critically examines AMF-associated bacteria, focusing on AAB diversity, the factors driving richness and community composition of these bacteria across various ecosystems, along with the physical, chemical, and biological connections that enable AMF to select and recruit beneficial bacterial symbionts on and within their structures and hyphospheres. Additionally, potential applications of these bacteria in agriculture are discussed, emphasizing the potential importance of AMF fungal highways in engineering plant rhizosphere and endophyte bacteria communities, and the importance of a functional core of AAB taxa as a promising tool to improve plant and soil productivity. Thus, AMF and their highly diverse bacterial taxa represent important tools that could be efficiently explored in sustainable agriculture, carbon sequestration, and reduction of greenhouse gas emissions related to nitrogen fertilizer applications. Nevertheless, future studies adopting integrated multidisciplinary approaches are crucial to better understand AAB functional diversity and the mechanisms that govern these tripartite relationships. [ABSTRACT FROM AUTHOR]

Yellow peach moth (Conogethes punctiferalis (Guenée), (Lepidoptera: Crambidae), YPM) and maize ear rot are important pests and diseases of maize (Zea mays L., (Poales: Poaceae)). In recent years, YPM has become the most destructive maize pest in the Huang-Huai-Hai summer maize region of China via the tunneling of larvae into maize ears. Interestingly, YPM infestation aggravates the occurrence of maize ear rot and causes heavier yield loss of maize in the field. However, few studies report whether maize ear rot would also affect the behavior of YPM. Here, we identified the effects of maize ear rot caused by four different fungi on maize ears' volatile organic compounds (VOCs) and the cascading effects on the behavior of YPM. The current results found that mated YPM females showed a preference for mock-inoculated maize ears (MIM) or mechanically damaged maize ears (MDM) but showed repellence to Penicillium oxalicum (Eurotiales: Aspergillaceae)-infected maize ears (POM), Trichoderma asperellum (Hypocreales: Hypocreaceae)-infected maize ears (TAM), Aspergillus phoenicis (Eurotiales: Aspergillaceae)-infected maize ears (APM), Aspergillus flavus (Eurotiales: Aspergillaceae)-infected maize ears (AFM) in the oviposition selection and four-arm olfactometer experiments, indicating that VOCs emitting from fungi-infected maize ears were all repellent to mated YPM females. Further analyses showed that 57 VOCs were identified from all treatments. The partial least squares discriminant analysis (PLS-DA) displayed a separation between TAM, APM, AFM and POM, MDM, and MIM, with 24.3% and 19.1% explanation rates of the first two PLS components. Moreover, the relative quantities of eight common VOCs from different treatments were lower, and the other three common VOCs were higher in fungi-infected maize ears than those in MIM or MDM. There were also 17 unique VOCs in fungi-infected maize ears. In conclusion, these results suggested that maize ear rot negatively affected the behavior of YPM by changing both components and proportions of maize ears' VOCs. These behavior-modifying VOCs may form the basis for the development of attractant or repellent formulations for YPM's management in the future. [ABSTRACT FROM AUTHOR]

The freshwater polyp Hydra viridissima (H. viridissima) harbors endosymbiotic Chlorella algae in addition to a species-specific microbiome. The molecular basis of the symbiosis between Hydra and Chlorella has been characterized to be metabolic in nature. Here, we studied the interaction between the extracellularly located microbiota and the algal photobiont, which resides in Hydra 's endodermal epithelium, with main focus on Legionella bacterium. We aimed at evaluating the influence of the symbiotic algae on microbial colonization and in shaping the host microbiome. We report that the microbiome composition of symbiotic and aposymbiotic (algae free) H. viridissima is significantly different and dominated by Legionella spp. Hvir in aposymbiotic animals. Co-cultivation of these animals resulted in horizontal transmission of Legionella spp. Hvir bacteria from aposymbiotic to symbiotic animals. Acquisition of this bacterium increased the release of algae into ambient water. From there, algae could subsequently be taken up again by the aposymbiotic animals. The presence of algal symbionts had negative impact on Legionella spp. Hvir and resulted in a decrease of the relative abundance of this bacterium. Prolonged co-cultivation ultimately resulted in the disappearance of the Legionella spp. Hvir bacterium from the Hydra tissue. Our observations suggest an important role of the photobiont in controlling an invasive species in a metacommunity and, thereby, shaping the microbiome. [ABSTRACT FROM AUTHOR]

The freshwater polyp Hydra viridissima (H. viridissima) harbors endosymbiotic Chlorella algae in addition to a species-specific microbiome. The molecular basis of the symbiosis between Hydra and Chlorella has been characterized to be metabolic in nature. Here, we studied the interaction between the extracellularly located microbiota and the algal photobiont, which resides in Hydra’s endodermal epithelium, with main focus on Legionella bacterium. We aimed at evaluating the influence of the symbiotic algae on microbial colonization and in shaping the host microbiome. We report that the microbiome composition of symbiotic and aposymbiotic (algae free) H. viridissima is significantly different and dominated by Legionella spp. Hvir in aposymbiotic animals. Co-cultivation of these animals resulted in horizontal transmission of Legionella spp. Hvir bacteria from aposymbiotic to symbiotic animals. Acquisition of this bacterium increased the release of algae into ambient water. From there, algae could subsequently be taken up again by the aposymbiotic animals. The presence of algal symbionts had negative impact on Legionella spp. Hvir and resulted in a decrease of the relative abundance of this bacterium. Prolonged co-cultivation ultimately resulted in the disappearance of the Legionella spp. Hvir bacterium from the Hydra tissue. Our observations suggest an important role of the photobiont in controlling an invasive species in a metacommunity and, thereby, shaping the microbiome.

Simple Summary: Plant growth-promoting rhizobacteria (PGPR) are rhizosphere-inhabiting eco-friendly bacteria that indirectly/directly enhance plant growth and development and are tipped as the 'Messiah" of plant protection against environmental stresses. However, their large-scale use in agriculture is still minimal due to the limited knowledge on them. From a metabolomics perspective, we review the current knowledge on PGPR–plant chemical communication leading to plant priming/resistant induction, highlight complex tripartite chemical interactions in the rhizosphere, and show how metabolomics can help unravel these chemical communications. Plant growth-promoting rhizobacteria (PGPR) are beneficial microorganisms colonising the rhizosphere. PGPR are involved in plant growth promotion and plant priming against biotic and abiotic stresses. Plant–microbe interactions occur through chemical communications in the rhizosphere and a tripartite interaction mechanism between plants, pathogenic microbes and plant-beneficial microbes has been defined. However, comprehensive information on the rhizosphere communications between plants and microbes, the tripartite interactions and the biochemical implications of these interactions on the plant metabolome is minimal and not yet widely available nor well understood. Furthermore, the mechanistic nature of PGPR effects on induced systemic resistance (ISR) and priming in plants at the molecular and metabolic levels is yet to be fully elucidated. As such, research investigating chemical communication in the rhizosphere is currently underway. Over the past decades, metabolomics approaches have been extensively used in describing the detailed metabolome of organisms and have allowed the understanding of metabolic reprogramming in plants due to tripartite interactions. Here, we review communication systems between plants and microorganisms in the rhizosphere that lead to plant growth stimulation and priming/induced resistance and the applications of metabolomics in understanding these complex tripartite interactions. [ABSTRACT FROM AUTHOR]

Arbuscular mycorrhizal (AM) fungi and rhizobium are likely important drivers of plant coexistence and grassland productivity due to complementary roles in supplying limiting nutrients. However, the interactive effects of mycorrhizal and rhizobial associations on plant community productivity and competitive dynamics remain unclear. To address this, we conducted a greenhouse experiment to determine the influences of these key microbial functional groups on communities comprising three plant species by comparing plant communities grown with or without each symbiont. We also utilized N-fertilization and clipping treatments to explore potential shifts in mycorrhizal and rhizobial benefits across abiotic and biotic conditions. Our research suggests AM fungi and rhizobium co-inoculation was strongly facilitative for plant community productivity and legume (Medicago sativa) growth and nodulation. Plant competitiveness shifted in the presence of AM fungi and rhizobium, favoring M. sativa over a neighboring C4 grass (Andropogon gerardii) and C3 forb (Ratibida pinnata). This may be due to rhizobial symbiosis as well as the relatively greater mycorrhizal growth response of M. sativa, compared to the other model plants. Clipping and N-fertilization altered relative costs and benefits of both symbioses, presumably by altering host-plant nitrogen and carbon dynamics, leading to a relative decrease in mycorrhizal responsiveness and proportional biomass of M. sativa relative to the total biomass of the entire plant community, with a concomitant relative increase in A. gerardii and R. pinnata proportional biomass. Our results demonstrate a strong influence of both microbial symbioses on host-plant competitiveness and community dynamics across clipping and N-fertilization treatments, suggesting the symbiotic rhizosphere community is critical for legume establishment in grasslands. [ABSTRACT FROM AUTHOR]

Yellow peach moth (Conogethes punctiferalis (Guenée), (Lepidoptera: Crambidae), YPM) and maize ear rot are important pests and diseases of maize (Zea mays L., (Poales: Poaceae)). In recent years, YPM has become the most destructive maize pest in the Huang-Huai-Hai summer maize region of China via the tunneling of larvae into maize ears. Interestingly, YPM infestation aggravates the occurrence of maize ear rot and causes heavier yield loss of maize in the field. However, few studies report whether maize ear rot would also affect the behavior of YPM. Here, we identified the effects of maize ear rot caused by four different fungi on maize ears’ volatile organic compounds (VOCs) and the cascading effects on the behavior of YPM. The current results found that mated YPM females showed a preference for mock-inoculated maize ears (MIM) or mechanically damaged maize ears (MDM) but showed repellence to Penicillium oxalicum (Eurotiales: Aspergillaceae)-infected maize ears (POM), Trichoderma asperellum (Hypocreales: Hypocreaceae)-infected maize ears (TAM), Aspergillus phoenicis (Eurotiales: Aspergillaceae)-infected maize ears (APM), Aspergillus flavus (Eurotiales: Aspergillaceae)-infected maize ears (AFM) in the oviposition selection and four-arm olfactometer experiments, indicating that VOCs emitting from fungi-infected maize ears were all repellent to mated YPM females. Further analyses showed that 57 VOCs were identified from all treatments. The partial least squares discriminant analysis (PLS-DA) displayed a separation between TAM, APM, AFM and POM, MDM, and MIM, with 24.3% and 19.1% explanation rates of the first two PLS components. Moreover, the relative quantities of eight common VOCs from different treatments were lower, and the other three common VOCs were higher in fungi-infected maize ears than those in MIM or MDM. There were also 17 unique VOCs in fungi-infected maize ears. In conclusion, these results suggested that maize ear rot negatively affected the behavior of YPM by changing both components and proportions of maize ears’ VOCs. These behavior-modifying VOCs may form the basis for the development of attractant or repellent formulations for YPM’s management in the future.

Controlled greenhouse studies have shown the numerous ways that soil microbes can impact plant growth and development. However, natural soil communities are highly complex, and plants interact with many bacterial and fungal taxa simultaneously. Due to logistical challenges associated with manipulating more complex microbiome communities, how microbial communities impact emergent patterns of plant growth therefore remains poorly understood. For instance, do the interactions between bacteria and fungi generally yield additive (i.e. sum of their parts) or nonadditive, higher order plant growth responses? Without this information, our ability to accurately predict plant responses to microbial inoculants is weakened. To address these issues, we conducted a meta-analysis to determine the type (additive or higher-order, nonadditive interactions), frequency, direction (positive or negative), and strength that bacteria and mycorrhizal fungi (arbuscular and ectomycorrhizal) have on six phenotypic plant growth responses. Our results demonstrate that co-inoculations of bacteria and mycorrhizal fungi tend to have positive additive effects on many commonly reported plant responses. However, ectomycorrhizal plant shoot height responds positively and nonadditively to co-inoculations of bacteria and ectomycorrhizal fungi, and the strength of additive effects also differs between mycorrhizae type. These findings suggest that inferences from greenhouse studies likely scale to more complex field settings and that inoculating plants with diverse, beneficial microbes is a sound strategy to support plant growth., Competing Interests: The authors declare no competing interests., (© The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.)

Interactions between arbuscular mycorrhizal fungi (AMF), plants, and the soil microbial community have the potential to increase the availability and uptake of phosphorus (P) and nitrogen (N) in agricultural systems. Nutrient exchange between plant roots, AMF, and the adjacent soil microbes occurs at the interface between roots colonized by mycorrhizal fungi and soil, referred to as the mycorrhizosphere. Research on the P exchange focuses on plant-AMF or AMF-microbe interactions, lacking a holistic view of P exchange between the plants, AMF, and other microbes. Recently, N exchange at both interfaces revealed the synergistic role of AMF and bacterial community in N uptake by the host plant. Here, we highlight work carried out on each interface and build upon it by emphasizing research involving all members of the tripartite network. Both nutrient systems are challenging to study due to the complex chemical and biological nature of the mycorrhizosphere. We discuss some of the effective methods to identify important nutrient processes and the tripartite members involved in these processes. The extrapolation of in vitro studies into the field is often fraught with contradiction and noise. Therefore, we also suggest some approaches that can potentially bridge the gap between laboratory-generated data and their extrapolation to the field, improving the applicability and contextual relevance of data within the field of mycorrhizosphere interactions. Overall, we argue that the research community needs to adopt a holistic tripartite approach and that we have the means to increase the applicability and accuracy of in vitro data in the field., Competing Interests: The authors declare no conflict of interest.

This study was aimed to investigate whether host plant species and lifestyles, and environmental conditions in the desert affect endophytic fungi composition. Endophytic fungal communities from parasitic plant Cynomorium songaricum and its host Nitraria tangutorum were investigated from three sites including Tonggu Naoer, Xilin Gaole, and Guazhou in Tengger and Badain Jaran Deserts in China using the next-generation sequencing of a ribosomal RNA gene region. Similarity and difference in endophytic fungal composition from different geographic locations were evaluated through multivariate statistical analysis. It showed that plant genetics was a deciding factor affecting endophytic fungal composition even when C. songaricum and N. tangutorum grow together tightly. Not only that, the fungal composition was also greatly affected by the local environment and rainfall. However, the distribution and richness of fungal species indicated that the geographical distance exerted little influence on characterizing the fungal composition. Overall, the findings suggested that plant species, parasitic or non-parasitic lifestyles of the plant, and local environment strongly affected the number and diversity of the endophytic fungal species, which may provide valuable insights into the microbe ecology, symbiosis specificity, and the tripartite relationship among parasitic plant, host, and endophytic fungi, especially under desert environment. [ABSTRACT FROM AUTHOR]

Upon infection with insect-borne microbial pathogens, plants are exposed to two types of damage simultaneously. Over the past decade, numerous molecular studies have been conducted to understand how plants respond to pathogens or herbivores. However, investigations of host responses typically focus on a single stress and are performed under static laboratory conditions. In this review, we highlight research that sheds light on how plants deploy broad-spectrum mechanisms against both vector-borne pathogens and insect vectors. Among the host genes involved in multistress resistance, many are involved in innate immunity and phytohormone signaling (especially jasmonate and salicylic acid). The potential for genome editing or chemical modulators to fine-tune crop defensive signaling, to develop sustainable methods to control insect-borne diseases, is discussed. There is increasing evidence that the interaction between plant host and vector-borne pathogens, can only be understood from a tripartite viewpoint, pathogen–vector–plant. Some aspects of plant innate immunity are also applicable to interactions between plants and phloem-infecting pathogens or herbivore vectors. Phytohormones and their regulation network via transcription factors, are at the forefront of the interactions between plant and vector-borne pathogens. Pathogens and herbivores have evolved strategies to convergently target jasmonic acid signaling at the jasmonate ZIM (JAZ)-MYC hub. [ABSTRACT FROM AUTHOR]

The dynamics of ecological communities depend partly on species interactions within and among trophic levels. Experimental work has demonstrated the impact of species interactions on the species involved, but it remains unclear whether these effects can also be detected in long‐term time series across heterogeneous landscapes. We analyzed a 19‐yr time series of patch occupancy by the Glanville fritillary butterfly Melitaea cinxia, its specialist parasitoid wasp Cotesia melitaearum, and the specialist fungal pathogen Podosphaera plantaginis infecting Plantago lanceolata, a host plant of the Glanville fritillary. These species share a network of more than 4,000 habitat patches in the Åland islands, providing a metacommunity data set of unique spatial and temporal resolution. To assess the influence of interactions among the butterfly, parasitoid, and mildew on metacommunity dynamics, we modeled local colonization and extinction rates of each species while including or excluding the presence of potentially interacting species in the previous year as predictors. The metapopulation dynamics of all focal species varied both along a gradient in host plant abundance, and spatially as indicated by strong effects of local connectivity. Colonization and to a lesser extent extinction rates depended also on the presence of interacting species within patches. However, the directions of most effects differed from expectations based on previous experimental and modeling work, and the inferred influence of species interactions on observed metacommunity dynamics was limited. These results suggest that although local interactions among the butterfly, parasitoid, and mildew occur, their roles in metacommunity spatiotemporal dynamics are relatively weak. Instead, all species respond to variation in plant abundance, which may in turn fluctuate in response to variation in climate, land use, or other environmental factors. [ABSTRACT FROM AUTHOR]

Blood-feeding enriched gut-microbiota boosts mosquitoes' anti-Plasmodium immunity. Here, we ask how Plasmodium vivax alters gut-microbiota, anti-Plasmodial immunity, and impacts tripartite Plasmodium-mosquito-microbiota interactions in the gut lumen. We used a metagenomics and RNAseq strategy to address these questions. In naïve mosquitoes, Elizabethkingia meningitis and Pseudomonas spp. are the dominant bacteria and blood-feeding leads to a heightened detection of Elizabethkingia, Pseudomonas and Serratia 16S rRNA. A parallel RNAseq analysis of blood-fed midguts also shows the presence of Elizabethkingia-related transcripts. After, P. vivax infected blood-meal, however, we do not detect bacterial 16S rRNA until circa 36 h. Intriguingly, the transcriptional expression of a selected array of antimicrobial arsenal cecropins 1–2, defensin-1, and gambicin remained low during the first 36 h—a time frame when ookinetes/early oocysts invaded the gut. We conclude during the preinvasive phase, P. vivax outcompetes midgut-microbiota. This microbial suppression likely negates the impact of mosquito immunity which in turn may enhance the survival of P. vivax. Detection of sequences matching to mosquito-associated Wolbachia opens a new inquiry for its exploration as an agent for “paratransgenesis-based” mosquito control.

Planorbidae snails are the intermediate host for the trematode parasite of the Schistosoma genus, which is responsible for schistosomiasis, a disease that affects both humans and cattle. The microbiota for Schistosoma has already been described as having an effect on host/parasite interactions, specifically through immunological interactions. Here, we sought to characterize the microbiota composition of seven Planorbidae species and strains. Individual snail microbiota was determined using 16S ribosomal DNA amplicon sequencing. The bacterial composition was highly specific to the host strain with limited interindividual variation. In addition, it displayed complete congruence with host phylogeny, revealing a phylosymbiosis pattern. These results were confirmed in a common garden, suggesting that the host highly constrains microbial composition. This study presents the first comparison of bacterial communities between several intermediate snail hosts of Schistosoma parasites, paving the way for further studies on the understanding of this tripartite interaction.

Abstract Background Tsetse flies are vectors of human and animal African trypanosomiasis. In spite of many decades of chemotherapy and vector control, the disease has not been eradicated. Other methods like the transformation of tsetse fly symbionts to render the fly refractory to trypanosome infection are being evaluated. The aim of the present study was to evaluate the association between trypanosome infections and the presence of symbionts in these tsetse species. Tsetse flies were trapped in two villages of the “Faro and Déo” Division of the Adamawa region of Cameroon. In the field, tsetse fly species were identified and their infection by trypanosomes was checked by microscopy. In the laboratory, DNA was extracted from their midguts and the presence of symbionts (Sodalis glossinidius and Wolbachia sp.) and trypanosomes was checked by PCR. Symbionts/trypanosomes association tests were performed. Results Three tsetse fly species including Glossina tachinoides (90.1%), Glossina morsitans submorsitans (9.4%) and Glossina fuscipes fuscipes (0.5%) were caught. In all the population we obtained an occurrence rate of 37.2% for Sodalis glossinidius and 67.6% for Wolbachia irrespective to tsetse flies species. S. glossinidius and Wolbachia sp. occurrence rates were respectively 37 and 68% for G. tachinoides and 28.6 and 59.5% for G. m. submorsitans. Between Golde Bourle and Mayo Dagoum significant differences were observed in the prevalence of symbionts. Prevalence of trypanosomes were 34.8% for Glossina tachinoides and 40.5% for Glossina morsitans submorsitans. In G. tachinoides, the trypanosome infection rates were 11, 2.6 and 13.7%, respectively, for T. brucei s.l., T. congolense forest type and T. congolense savannah type. In G. m. submorsitans, these infection rates were 16.7, 9.5 and, 2.4% respectively, for T. brucei s.l., T. congolense forest type and T. congolense savannah type. Conclusions The rate of tsetse fly infection by trypanosomes was low compared to those obtained in HAT foci of south Cameroon, and this rate was not statistically linked to the rate of symbiont occurrence. This study allowed to show for the first time the presence of Wolbachia sp. in the tsetse fly sub-species Glossina morsitans submorsitans and Glossina tachinoides.

Serendipita (=Piriformospora) indica is a fungal endophytic symbiont with the capabilities to enhance plant growth and confer resistance to different stresses. However, the application of this fungus in the field has led to inconsistent results, perhaps due to antagonism with other microbes. Here, we studied the impact of individual bacterial isolates from the endophytic bacterial community on the in vitro growth of S. indica. We further analyzed how combinations of bacteria and S. indica influence plant growth and protection against the phytopathogens Fusarium oxysporum and Rhizoctonia solani. Bacterial strains of the genera Bacillus, Enterobacter and Burkholderia negatively affected S. indica growth on plates, whereas Mycolicibacterium, Rhizobium, Paenibacillus strains and several other bacteria from different taxa stimulated fungal growth. To further explore the potential of bacteria positively interacting with S. indica, four of the most promising strains belonging to the genus Mycolicibacterium were selected for further experiments. Some dual inoculations of S. indica and Mycolicibacterium strains boosted the beneficial effects triggered by S. indica, further enhancing the growth of tomato plants, and alleviating the symptoms caused by the phytopathogens F. oxysporum and R. solani. However, some combinations of S. indica and bacteria were less effective than individual inoculations. By analyzing the genomes of the Mycolicibacterium strains, we revealed that these bacteria encode several genes predicted to be involved in the stimulation of S. indica growth, plant development and tolerance to abiotic and biotic stresses. Particularly, a high number of genes related to vitamin and nitrogen metabolism were detected. Taking into consideration multiple interactions on and inside plants, we showed in this study that some bacterial strains may induce beneficial effects on S. indica and could have an outstanding influence on the plant-fungus symbiosis.

Mutualistic root associations with arbuscular mycorrhizal (AM) fungi are known to alter interactions with insects aboveground. In this study, we investigated whether root symbiosis with Rhizophagus irregularis modulates alterations in Medicago truncatula that affect pea aphid’s (Acyrthosiphon pisum) fitness. The results indicate that aphid colony weight increased after feeding on shoots of high R. irregularis-colonized plants relative to non-mycorrhizal controls. Moreover, when given a choice, aphid adults preferred high R. irregularis-colonized plants compared to non-mycorrhizal plants. Interestingly, we identified genes strongly regulated by aphid feeding in shoots (β-1,3 glucanase, thaumatin-like protein, ethylene response factor (ERF) 1, gibberellin (GA) 20-oxidase, and GA 2-oxidase), by AM symbiosis in roots (oxo-phytodienoic acid reductase, ERF1, and GA 20-oxidase), and a gene (GA 2-oxidase) exclusively induced in roots during this tripartite interaction. Our data provide novel information about changes in plant gene expression during aphid-plant-AM fungus interactions, and serve as foundation for future transcriptome studies.

Premise: Multipartite mutualisms are widespread in nature, but population‐level variation in these interactions is rarely quantified. In the model multipartite mutualism between legumes, arbuscular mycorrhizal (AM) fungi and rhizobia bacteria, host responses to microbial partners are expected to be synergistic because the nutrients provided by each microbe colimit plant growth, but tests of this prediction have not been done in multiple host populations. Methods: To test whether plant response to associations with AM fungi and rhizobia varies among host populations and whether synergistic responses to microbial mutualists are common, we grew 34 Medicago truncatula populations in a factorial experiment that manipulated the presence or absence of each mutualist. Results: Plant growth increased in response to each mutualist, but there were no synergistic effects. Instead, plant response to inoculation with AM fungi was an order of magnitude higher than with rhizobia. Plant response to AM fungi varied among populations, whereas responses to rhizobia were relatively uniform. There was a positive correlation between plant host response to each mutualist but no correlation between AM fungal colonization and rhizobia nodulation of plant roots. Conclusions: The greater population divergence in host response to AM fungi relative to rhizobia, weak correlation in host response to each microbial mutualist, and the absence of a correlation between measures of AM fungal and rhizobia performance suggests that each plant–microbe mutualism evolved independently among M. truncatula populations. [ABSTRACT FROM AUTHOR]

Aims: Plants host communities of fungal and bacterial endophytes, establishing a complex network of multipartite interactions, but the mechanisms whereby they interact are poorly understood. Some fungi, such as the beneficial mycorrhiza-like fungus Serendipita (=Piriformospora) indica, can be helped by bacteria for establishment, survival and colonization. Although this fungus harbors a Rhizobium as an endofungal bacterium, we hypothesized that other bacteria might also establish associations with the fungus and combining S. indica with bacteria might enhance plant growth and health. Methods: The interactions among S. indica and four endophytic Proteobacteria belonging to Methylobacterium, Tardiphaga, Rhodanobacter and Trinickia spp. were characterized in vitro and for their effect on tomato growth and biocontrol of Fusarium oxysporum and Rhizoctonia solani. Possible mechanisms behind these interactions were described based on genome and microscopic analyses, using fungal and bacterial strains tagged with fluorescent markers. Results: All bacteria stimulated S. indica growth in vitro. Moreover, several of the bacteria stimulated growth of tomato plants, but co-inoculations with S. indica and bacteria did not perform better than single inoculations. Contrarily, combinations of S. indica and bacteria significantly reduced disease progression of fungal pathogens. These microbes seem to cooperate in the process of root colonization for instance by increasing fungal sporulation and hyphae expansion, showing multipartite interaction between microbes and plants. Interestingly, the strain of Trinickia internally colonizes spores of S. indica as an endofungal bacterium during in vitro-co-culturing, suggesting further that the fungus might acquire formerly unrecognized genera of bacteria and genome analysis of the bacteria revealed many genes potentially involved in fungal and plant growth stimulation, biocontrol and root colonization, highlighting putative mechanisms of plant-fungal-bacterial interaction. Conclusions: Our study represents an important step towards unraveling the complex interactions among plants, S. indica, endophytic bacteria and fungal pathogens, and indicates that adding bacteria to fungal inoculum could have a remarkable impact on the plant-S. indica symbiosis. [ABSTRACT FROM AUTHOR]

Blood-feeding enriched gut-microbiota boosts mosquitoes' anti- Plasmodium immunity. Here, we ask how Plasmodium vivax alters gut-microbiota, anti- Plasmodial immunity, and impacts tripartite Plasmodium -mosquito-microbiota interactions in the gut lumen. We used a metagenomics and RNAseq strategy to address these questions. In naïve mosquitoes, Elizabethkingia meningitis and Pseudomonas spp. are the dominant bacteria and blood-feeding leads to a heightened detection of Elizabethkingia, Pseudomonas and Serratia 16S rRNA. A parallel RNAseq analysis of blood-fed midguts also shows the presence of Elizabethkingia-related transcripts. After, P. vivax infected blood-meal, however, we do not detect bacterial 16S rRNA until circa 36 h. Intriguingly, the transcriptional expression of a selected array of antimicrobial arsenal cecropins 1–2, defensin-1, and gambicin remained low during the first 36 h—a time frame when ookinetes/early oocysts invaded the gut. We conclude during the preinvasive phase, P. vivax outcompetes midgut-microbiota. This microbial suppression likely negates the impact of mosquito immunity which in turn may enhance the survival of P. vivax. Detection of sequences matching to mosquito-associated Wolbachia opens a new inquiry for its exploration as an agent for "paratransgenesis-based" mosquito control. [ABSTRACT FROM AUTHOR]

Planorbidae snails are the intermediate host for the trematode parasite of the Schistosoma genus, which is responsible for schistosomiasis, a disease that affects both humans and cattle. The microbiota for Schistosoma has already been described as having an effect on host/parasite interactions, specifically through immunological interactions. Here, we sought to characterize the microbiota composition of seven Planorbidae species and strains. Individual snail microbiota was determined using 16S ribosomal DNA amplicon sequencing. The bacterial composition was highly specific to the host strain with limited interindividual variation. In addition, it displayed complete congruence with host phylogeny, revealing a phylosymbiosis pattern. These results were confirmed in a common garden, suggesting that the host highly constrains microbial composition. This study presents the first comparison of bacterial communities between several intermediate snail hosts of Schistosoma parasites, paving the way for further studies on the understanding of this tripartite interaction. [ABSTRACT FROM AUTHOR]

Serendipita (= Piriformospora) indica is a fungal endophytic symbiont with the capabilities to enhance plant growth and confer resistance to different stresses. However, the application of this fungus in the field has led to inconsistent results, perhaps due to antagonism with other microbes. Here, we studied the impact of individual bacterial isolates from the endophytic bacterial community on the in vitro growth of S. indica. We further analyzed how combinations of bacteria and S. indica influence plant growth and protection against the phytopathogens Fusarium oxysporum and Rhizoctonia solani. Bacterial strains of the genera Bacillus, Enterobacter and Burkholderia negatively affected S. indica growth on plates, whereas Mycolicibacterium, Rhizobium, Paenibacillus strains and several other bacteria from different taxa stimulated fungal growth. To further explore the potential of bacteria positively interacting with S. indica , four of the most promising strains belonging to the genus Mycolicibacterium were selected for further experiments. Some dual inoculations of S. indica and Mycolicibacterium strains boosted the beneficial effects triggered by S. indica , further enhancing the growth of tomato plants, and alleviating the symptoms caused by the phytopathogens F. oxysporum and R. solani. However, some combinations of S. indica and bacteria were less effective than individual inoculations. By analyzing the genomes of the Mycolicibacterium strains, we revealed that these bacteria encode several genes predicted to be involved in the stimulation of S. indica growth, plant development and tolerance to abiotic and biotic stresses. Particularly, a high number of genes related to vitamin and nitrogen metabolism were detected. Taking into consideration multiple interactions on and inside plants, we showed in this study that some bacterial strains may induce beneficial effects on S. indica and could have an outstanding influence on the plant-fungus symbiosis. [ABSTRACT FROM AUTHOR]

The main selective force driving floral evolution and diversity is plant–pollinator interactions. Pollinators use floral signals and indirect cues to assess flower reward, and the ensuing flower choice has major implications for plant fitness. While many pollinator behaviors have been described, the impact of parasites on pollinator foraging decisions and plant–pollinator interactions have been largely overlooked. Growing evidence of the transmission of parasites through the shared‐use of flowers by pollinators demonstrate the importance of behavioral immunity (altered behaviors that enhance parasite resistance) to pollinator health. During foraging bouts, pollinators can protect themselves against parasites through self‐medication, disease avoidance, and grooming. Recent studies have documented immune behaviors in foraging pollinators, as well as the impacts of such behaviors on flower visitation. Because pollinator parasites can affect flower choice and pollen dispersal, they may ultimately impact flower fitness. Here, we discuss how pollinator immune behaviors and floral traits may affect the presence and transmission of pollinator parasites, as well as how pollinator parasites, through these immune behaviors, can impact plant–pollinator interactions. We further discuss how pollinator immune behaviors can impact plant fitness, and how floral traits may adapt to optimize plant fitness in response to pollinator parasites. We propose future research directions to assess the role of pollinator parasites in plant–pollinator interactions and evolution, and we propose better integration of the role of pollinator parasites into research related to pollinator optimal foraging theory, floral diversity and agricultural practices. [ABSTRACT FROM AUTHOR]

Interactions between ecological communities of herbivores and microbes are commonly mediated by a shared plant. A tripartite interaction between a pathogenic fungus–host plant–herbivorous insect is an example of such mutual influences. In such a system a fungal pathogen commonly has a negative influence on the morphology and biochemistry of the host plant, with consequences for insect herbivore performance. Here we studied whether the biotrophic fungus Podosphaera ferruginea, attacking the great burnet Sanguisorba officinalis, affects caterpillar performance of the endangered scarce large blue butterfly Phengaris teleius. Our results showed that the pathogenic fungus affected the number and size of inflorescences produced by food‐plants and, more importantly, had indirect, plant‐mediated effects on the abundance, body mass and immune response of caterpillars. Specifically, we found the relationship between caterpillar abundance and variability in inflorescence size on a plant to be positive among healthy food‐plants, and negative among infected food‐plants. Caterpillars that fed on healthy food‐plants were smaller than those that fed on infected food‐plants in one studied season, while there was no such difference in the other season. We observed the relationship between caterpillar immune response and the proportion of infected great burnets within a habitat patch to be positive when caterpillars fed on healthy food‐plants, and negative when caterpillars fed on infected food‐plants. Our results suggest that this biotrophic fungal infection of the great burnet may impose a significant indirect influence on P. teleius caterpillar performance with potential consequences for the population dynamics and structure of this endangered butterfly. [ABSTRACT FROM AUTHOR]

Abstract Many floral traits have evolved through pollinator-mediated selection. In selecting flowers for forage, pollinators rely on multi-modal flower signals and innate preferences. However, pollinators are known for their flexible foraging behavior which varies with experience and numerous cues, such as the presence of competitors and floral resource availability. The shared use of flowers by many pollinators leads to high rate of parasite transmission among pollinators, and flowers can be seen as hot-spots of parasite dispersal. Throughout the animal kingdom, behavioral adaptations enable avoidance of parasite exposure. Bumblebees are known to avoid contaminated flowers, however nothing is known regarding the impact of parasite presence on overall pollinator visitation. In this study, we measured the effect of a larval honey bee parasite, the fungus Ascosphaera apis causing chalkbrood disease, on hymenopteran pollinator visitation of several plant species in a natural setting. Several contaminated flowering plant species suffered not only the subsequent reduction of visitation by honey bees but also the subsequent reduction of their overall pollinator visitation. Two plant species with similar flower architecture were the least impacted by the presence of the spores. This study highlights the negative impact of the presence of pollinator parasites for plants and its possible consequences for floral evolution. Graphical abstract Image 1 Highlights • The shared-use of flowers by pollinators play an important role in the transmission of pollinator parasites. • Pollinators tend to avoid flowers bearing parasites. • The presence of honey bee larval fungal disease on an inflorescence may lead to the reduction of pollinator visitation. • The avoidance of contaminated inflorescence seems to depend simultaneously on the pollinator genus and the plant species. [ABSTRACT FROM AUTHOR]

Mutualistic root associations with arbuscular mycorrhizal (AM) fungi are known to alter interactions with insects aboveground. In this study, we investigated whether root symbiosis with Rhizophagus irregularis modulates alterations in Medicago truncatula that affect pea aphid's (Acyrthosiphon pisum) fitness. The results indicate that aphid colony weight increased after feeding on shoots of high R. irregularis-colonized plants relative to non-mycorrhizal controls. Moreover, when given a choice, aphid adults preferred high R. irregularis-colonized plants compared to non-mycorrhizal plants. Interestingly, we identified genes strongly regulated by aphid feeding in shoots (β-1,3 glucanase, thaumatin-like protein, ethylene response factor (ERF) 1, gibberellin (GA) 20-oxidase, and GA 2-oxidase), by AM symbiosis in roots (oxo-phytodienoic acid reductase, ERF1, and GA 20-oxidase), and a gene (GA 2-oxidase) exclusively induced in roots during this tripartite interaction. Our data provide novel information about changes in plant gene expression during aphid-plant-AM fungus interactions, and serve as foundation for future transcriptome studies. [ABSTRACT FROM AUTHOR]

Understanding the intricate interplay between the gut microbiota and the immune response in insects is crucial, given its diverse impact on the pathogenesis of various microbial species. The microbiota's modulation of the host immune system is one such mechanism, although its complete impact on immune responses remains elusive. This study investigated the tripartite interaction between the gut microbiota, pathogens, and the host's response in Galleria mellonella larvae reared under axenic (sterile) and conventional (non-sterile) conditions. The influence of the microbiota on host fitness during infections was evaluated via two different routes: oral infection induced by Bacillus thuringiensis subsp. galleriae ( Btg ), and topical infection induced by Metarhizium robertsii ( Mr ). We observed that larvae without a microbiota can successfully fulfill their life cycle, albeit with more variation in their developmental time. We subsequently performed survival assays on final-instar larvae, using the median lethal dose (LD 50 ) of Btg and Mr . Our findings indicated that axenic larvae were more vulnerable to an oral infection of Btg ; specifically, a dose that was calculated to be half-lethal for the conventional group resulted in a 90%-100% mortality rate in the axenic group. Through a dual-analysis experimental design, we could identify the status of the gut microbiota using 16S rRNA sequencing and assess the level of immune-related gene expression in the same group of larvae at basal conditions and during infection. This analysis revealed that the microbiota of our conventionally reared population was dominated entirely by four Enterococcus species, and these species potentially stimulated the immune response in the gut, due to the increased basal expression of two antimicrobial peptides (AMPs)-gallerimycin and gloverin-in the conventional larvae compared with the axenic larvae. Furthermore, Enterococcus mundtii , isolated from the gut of conventional larvae, showed inhibition activity against Btg in vitro . Lastly, other immune effectors, namely, phenoloxidase activity in the hemolymph and total reactive oxygen/nitrogen species (ROS/RNS) in the gut, were tested to further investigate the extent of the stimulation of the microbiota on the immune response. These findings highlight the immune-modulatory role of the Enterococcus- dominated gut microbiota, an increasingly reported microbiota assemblage of laboratory populations of Lepidoptera, and its influence on the host's response to oral and topical infections., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2023 Upfold, Rejasse, Nielsen-Leroux, Jensen and Sanchis-Borja.)

In Europe, the most widely used Christmas tree species, Abies nordmanniana, has a long history of infestation with the adelgid Dreyfusia nordmannianae . Since 2011, the species has furthermore been increasingly damaged by the fungus Neonectria neomacrospora . The objective was to study whether infestations by N. neomacrospora were facilitated by the presence of adelgids in Nordmann fir and to explore the genetic components of this potential interplay. The damage caused by D. nordmannianae and N. neomacrospora in two Nordmann fir clonal seed orchards in Denmark was evaluated in 2014, and an experimental infestation was conducted to test the performance of Nordmann fir somatic embryogenesis-derived trees exposed to N. neomacrospora and D. nordmannianae individually or in combination by setting up an artificial infestation chamber. The genetic correlation between the two diseases was 0.54 at two clonal seed orchards, indicating that the trees susceptible to N. neomacrospora were also susceptible to D. nordmannianae or vice versa. In the experimental test, only trees in the treatment with both D. nordmannianae and N. neomacrospora developed needle loss and dieback symptoms. Thus, both the field evaluations and the experimental test revealed an interplay between D. nordmannianae and N. neomacrospora damage on Nordmann fir trees. Future studies should explore in more detail how D. nordmannianae interacts with N. neomacrospora . Our findings and future studies on this topic could have important implications for suitable breeding programs for Nordmann fir Christmas trees and forest pest management. [ABSTRACT FROM AUTHOR]

Abstract: Although insect herbivores and fungal pathogens frequently share the same individual host plant, we lack general insights in how fungal infection affects insect preference and performance. We addressed this question in a meta‐analysis of 1,113 case studies gathered from 101 primary papers that compared preference or performance of insect herbivores on control vs. fungus challenged plants. Generally, insects preferred, and performed better on, not challenged plants, regardless of experimental conditions. Insect response to fungus infection significantly differed according to fungus lifestyle, insect feeding guild, and the spatial scale of the interaction (local/distant). Insect performance was reduced on plants challenged by biotrophic pathogens or endophytes but not by necrotrophic pathogens. For both chewing and piercing‐sucking insects, performance was reduced on challenged plants when interactions occurred locally but not distantly. In plants challenged by biotrophic pathogens, both preference and performance of herbivores were negatively impacted, whereas infection by necrotrophic pathogens reduced herbivore preference more than performance and endophyte infection reduced only herbivore performance. Our study demonstrates that fungi could be important but hitherto overlooked drivers of plant‐herbivore interactions, suggesting both direct and plant‐mediated effects of fungi on insect's behavior and development. [ABSTRACT FROM AUTHOR]

Plants engage in complex multipartite interactions with mutualists and antagonists, but these interactions are rarely included in studies that explore plant invasiveness. When considered in isolation, we know that beneficial microbes can enhance an exotic plant's invasive ability and that herbivorous insects often decrease an exotic plant's likeliness of success. However, the effect of these partners on plant fitness has not been well characterized when all three species coevolve. We use computational evolutionary modeling of a trait-based system to test how microbes and herbivores simultaneously coevolving with an invading plant affect the invaders' probability of becoming established. Specifically, we designed a model that explores how a beneficial microbe would influence the outcome of an interaction between a plant and herbivore. To model novel interactions, we included a phenotypic trait shared by each species. Making this trait continuous and selectable allows us to explore how trait similarities between coevolving plants, herbivores and microbes affect fitness. Using this model, we answer the following questions: (1) Can a beneficial plant-microbe interaction influence the evolutionary outcome of antagonistic interactions between plants and herbivores? (2) How does the initial trait similarity between interacting organisms affect the likelihood of plant survival in novel locations? (3) Does the effect of tripartite interactions on the invasion success of a plant depend on whether organisms interact through trait similarity [Enemy Release Hypothesis (ERH)] or dissimilarity (Biotic Resistance Hypothesis)? We found that it was much more difficult for plants to invade under the ERH but that beneficial microbes increase the probability of plant survival in a novel range under both hypotheses. To our knowledge, this model is the first to use tripartite interactions to explore novel species introductions. It represents a step towards gaining a better understanding of the factors influencing establishment of exotic species to prevent future invasions. [ABSTRACT FROM AUTHOR]

Bacteria, ectomycorrhizal (EcM) fungi, and land plants have been coevolving for nearly 200 million years, and their interactions presumably contribute to the function of terrestrial ecosystems. The direction, stability, and strength of bacteria-EcM fungi interactions across landscapes and across a single plant host, however, remains unclear. Moreover, the genetic mechanisms that govern them have not been addressed. To these ends, we collected soil samples from Bishop pine forests across a climate-latitude gradient spanning coastal California, fractionated the soil samples based on their proximity to EcM-colonized roots, characterized the microbial communities using amplicon sequencing, and generated linear regression models showing the impact that select bacterial taxa have on EcM fungal abundance. In addition, we paired greenhouse experiments with transcriptomic analyses to determine the directionality of these relationships and identify which genes EcM-synergist bacteria express during tripartite symbioses. Our data reveal that ectomycorrhizas (i.e., EcM-colonized roots) enrich conserved bacterial taxa across climatically heterogeneous regions. We also show that phylogenetically diverse EcM synergists are positively associated with plant and fungal growth and have unique gene expression profiles compared with EcM-antagonist bacteria. In sum, we identify common mechanisms that facilitate widespread and diverse multipartite symbioses, which inform our understanding of how plants develop in complex environments. [Display omitted] • Ectomycorrhizas select a small group of bacteria across a climate-latitude gradient • Positive bacteria-ectomycorrhiza interactions are linked to plant and fungal growth • Cytokinin and betalain biosynthesis may drive bacteria-ectomycorrhiza relationships Berrios et al. combine large-scale environmental sampling efforts and small-scale plant growth experiments to capture the direction, strength, and stability of bacteria-ectomycorrhiza interactions across landscape scales. These analyses suggest that multipartite interactions are a rule and not an exception in plant microbiomes. [ABSTRACT FROM AUTHOR]

Soilborne fungal and oomycete pathogens are the causal agents of several important plant diseases. Infection frequently co-occurs with herbivory by root-feeding insects, facilitating tripartite interactions that modify plant performance and mortality. In an agricultural context, interactions between pathogens, herbivores, and plants can have important consequences for yield protection. However, belowground interactions are inherently difficult to observe and are often overlooked. Here, we review the impact of direct and indirect interactions between root-associated insects, fungi, and oomycetes on the development of plant disease. We explore the relationship between insect feeding injury and pathogen infection, as well as the role of insects as vectors of fungal and oomycete pathogens. Synergistic interactions between insects and phytopathogens may be important in weed suppression, and we highlight several promising candidates for biocontrol. Bridging the gap between entomological and pathological research is a critical step in understanding how interactions between insects and microorganisms modify the community structure of the rhizosphere, and how this impacts plant functioning. Furthermore, the identification of belowground interactions is required to develop effective pest monitoring and management strategies. [ABSTRACT FROM AUTHOR]

Many host-plants exhibit genetic variation in resistance to pathogens; however, little is known about the extent to which genetic variation in pathogen resistance influences other members of the host-plant community, especially arthropods at higher trophic levels. We addressed this knowledge gap by using a common garden experiment to examine whether genotypes of Populus trichocarpa varied in resistance to a leaf-blistering pathogen, Taphrina sp., and in the density of web-building spiders, the dominant group of predatory arthropods. In addition, we examined whether variation in spider density was explained by variation in the density and size of leaf blisters caused by Taphrina. We found that P. trichocarpa genotypes exhibited strong differences in their resistance to Taphrina and that P. trichocarpa genotypes that were more susceptible to Taphrina supported more web-building spiders, the dominant group of predatory arthropods. We suspect that this result is caused by blisters increasing the availability of suitable habitat for predators, and not due to variation in herbivores because including herbivore density as a covariate did not affect our models. Our study highlights a novel pathway by which genetic variation in pathogen resistance may affect higher trophic levels in arthropod communities. [ABSTRACT FROM AUTHOR]

The unicellular pathogenic protozoan Trypanosoma brucei gambiense is responsible for the chronic form of sleeping sickness. This vector-borne disease is transmitted to humans by the tsetse fly of the group Glossina palpalis, including the subspecies G. p. gambiensis, in which the parasite completes its developmental cycle. Sleeping sickness control strategies can therefore target either the human host or the fly vector. Indeed, suppression of one step in the parasite developmental cycle could abolish parasite transmission to humans, with consequences on the spreading of the disease. In order to develop this type of approach, we have identified, at the proteome level, events resulting from the tripartite interaction between the tsetse fly G. p. gambiensis, its microbiome, and the trypanosome. Proteomes were analyzed from four biological replicates of midguts from flies sampled three days post-feeding on either a trypanosome-infected (stimulated flies) or a non-infected (non-stimulated flies) bloodmeal. Over 500 proteins were identified in the midguts of flies from both feeding groups, thirteen of which were shown to be differentially expressed in trypanosome-stimulated versus non-stimulated flies. Functional annotation revealed that several of these proteins have important functions that could be involved in modulating the fly infection process by trypanosomes (and thus fly vector competence), including anti-oxidant and anti-apoptotic, cellular detoxifying, trypanosome agglutination, and immune stimulating or depressive effects. The results show a strong potential for diminishing or even disrupting fly vector competence, and their application holds great promise for improving the control of sleeping sickness.

Tsetse flies (Glossina sp.) that transmit trypanosomes causing human (and animal) African trypanosomiasis (HAT and AAT, respectively) harbor symbiotic microorganisms, including the obligate primary symbiont Wigglesworthia glossinidia. A relationship between Wigglesworthia and tsetse fly infection by trypanosomes has been suggested, as removal of the symbiont results in a higher susceptibility to midgut infection in adult flies. To investigate this relationship and to decipher the role of W. glossinidia in the fly's susceptibility to trypanosome infection, we challenged flies with trypanosomes and subsequently analyzed and compared the transcriptomes of W. glossinidia from susceptible and refractory tsetse flies at three time points (3, 10, and 20 days). More than 200 W. glossinidia genes were found to be differentially expressed between susceptible and refractory flies. The high specificity of these differentially expressed genes makes it possible to distinguish Wigglesworthia inhabiting these two distinct groups of flies. Furthermore, gene expression patterns were observed to evolve during the infection time course, such that very few differentially expressed genes were found in common in Wigglesworthia from the 3-, 10- and 20-day post-feeding fly samples.The overall results clearly demonstrate that the taking up of trypanosomes by flies, regardless of whether flies proceed with the developmental program of Trypanosoma brucei gambiense, strongly alters gene expression in Wigglesworthia. These results therefore provide a novel framework for studies that aim to decrease or even abolish tsetse fly vector competence.

Sodalis glossinidius, one of the three tsetse fly maternally inherited symbionts, was previously shown to favor fly infection by trypanosomes, the parasites causing human sleeping sickness. Among a population of flies taking a trypanosome-infected blood meal, only a few individuals will acquire the parasite; the others will escape infection and be considered as refractory to trypanosome infection. The aim of the work was to investigate whether fly refractoriness could be associated with specific Sodalis gene expression. The transcriptome of S. glossinidius harbored by flies that were fed either with a noninfected blood meal (control) or with a trypanosome-infected meal but that did not develop infection were analyzed, using microarray technology, and compared. The analysis using the microarray procedure yielded 17 genes that were found to have a significant differential expression between the two groups. Interestingly, all these genes were overexpressed in self-cured (refractory) flies. Further analysis of functional annotation of these genes indicated that most associated biological process terms were related to metabolic and biosynthetic processes as well as to oxido-reduction mechanisms. These results evidence the occurrence of molecular crosstalk between the different partners, induced by the passage of the trypanosomes through the fly’s gut even though the parasites were unable to establish in the gut and to develop a permanent infection.

he unicellular pathogenic protozoan Trypanosoma brucei gambiense is responsible for the chronic form of sleeping sickness. This vector-borne disease is transmitted to humans by the tsetse fly of the group Glossina palpalis, including the subspecies G. p. gambiensis, in which the parasite completes its developmental cycle. Sleeping sickness control strategies can therefore target either the human host or the fly vector. Indeed, suppression of one step in the parasite developmental cycle could abolish parasite transmission to humans, with consequences on the spreading of the disease. In order to develop this type of approach, we have identified, at the proteome level, events resulting from the tripartite interaction between the tsetse fly G. p. gambiensis, its microbiome, and the trypanosome. Proteomes were analyzed from four biological replicates of midguts from flies sampled 3 days post-feeding on either a trypanosome-infected (stimulated flies) or a non-infected (non-stimulated flies) bloodmeal. Over 500 proteins were identified in the midguts of flies from both feeding groups, 13 of which were shown to be differentially expressed in trypanosome-stimulated vs. non-stimulated flies. Functional annotation revealed that several of these proteins have important functions that could be involved in modulating the fly infection process by trypanosomes (and thus fly vector competence), including anti-oxidant and anti-apoptotic, cellular detoxifying, trypanosome agglutination, and immune stimulating or depressive effects. The results show a strong potential for diminishing or even disrupting fly vector competence, and their application holds great promise for improving the control of sleeping sickness. [ABSTRACT FROM AUTHOR]