Global insights into endophytic bacterial communities of terrestrial plants: Exploring the potential applications of endophytic microbiota in sustainable agriculture.

Endophytic microorganisms are indispensable symbionts during plant growth and development and often serve functions such as growth promotion and stress resistance in plants. Therefore, an increasing number of researchers have applied endophytes for multifaceted phytoremediation (e.g., organic pollutants and heavy metals) in recent years. With the availability of next-generation sequencing technologies, an increasing number of studies have shifted the focus from culturable bacteria to total communities. However, information on the composition, structure, and function of bacterial endophytic communities is still not widely synthesized. To explore the general patterns of variation in bacterial communities between plant niches, we reanalyzed data from 1499 samples in 30 individual studies from different continents and provided comprehensive insights. A group of bacterial genera were commonly found in most plant roots and shoots. Our analysis revealed distinct variations in the diversity, composition, structure, and function of endophytic bacterial communities between plant roots and shoots. These variations underscore the sophisticated mechanisms by which plants engage with their endophytic microbiota, optimizing these interactions to bolster growth, health, and resilience against stress. Highlighting the strategic role of endophytic bacteria in promoting sustainable agricultural practices and environmental stewardship, our study not only offers global insights into the endophytic bacterial communities of terrestrial plants but also underscores the untapped potential of these communities as invaluable resources for future research.

Interactions between Epichloë endophyte and the plant microbiome impact nitrogen responses in host Achnatherum inebrians plants.

The clavicipitaceous fungus Epichloë gansuensis forms symbiotic associations with drunken horse grass (Achnatherum inebrians), providing biotic and abiotic stress protection to its host. However, it is unclear how E. gansuensis affects the assembly of host plant-associated bacterial communities after ammonium nitrogen (NH4+-N) treatment. We examined the shoot- and root-associated bacterial microbiota and root metabolites of A. inebrians when infected (I) or uninfected (F) with E. gansuensis endophyte. The results showed more pronounced NH4+-N-induced microbial and metabolic changes in the endophyte-infected plants compared to the endophyte-free plants. E. gansuensis significantly altered bacterial community composition and ß-diversity in shoots and roots and increased bacterial α-diversity under NH4+-N treatment. The relative abundance of 117 and 157 root metabolites significantly changed with E. gansuensis infection under water and NH4+-N treatment compared to endophyte-free plants. Root bacterial community composition was significantly related to the abundance of the top 30 metabolites [variable importance in the projection (VIP) > 2 and VIP > 3] contributing to differences between I and F plants, especially alkaloids. The correlation network between root microbiome and metabolites was complex. Microorganisms in the Proteobacteria and Firmicutes phyla were significantly associated with the R00693 metabolic reaction of cysteine and methionine metabolism. Co-metabolism network analysis revealed common metabolites between host plants and microorganisms.IMPORTANCEOur results suggest that the effect of endophyte infection is sensitive to nitrogen availability. Endophyte symbiosis altered the composition of shoot and root bacterial communities, increasing bacterial diversity. There was also a change in the class and relative abundance of metabolites. We found a complex co-occurrence network between root microorganisms and metabolites, with some metabolites shared between the host plant and its microbiome. The precise ecological function of the metabolites produced in response to endophyte infection remains unknown. However, some of these compounds may facilitate plant-microbe symbiosis by increasing the uptake of beneficial soil bacteria into plant tissues. Overall, these findings advance our understanding of the interactions between the microbiome, metabolome, and endophyte symbiosis in grasses. The results provide critical insight into the mechanisms by which the plant microbiome responds to nutrient stress in the presence of fungal endophytes.

Plant-endophyte communication: Scaling from molecular mechanisms to ecological outcomes.

Diverse communities of fungal endophytes reside in plant tissues, where they affect and are affected by plant physiology and ecology. For these intimate interactions to form and persist, endophytes and their host plants engage in intricate systems of communication. The conversation between fungal endophytes and plant hosts ultimately dictates endophyte community composition and function and has cascading effects on plant health and plant interactions. In this review, we synthesize our current knowledge on the mechanisms and strategies of communication used by endophytic fungi and their plant hosts. We discuss the molecular mechanisms of communication that lead to organ specificity of endophytic communities and distinguish endophytes, pathogens, and saprotrophs. We conclude by offering emerging perspectives on the relevance of plant-endophyte communication to microbial community ecology and plant health and function.

Anti-herbivory defences delivered by Epichloë fungal endophytes: a quantitative review of alkaloid concentration variation among hosts and plant parts.

BACKGROUND AND AIMS: In the subfamily Poöideae (Poaceae), certain grass species possess anti-herbivore alkaloids synthesized by fungal endophytes that belong to the genus Epichloë (Clavicipitaceae). The protective role of these symbiotic endophytes can vary, depending on alkaloid concentrations within specific plant-endophyte associations and plant parts. METHODS: We conducted a literature review to identify articles containing alkaloid concentration data for various plant parts in six important pasture species, Lolium arundinaceum, Lolium perenne, Lolium pratense, Lolium multiflorum|Lolium rigidum and Festuca rubra, associated with their common endophytes. We considered the alkaloids lolines (1-aminopyrrolizidines), peramine (pyrrolopyrazines), ergovaline (ergot alkaloids) and lolitrem B (indole-diterpenes). While all these alkaloids have shown bioactivity against insect herbivores, ergovaline and lolitrem B are harmful for mammals. KEY RESULTS: Loline alkaloid levels were higher in the perennial grasses L. pratense and L. arundinaceum compared to the annual species L. multiflorum and L. rigidum, and higher in reproductive tissues than in vegetative structures. This is probably due to the greater biomass accumulation in perennial species that can result in higher endophyte mycelial biomass. Peramine concentrations were higher in L. perenne than in L. arundinaceum and not affected by plant part. This can be attributed to the high within-plant mobility of peramine. Ergovaline and lolitrem B, both hydrophobic compounds, were associated with plant parts where fungal mycelium is usually present, and their concentrations were higher in plant reproductive tissues. Only loline alkaloid data were sufficient for below-ground tissue analyses and concentrations were lower than in above-ground parts. CONCLUSIONS: Our study provides a comprehensive synthesis of fungal alkaloid variation across host grasses and plant parts, essential for understanding the endophyte-conferred defence extent. The patterns can be understood by considering endophyte growth within the plant and alkaloid mobility. Our study identifies research gaps, including the limited documentation of alkaloid presence in roots and the need to investigate the influence of different environmental conditions.

Environmental drivers and cryptic biodiversity hotspots define endophytes in Earth's largest terrestrial biome.

Understanding how symbiotic associations differ across environmental gradients is key to predicting the fate of symbioses as environments change, and it is vital for detecting global reservoirs of symbiont biodiversity in a changing world.1,2,3 However, sampling of symbiotic partners at the full-biome scale is difficult and rare. As Earth's largest terrestrial biome, boreal forests influence carbon dynamics and climate regulation at a planetary scale. Plants and lichens in this biome host the highest known phylogenetic diversity of fungal endophytes, which occur within healthy photosynthetic tissues and can influence hosts' resilience to stress.4,5 We examined how communities of endophytes are structured across the climate gradient of the boreal biome, focusing on the dominant plant and lichen species occurring across the entire south-to-north span of the boreal zone in eastern North America. Although often invoked for understanding the distribution of biodiversity, neither a latitudinal gradient nor mid-domain effect5,6,7 can explain variation in endophyte diversity at this trans-biome scale. Instead, analyses considering shifts in forest characteristics, Picea biomass and age, and nutrients in host tissues from 46° to 58° N reveal strong and distinctive signatures of climate in defining endophyte assemblages in each host lineage. Host breadth of endophytes varies with climate factors, and biodiversity hotspots can be identified at plant-community transitions across the boreal zone at a global scale. Placed against a backdrop of global circumboreal sampling,4 our study reveals the sensitivity of endophytic fungi, their reservoirs of biodiversity, and their important symbiotic associations, to climate.

Response of tomatoes to inactivated endophyte LSE01 under combined stress of high-temperature and drought.

Endophytes can assist crops in adapting to high temperatures and drought conditions, thereby reducing agricultural losses. However, the mechanism through which endophytes regulate crop resistance to high temperatures and drought stress remains unclear, and concerns regarding safety and stability exist with active endophytes. Thus, heat-treated endophytic bacteria LSE01 (HTB) were employed as a novel microbial fertilizer to investigate their effects on plant adaptation to high temperatures and drought conditions. The results indicated that the diameter and weight of tomatoes treated with HTB under stress conditions increased by 23.04% and 71.15%, respectively, compared to the control. Tomato yield did not significantly decrease compared to non-stress conditions. Additionally, the contents of vitamin C, soluble sugars, and proteins treated with HTB increased by 18.81%, 11.54%, and 99.75%, respectively. Mechanistic research revealed that HTB treatment enhances tomato's stress resistance by elevating photosynthetic pigment and proline contents, enhancing antioxidant enzyme activities, and reducing the accumulation of MDA. Molecular biology research demonstrates that HTB treatment upregulates the expression of drought-resistant genes (GA2ox7, USP1, SlNAC3, SlNAC4), leading to modifications in stomatal conductance, plant morphology, photosynthetic intensity, and antioxidant enzyme synthesis to facilitate adaptation to dry conditions. Furthermore, the upregulation of the heat-resistant gene (SlCathB2-2) can increases the thickness of tomato cell walls, rendering them less vulnerable to heat stress. In summary, HTB endows tomatoes with the ability to adapt to high temperatures and drought conditions, providing new opportunities for sustainable agriculture.

Deciphering the interaction of bacteria inoculants with the recipient endophytic community in grapevine micropropagated plants.

Engineering the plant microbiome with beneficial endophytic bacteria can improve the growth, health, and productivity of the holobiont. Here, we administered two beneficial bacterial strains, Kosakonia VR04 sp. and Rhizobium GR12 sp., to micropropagated grapevine cuttings obtained via somatic embryogenesis. While both strains colonized the plant endosphere, only Rhizobium GR12 sp. increased root biomass under nutritional-deficit conditions, as supported by the plant growth promotion traits detected in its genome. Phylogenetic and co-occurrence analyses revealed that the plant native bacterial community, originally dominated by Streptococcaceae and Micrococcaceae, dramatically changed depending on the inoculation treatments, as invading strains differently affected the relative abundance and the interactions of pre-existing taxa. After 30 days of plantlets' growth, Pantoea became a predominant taxon, and considering untreated plantlets as references, Rhizobium sp. GR12 showed a minor impact on the endophytic bacterial community. On the other hand, Kosakonia sp. VR04 caused a major change in community composition, suggesting an opportunistic colonization pattern. Overall, the results corroborate the importance of preserving the native endophytic community structure and functions during plant microbiome engineering.IMPORTANCEA better comprehension of bacterial colonization processes and outcomes could benefit the use of plant probiotics in the field. In this study, we applied two different beneficial bacteria to grapevine micropropagated plantlets and described how the inoculation of these strains impacts endophytic microbiota assembly. We showed that under nutritional deficit conditions, the response of the receiving endophytic bacterial communities to the invasion of the beneficial strains related to the manifestation of plant growth promotion effects by the inoculated invading strains. Rhizobium sp. GR12 was able to preserve the native microbiome structure despite its effective colonization, highlighting the importance of the plant-endophyte associations for the holobiont performance. Moreover, our approach showed that the use of micropropagated plantlets could be a valuable strategy to study the interplay among the plant, its native microbiota, and the invader on a wider portfolio of species besides model plants, facilitating the application of new knowledge in agriculture.

Endophytic fungi: Unravelling plant-endophyte interaction and the multifaceted role of fungal endophytes in stress amelioration.

Endophytic fungi colonize interior plant tissue and mostly form mutualistic associations with their host plant. Plant-endophyte interaction is a complex mechanism and is currently a focus of research to understand the underlying mechanism of endophyte asymptomatic colonization, the process of evading plant immune response, modulation of gene expression, and establishment of a balanced mutualistic relationship. Fungal endophytes rely on plant hosts for nutrients, shelter, and transmission and improve the host plant's tolerance against biotic stresses, including -herbivores, nematodes, bacterial, fungal, viral, nematode, and other phytopathogens. Endophytic fungi have been reported to improve plant health by reducing and eradicating the harmful effect of phytopathogens through competition for space or nutrients, mycoparasitism, and through direct or indirect defense systems by producing secondary metabolites as well as by induced systemic resistance (ISR). Additionally, for efficient crop improvement, practicing them would be a fruitful step for a sustainable approach. This review article summarizes the current research progress in plant-endophyte interaction and the fungal endophyte mechanism to overcome host defense responses, their subsequent colonization, and the establishment of a balanced mutualistic interaction with host plants. This review also highlighted the potential of fungal endophytes in the amelioration of biotic stress. We have also discussed the relevance of various bioactive compounds possessing antimicrobial potential against a variety of agricultural pathogens. Furthermore, endophyte-mediated ISR is also emphasized.

Eliciting transcriptomic and antioxidant defensive responses against Rhizoctonia root rot of sorghum using the endophyte Aspergillus oryzae YRA3.

Environmental pollution due to the improper use of the chemical fungicides represents a vital ecological problem, which affects human and animal health, as well as the microbial biodiversity and abundance in the soil. In this study, an endophytic fungus Aspergillus oryzae YRA3, isolated from the wild plant Atractylis carduus (Forssk.) C.Chr, was tested for its biocontrol activity against Rhizoctonia root rot of sorghum. The antagonistic potential of A. oryzae YRA3 was tested against Rhizoctonia solani in vitro. A full inhibition in the growth of R. solani was recorded indicating a strong antagonistic potential for this endophyte. To investigate the chemical composition of its metabolites, GC/MS analysis was used and thirty-two compounds in its culture filtrate were identified. Among these metabolites, some compounds with an antifungal background were detected including palmitic acid, 2-heptanone, and 2,3-butanediol. To these antifungal metabolites the antagonistic activity of A. oryzae YRA3 can be attributed. In the greenhouse experiment, treating of the infected sorghum plants with A. oryzae YRA3 significantly reduced severity of the Rhizoctonia root rot by 73.4%. An upregulation of the defensive genes (JERF3), (POD) and (CHI II) was recorded in sorghum roots when were inoculated with A. oryzae YRA3. In addition, an increment in the activity of peroxidase and polyphenol oxidase, as well as the total phenolic content in the sorghum roots was also recorded. Furthermore, the results obtained from the greenhouse experiment revealed a growth-promoting effect for inoculating the sorghum plants with A. oryzae YRA3. It can be concluded that A. oryzae YRA3 can be a probable biological agent to control this disease in sorghum. However, its evaluation under field conditions is highly needed in the future studies.

Plant and microbial features governing an endophytic lifestyle.

Beneficial microorganisms colonizing internal plant tissues, the endophytes, support their host through plant growth promotion, pathogen protection, and abiotic stress alleviation. Their efficient application in agriculture requires the understanding of the molecular mechanisms and environmental conditions that facilitate in planta accommodation. Accumulating evidence reveals that commensal microorganisms employ similar colonization strategies as their pathogenic counterparts. Fine-tuning of immune response, motility, and metabolic crosstalk accounts for their differentiation. For a holistic perspective, in planta experiments with microbial collections and comprehensive genome data exploration are crucial. This review describes the most recent findings on factors involved in endophytic colonization processes, focusing on bacteria and fungi, and discusses required methodological approaches to unravel their relevance within a community context.

Native plants change the endophyte assembly and growth of an invasive plant in response to climatic factors.

Climate change, microbial endophytes, and local plants can affect the establishment and expansion of invasive species, yet no study has been performed to assess these interactions. Using a growth chamber, we integrated the belowground (rhizosphere soils) and aboveground (mixture of mature leaf and leaf litter) microbiota into an experimental framework to evaluate the impacts of four native plants acting as microbial inoculation sources on endophyte assembly and growth of the invasive plant Ageratina adenophora in response to drought stress and temperature change. We found that fungal and bacterial enrichment in the leaves and roots of A. adenophora exhibited distinct patterns in response to climatic factors. Many fungi were enriched in roots in response to high temperature and drought stress; in contrast, many bacteria were enriched in leaves in response to low temperature and drought stress. Inoculation of microbiota from phylogenetically close native plant species (i.e., Asteraceae Artemisia atrovirens) causes the recipient plant A. adenophora (Asteraceae) to enrich dominant microbial species from inoculation sources, which commonly results in a lower dissimilar endophytic microbiota and thus produces more negative growth effects when compared to non-Asteraceae inoculations. Drought, microbial inoculation source, and temperature directly impacted the growth of A. adenophora. Both drought and inoculation also indirectly impacted the growth of A. adenophora by changing the root endophytic fungal assembly. Our data indicate that native plant identity can greatly impact the endophyte assembly and host growth of invasive plants, which is regulated by drought and temperature.IMPORTANCEThere has been increasing interest in the interactions between global changes and plant invasions; however, it remains to quantify the role of microbial endophytes in plant invasion with a consideration of their variation in the root vs leaf of hosts, as well as the linkages between microbial inoculations, such as native plant species, and climatic factors, such as temperature and drought. Our study found that local plants acting as microbial inoculants can impact fungal and bacterial enrichment in the leaves and roots of the invasive plant Ageratina adenophora and thus produce distinct growth effects in response to climatic factors; endophyte-mediated invasion of A. adenophora is expected to operate more effectively under favorable moisture. Our study is important for understanding the interactions between climate change, microbial endophytes, and local plant identity in the establishment and expansion of invasive species.

Hordeum vulgare differentiates its response to beneficial bacteria.

BACKGROUND: In nature, beneficial bacteria triggering induced systemic resistance (ISR) may protect plants from potential diseases, reducing yield losses caused by diverse pathogens. However, little is known about how the host plant initially responds to different beneficial bacteria. To reveal the impact of different bacteria on barley (Hordeum vulgare), bacterial colonization patterns, gene expression, and composition of seed endophytes were explored. RESULTS: This study used the soil-borne Ensifer meliloti, as well as Pantoea sp. and Pseudomonas sp. isolated from barley seeds, individually. The results demonstrated that those bacteria persisted in the rhizosphere but with different colonization patterns. Although root-leaf translocation was not observed, all three bacteria induced systemic resistance (ISR) against foliar fungal pathogens. Transcriptome analysis revealed that ion- and stress-related genes were regulated in plants that first encountered bacteria. Iron homeostasis and heat stress responses were involved in the response to E. meliloti and Pantoea sp., even if the iron content was not altered. Heat shock protein-encoding genes responded to inoculation with Pantoea sp. and Pseudomonas sp. Furthermore, bacterial inoculation affected the composition of seed endophytes. Investigation of the following generation indicated that the enhanced resistance was not heritable. CONCLUSIONS: Here, using barley as a model, we highlighted different responses to three different beneficial bacteria as well as the influence of soil-borne Ensifer meliloti on the seed microbiome. In total, these results can help to understand the interaction between ISR-triggering bacteria and a crop plant, which is essential for the application of biological agents in sustainable agriculture.

Harnessing the action mechanisms of microbial endophytes for enhancing plant performance and stress tolerance: current understanding and future perspectives.

Microbial endophytes are microorganisms that reside within plant tissues without causing any harm to their hosts. These microorganisms have been found to confer a range of benefits to plants, including increased growth and stress tolerance. In this review, we summarize the recent advances in our understanding of the mechanisms by which microbial endophytes confer abiotic and biotic stress tolerance to their host plants. Specifically, we focus on the roles of endophytes in enhancing nutrient uptake, modulating plant hormones, producing secondary metabolites, and activating plant defence responses. We also discuss the challenges associated with developing microbial endophyte-based products for commercial use, including product refinement, toxicology analysis, and prototype formulation. Despite these challenges, there is growing interest in the potential applications of microbial endophytes in agriculture and environmental remediation. With further research and development, microbial endophyte-based products have the potential to play a significant role in sustainable agriculture and environmental management.

Cryptic functional diversity within a grass mycobiome.

Eukaryotic hosts harbor tremendously diverse microbiomes that affect host fitness and response to environmental challenges. Fungal endophytes are prominent members of plant microbiomes, but we lack information on the diversity in functional traits affecting their interactions with their host and environment. We used two culturing approaches to isolate fungal endophytes associated with the widespread, dominant prairie grass Andropogon gerardii and characterized their taxonomic diversity using rDNA barcode sequencing. A randomly chosen subset of fungi representing the diversity of each leaf was then evaluated for their use of different carbon compound resources and growth on those resources. Applying community phylogenetic analyses, we discovered that these fungal endophyte communities are comprised of phylogenetically distinct assemblages of slow- and fast-growing fungi that differ in their use and growth on differing carbon substrates. Our results demonstrate previously undescribed and cryptic functional diversity in carbon resource use and growth in fungal endophyte communities of A. gerardii.

Assembly and Function of Seed Endophytes in Response to Environmental Stress.

Seeds are colonized by diverse microorganisms that can improve the growth and stress resistance of host plants. Although understanding the mechanisms of plant endophyte-host plant interactions is increasing, much of this knowledge does not come from seed endophytes, particularly under environmental stress that the plant host grows to face, including biotic (e.g., pathogens, herbivores and insects) and abiotic factors (e.g., drought, heavy metals and salt). In this article, we first provided a framework for the assembly and function of seed endophytes and discussed the sources and assembly process of seed endophytes. Following that, we reviewed the impact of environmental factors on the assembly of seed endophytes. Lastly, we explored recent advances in the growth promotion and stress resistance enhancement of plants, functioning by seed endophytes under various biotic and abiotic stressors.

The Rice Endophyte-Derived α-Mannosidase ShAM1 Degrades Host Cell Walls To Activate DAMP-Triggered Immunity against Disease.

Endophytes play an important role in shaping plant growth and immunity. However, the mechanisms for endophyte-induced disease resistance in host plants remain unclear. Here, we screened and isolated the immunity inducer ShAM1 from the endophyte Streptomyces hygroscopicus OsiSh-2, which strongly antagonizes the pathogen Magnaporthe oryzae. Recombinant ShAM1 can trigger rice immune responses and induce hypersensitive responses in various plant species. After infection with M. oryzae, blast resistance was dramatically improved in ShAM1-inoculated rice. In addition, the enhanced disease resistance by ShAM1 was found to occur through a priming strategy and was mainly regulated through the jasmonic acid-ethylene (JA/ET)-dependent signaling pathway. ShAM1 was identified as a novel α-mannosidase, and its induction of immunity is dependent on its enzyme activity. When we incubated ShAM1 with isolated rice cell walls, the release of oligosaccharides was observed. Notably, extracts from the ShAM1-digested cell wall can enhance the disease resistance of the host rice. These results indicated that ShAM1 triggered immune defense against pathogens by damage-associated molecular pattern (DAMP)-related mechanisms. Our work provides a representative example of endophyte-mediated modulation of disease resistance in host plants. The effects of ShAM1 indicate the promise of using active components from endophytes as plant defense elicitors for the management of plant disease. IMPORTANCE The specific biological niche inside host plants allows endophytes to regulate plant disease resistance effectively. However, there have been few reports on the role of active metabolites from endophytes in inducing host disease resistance. In this study, we demonstrated that an identified α-mannosidase protein, ShAM1, secreted by the endophyte S. hygroscopicus OsiSh-2 could activate typical plant immunity responses and induce a timely and cost-efficient priming defense against the pathogen M. oryzae in rice. Importantly, we revealed that ShAM1 enhanced plant disease resistance through its hydrolytic enzyme (HE) activity to digest the rice cell wall and release damage-associated molecular patterns. Taken together, these findings provide an example of the interaction mode of endophyte-plant symbionts and suggest that HEs derived from endophytes can be used as environmentally friendly and safe prevention agent for plant disease control.

Therapeutic compounds from medicinal plant endophytes: molecular and metabolic adaptations.

During the last few decades, endophytes have attracted increased attention due to their ability to produce a plethora of bioactive secondary metabolites. These compounds not only help the endophytes to outcompete other plant-associated microbes or pathogens through quorum sensing, but also enable them to surmount the plant immune system. However, only a very few studies have described the interlink between various biochemical and molecular factors of host-microbe interactions involved in the production of these pharmacological metabolites. The peculiar mechanisms by which endophytes modulate plant physiology and metabolism through elicitors, as well as how they use transitional compounds of primary and secondary metabolism as nutrients and precursors for the synthesis of new compounds or enhancing existing metabolites, are still less understood. This study thus attempts to address the aspects of synthesis of such metabolites used in therapeutics by the endophytes in the light of their ecological significance, adaptation, and intercommunity interactions. Our study explores how endophytes adapt to the specific host environment, especially in medicinal plants that produce metabolites with pharmacological potential and simultaneously modulate host gene expression for the biosynthesis of these metabolites. We also discuss the differential interactions of fungal and bacterial endophytes with their hosts.

Current Scenario and Future Prospects of Endophytic Microbes: Promising Candidates for Abiotic and Biotic Stress Management for Agricultural and Environmental Sustainability.

Globally, substantial research into endophytic microbes is being conducted to increase agricultural and environmental sustainability. Endophytic microbes such as bacteria, actinomycetes, and fungi inhabit ubiquitously within the tissues of all plant species without causing any harm or disease. Endophytes form symbiotic relationships with diverse plant species and can regulate numerous host functions, including resistance to abiotic and biotic stresses, growth and development, and stimulating immune systems. Moreover, plant endophytes play a dominant role in nutrient cycling, biodegradation, and bioremediation, and are widely used in many industries. Endophytes have a stronger predisposition for enhancing mineral and metal solubility by cells through the secretion of organic acids with low molecular weight and metal-specific ligands (such as siderophores) that alter soil pH and boost binding activity. Finally, endophytes synthesize various bioactive compounds with high competence that are promising candidates for new drugs, antibiotics, and medicines. Bioprospecting of endophytic novel secondary metabolites has given momentum to sustainable agriculture for combating environmental stresses. Biotechnological interventions with the aid of endophytes played a pivotal role in crop improvement to mitigate biotic and abiotic stress conditions like drought, salinity, xenobiotic compounds, and heavy metals. Identification of putative genes from endophytes conferring resistance and tolerance to crop diseases, apart from those involved in the accumulation and degradation of contaminants, could open new avenues in agricultural research and development. Furthermore, a detailed molecular and biochemical understanding of endophyte entry and colonization strategy in the host would better help in manipulating crop productivity under changing climatic conditions. Therefore, the present review highlights current research trends based on the SCOPUS database, potential biotechnological interventions of endophytic microorganisms in combating environmental stresses influencing crop productivity, future opportunities of endophytes in improving plant stress tolerance, and their contribution to sustainable remediation of hazardous environmental contaminants.

Multitrophic Interactions Between Arbuscular Mycorrhizal Fungi, Foliar Endophytic Fungi and Aphids.

Almost all living plants can be simultaneously colonised by arbuscular mycorrhizal fungi in the roots and endophytes in the shoots, while also being attacked by insect herbivores. However, to date, no study has ever examined the multitrophic interactions between these two different fungal groups and insects on any species of forb. Here, we examined the effects of two commercial species mixtures of arbuscular mycorrhizal fungi (AMF) and two foliar endophytes (Colletotrichum acutatum and Cladosporium oxysporum) on the growth of an invasive weed, Impatiens glandulifera, and the aphids that attack it. AMF reduced plant biomass, which was most evident when C. oxysporum was inoculated. Mycorrhizal fungi had few effects on aphids, and these depended on the identity of the endophytes present. Meanwhile, endophytes tended to increase aphid numbers, but this depended on the identity of the AMF inoculum. Throughout, there were differences in the responses of the plant to the two mycorrhizal mixtures, demonstrating clear AMF specificity in this plant. These specific effects were also strongly affected by the endophytes, with a greater number of interactions found between the AMF and endophytes than between the endophytes themselves. In particular, AMF reduced infection levels by the endophytes, while some endophyte inoculations reduced mycorrhizal colonisation. We suggest that both AMF and endophytes could play an important part in future biological control programmes of weeds, but further multitrophic experiments are required to unravel the complexity of interactions between spatially separated parts of the plant microbiome.

Plant Host Traits Mediated by Foliar Fungal Symbionts and Secondary Metabolites.

Fungal symbionts living inside plant leaves ("endophytes") can vary from beneficial to parasitic, but the mechanisms by which the fungi affect the plant host phenotype remain poorly understood. Chemical interactions are likely the proximal mechanism of interaction between foliar endophytes and the plant, as individual fungal strains are often exploited for their diverse secondary metabolite production. Here, we go beyond single strains to examine commonalities in how 16 fungal endophytes shift plant phenotypic traits such as growth and physiology, and how those relate to plant metabolomics profiles. We inoculated individual fungi on switchgrass, Panicum virgatum L. This created a limited range of plant growth and physiology (2-370% of fungus-free controls on average), but effects of most fungi overlapped, indicating functional similarities in unstressed conditions. Overall plant metabolomics profiles included almost 2000 metabolites, which were broadly correlated with plant traits across all the fungal treatments. Terpenoid-rich samples were associated with larger, more physiologically active plants and phenolic-rich samples were associated with smaller, less active plants. Only 47 metabolites were enriched in plants inoculated with fungi relative to fungus-free controls, and of these, Lasso regression identified 12 metabolites that explained from 14 to 43% of plant trait variation. Fungal long-chain fatty acids and sterol precursors were positively associated with plant photosynthesis, conductance, and shoot biomass, but negatively associated with survival. The phytohormone gibberellin, in contrast, was negatively associated with plant physiology and biomass. These results can inform ongoing efforts to develop metabolites as crop management tools, either by direct application or via breeding, by identifying how associations with more beneficial components of the microbiome may be affected.