Plant-microbe Symbiosis Research Articles

A conserved juxtamembrane motif in plant NFR5 receptors is essential for root nodule symbiosis

Establishment of root nodule symbiosis is initiated by the perception of bacterial Nod factor ligands by the plant LysM receptor kinases NFR1 and NFR5. Receptor signaling initiating the symbiotic pathway depends on the kinase activity of NFR1, while the signaling mechanism of the catalytically inactive NFR5 pseudokinase is unknown. Here, we present the crystal structure of the signaling-competent Lotus japonicus NFR5 intracellular domain, comprising the juxtamembrane region and pseudokinase domain. The juxtamembrane region is structurally well defined and forms two α-helices, αA and αA', which contain an exposed hydrophobic motif. We demonstrate that this "juxtamembrane motif" promotes NFR5-NFR5 and NFR1-NFR5 interactions and is essential for symbiotic signaling. Conservation analysis reveals that the juxtamembrane motif is present throughout NFR5-type receptors and is required for symbiosis signaling from barley RLK10, suggesting a conserved and broader function for this motif in plant-microbe symbioses.

Recycling steel slag as fertiliser proxy in agriculture is good circular economy but disrupts plant microbial symbioses in the soil

Modern agriculture depends on synthetic fertilisers to ensure food security but their manufacture and use accounts for ~5 % of the global greenhouse gas emissions. Achieving climate change targets therefore requires alternatives, that while maintaining crop productivity, reduce emissions across the lifecycle of fertiliser utilisation. Steel slag, a nutrient-rich by-product of steel manufacture, offers a viable alternative. Being substantially cheaper than fertilisers, it is economically attractive for farmers, particularly in low-middle income countries of the Global South. However, slag application in agriculture poses risk of pollutant transfer to the human food chain and disruption of key plant-microbe symbioses like the arbuscular mycorrhizal fungi (AMF). Here, using barley as a model crop, we tested the suitability of slag as a fertiliser proxy. Mycorrhizal and non-mycorrhizal barley were grown in soils ameliorated with slag in concentrations of 0, 2, 5 and 10 t ha−1. We analysed slag-mycorrhiza interaction and their combined effects on crop yield and risks to human nourishment. Slag increased grain yield by respective 32 and 21 % in mycorrhizal and non-mycorrhizal barley. Grain concentration of metal pollutants in mycorrhizal and non-mycorrhizal barley fertilised with slag were within the WHO recommended limits. But slag reduced mycorrhizal colonisation in barley roots and extraradical hyphal spread in the soil. The consequent decline in symbiont function lowered AMF-mediated plant nutrient uptake and increased mineral losses in leachates. AMF are keystone species of the soil microbiome. Loss of AMF function presents long-term ecological consequences for agriculture and necessitates a careful evaluation of slag application to soil.

Research Progress in the Joint Remediation of Plants–Microbes–Soil for Heavy Metal-Contaminated Soil in Mining Areas: A Review

Plants growing in heavy metal (HM)-contaminated soil have evolved a special detoxification mechanism. The rhizosphere gathers many living substances and their secretions at the center of plant roots, which has a unique ecological remediation effect. It is of great significance to thoroughly understand the ecological process of rhizosphere pollution under heavy metals (HMs) stress and develop biotechnology for joint remediation using plants and their coexisting microbial systems according to the mechanism of rhizosphere stress. Microbes can weaken the toxicity of HM pollutants by transforming the existing forms or reducing the bioavailability in the rhizosphere. Microbes survive in the HM-polluted soils through the production of stress-resistant substances, the participation of proteins, and the expression of heavy metal resistance genes, which strengthens the resistance of plants. Moreover, microbes can improve the nutritional status of plants to improve plant resistance to HMs. Plants, in turn, provide a habitat for microbes to survive and reproduce, which greatly accelerates the process of bioremediation. Briefly, the combined remediation of soil HMs pollution by plants and microbes is a promising, green, and sustainable strategy. Here, we mainly elucidate the joint remediation mechanism of plant–microbe symbiosis and introduce the coping characteristics of plants, microbes, and their symbiotic system, hoping to provide a scientific basis for the remediation of HM-contaminated soil in mining areas and the sustainable development of the ecological environment.

Host specificity of plant‐associated bacteria is negatively associated with genome size and host abundance along a latitudinal gradient

AbstractHost specialization plays a critical role in the ecology and evolution of plant–microbe symbiosis. Theory predicts that host specialization is associated with microbial genome streamlining and is influenced by the abundance of host species, both of which can vary across latitudes, leading to a latitudinal gradient in host specificity. Here, we quantified the host specificity and composition of plant–bacteria symbioses on leaves across 329 tree species spanning a latitudinal gradient. Our analysis revealed a predominance of host‐specialized leaf bacteria. The degree of host specificity was negatively correlated with bacterial genome size and the local abundance of host plants. Additionally, we found an increased host specificity at lower latitudes, aligning with the high prevalence of small bacterial genomes and rare host species in the tropics. These findings underscore the importance of genome streamlining and host abundance in the evolution of host specificity in plant‐associated bacteria along the latitudinal gradient.

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 β-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.

The dynamic interplay of root exudates and rhizosphere microbiome

The rhizosphere microbiome plays a vital role in plant growth, health, and nutrient acquisition. One of the key factors that shape the composition and function of the rhizosphere microbiome is root exudates, the complex mixture of organic compounds released by plant roots. Root exudates serve as a source of energy and nutrients for the rhizosphere microbiome, as well as a means of communication between plants and microbes. The dynamic interplay between root exudates and rhizosphere microbiome is a complex and highly regulated process that involves multiple feedback loops and interactions. Recent studies have revealed that the composition and quantity of root exudates are modulated by a range of biotic and abiotic factors, including plant genotype, soil type, nutrient availability, and microbial community structure. In turn, the rhizosphere microbiome can influence the production and composition of root exudates, through processes such as nutrient cycling, plant hormone synthesis, and modulation of plant defense responses. Understanding the dynamics of root exudates and rhizosphere microbiomes is crucial for developing effective strategies for microbiome engineering, plant-microbe symbiosis, and sustainable agriculture. This review provides an overview of the current state of knowledge on the dynamic interplay between root exudates and rhizosphere microbiomes, highlighting the key factors and mechanisms that govern this complex relationship.

Deciphering key factors in pathogen-suppressive microbiome assembly in the rhizosphere.

In a plant-microbe symbiosis, the host plant plays a key role in promoting the association of beneficial microbes and maintaining microbiome homeostasis through microbe-associated molecular patterns (MAMPs). The associated microbes provide an additional layer of protection for plant immunity and help in nutrient acquisition. Despite identical MAMPs in pathogens and commensals, the plant distinguishes between them and promotes the enrichment of beneficial ones while defending against the pathogens. The rhizosphere is a narrow zone of soil surrounding living plant roots. Hence, various biotic and abiotic factors are involved in shaping the rhizosphere microbiome responsible for pathogen suppression. Efforts have been devoted to modifying the composition and structure of the rhizosphere microbiome. Nevertheless, systemic manipulation of the rhizosphere microbiome has been challenging, and predicting the resultant microbiome structure after an introduced change is difficult. This is due to the involvement of various factors that determine microbiome assembly and result in an increased complexity of microbial networks. Thus, a comprehensive analysis of critical factors that influence microbiome assembly in the rhizosphere will enable scientists to design intervention techniques to reshape the rhizosphere microbiome structure and functions systematically. In this review, we give highlights on fundamental concepts in soil suppressiveness and concisely explore studies on how plants monitor microbiome assembly and homeostasis. We then emphasize key factors that govern pathogen-suppressive microbiome assembly. We discuss how pathogen infection enhances plant immunity by employing a cry-for-help strategy and examine how domestication wipes out defensive genes in plants experiencing domestication syndrome. Additionally, we provide insights into how nutrient availability and pH determine pathogen suppression in the rhizosphere. We finally highlight up-to-date endeavors in rhizosphere microbiome manipulation to gain valuable insights into potential strategies by which microbiome structure could be reshaped to promote pathogen-suppressive soil development.

Effect of moss removal on soil multifunctionality during vegetation restoration in subtropical ecosystems

Mosses are multifunctional communities that are increasingly recognized as potential and sustainable resources to restore degraded ecosystems. However, available information is limited on the influence of mosses on soil multifunctionality during vegetation restoration in subtropical ecosystems. We investigated the effects of mosses on soil multifunctionality and four single functions in three vegetation restoration approaches (monoculture plantations, monoculture forage grasses and intercropping of trees and forage grasses) by conducting a moss removal and retention experiment. Moss removal decreased soil multifunctionality and the single functions of nutrient provisioning, water retention and plant–microbe symbiosis, particularly in monoculture plantations, in the 0–5 cm soil layer. Moss removal decreased the phospholipid fatty acid abundance of soil microbes (e.g., bacteria, Gram-negative bacteria and general fungi) in the 2–5 cm soil layer but had nonsignificant effects on the nematode community. Random forest analysis showed that moss properties were more important factors than the soil physicochemical, microbial and nematode properties linked to soil multifunctionality. Moss properties (diversity, thickness, biomass, carbon and nitrogen concentrations, carbon to nitrogen ratio, biological nitrogen fixation rate and saturated water absorption content) were positively associated with soil multifunctionality, nutrient provisioning, water retention and plant–microbe symbiosis. These findings highlight the importance of preserving mosses to maintain soil multifunctionality during vegetation restoration in degraded subtropical ecosystems, especially in monoculture plantations.

Tripartite associations: A bacterial symbiont of fungi promotes plant growth without compromising the benefits conferred by an Epichloë endophyte

Few studies have evaluated the effects of bacteria that form associations with fungi on plant-microbial symbioses. We investigated the effects of a novel symbiotic bacterium (E226) of Epichloë, a well-researched mutualistic fungal endophyte of grasses, on perennial ryegrass (Lolium perenne) also associated with Epichloë. We hypothesised that E226 would promote plant growth but would not interfere with the in-planta growth of Epichloë and its production of antiherbivore alkaloids. E226, identified as Micrococcus luteus, formed an ectosymbiotic relationship with Epichloë when cultured on artificial media (i.e., bacterial cells were located on the hyphal surface) and possessed plant-growth promoting traits identified through whole genome analysis. Seeds of L. perenne, already colonised by an Epichloë strain, were inoculated with E226. The bacterium established within the seedlings, and the abundance of M. luteus populations initially increased with plant age. In agreement with our hypotheses, plant inoculation with E226 enhanced the production of leaves and did not affect the growth of Epichloë or the concentration of Epichloë-derived alkaloids. The putative abilities of E226 to solubilise phosphate and produce vitamins and metabolic cofactors may explain the observed plant growth promotion.

Supporting urban greenspace with microbial symbiosis

Societal Impact StatementCities are stressful environments for plants, plagued by heat, pollution, and biodiversity loss. As a result, plant communities tend to suffer in green roofs, parks, and living walls. Finding solutions to help plants grow in stressful environments is a goal of the sustainable city. One solution is to better incorporate plant–microbe symbiosis in green architecture. Symbiotic fungi and bacteria can provide nutrients, water, and help plants to cope with urban stress. The reconceptualization of green infrastructure from a microbial‐focused perspective has the potential to improve plant health, growth, and diversity in cities.SummaryPlant communities in cities help maintain the health and stability of urban ecosystems and inhabitants. Ensuring that greenspace is healthy and productive is a key goal of green infrastructure and landscape architecture (GILA). However, cities are stressful environments for plants. In natural ecosystems, plants live in symbiosis with fungi, bacteria, and other microbes that can help alleviate stress. Microbial communities may also help with stress associated with urban environments. Incorporating mutualistic symbioses into GILA is a sustainable way to enhance urban greenspace. Here, we address key stressors for GILA in cities, including dependency on fertilizers, pathogens, drought, fewer pollinators, pollution, and reduced plant biodiversity. For each of these stressors, we discuss how symbiotic fungi and bacteria can help mitigate these issues, including case‐use scenarios. We conclude with new approaches to deliberately incorporate mutualisms in cities and open dialogues with stakeholders.

Enhancing function of plant-microbial symbiosis for pollution mitigation and carbon sequestration

Enhancing function of plant-microbial symbiosis for pollution mitigation and carbon sequestration

Advances in the study of the function and mechanism of the action of flavonoids in plants under environmental stresses.

This review summarizes the anti-stress effects of flavonoids in plants and highlights its role in the regulation of polar auxin transport and free radical scavenging mechanism. As secondary metabolites widely present in plants, flavonoids play a vital function in plant growth, but also in resistance to stresses. This review introduces the classification, structure and synthetic pathways of flavonoids. The effects of flavonoids in plant stress resistance were enumerated, and the mechanism of flavonoids in plant stress resistance was discussed in detail. It is clarified that plants under stress accumulate flavonoids by regulating the expression of flavonoid synthase genes. It was also determined that the synthesized flavonoids are transported in plants through three pathways: membrane transport proteins, vesicles, and bound to glutathione S-transferase (GST). At the same time, the paper explores that flavonoids regulate polar auxin transport (PAT) by acting on the auxin export carrier PIN-FORMED (PIN) in the form of ATP-binding cassette subfamily B/P-glycoprotein (ABCB/PGP) transporter, which can help plants to respond in a more dominant form to stress. We have demonstrated that the number and location of hydroxyl groups in the structure of flavonoids can determine their free radical scavenging ability and also elucidated the mechanism by which flavonoids exert free radical removal in cells. We also identified flavonoids as signaling molecules to promote rhizobial nodulation and colonization of arbuscular mycorrhizal fungi (AMF) to enhance plant-microbial symbiosis in defense to stresses. Given all this knowledge, we can foresee that the in-depth study of flavonoids will be an essential way to reveal plant tolerance and enhance plant stress resistance.

Epigenetic control is involved in molecular dialogue in plant-microbe symbiosis.

This article is a Commentary on Vigneaud et al. (2023), 238: 2561–2577.

Biotization of in vitro oil palm (Elaeis guineensis Jacq.) and its plant-microbe interactions.

Continuous discovery of novel in vitro plant culture practices is always essential to promote better plant growth in the shortest possible cultivation period. An alternative approach to conventional micropropagation practice could be achieved through biotization by inoculating selected Plant Growth Promoting Rhizobacteria (PGPR) into the plant tissue culture materials (e.g., callus, embryogenic callus, and plantlets). Such biotization process often allows the selected PGPR to form a sustaining population with various stages of in vitro plant tissues. During the biotization process, plant tissue culture material imposes developmental and metabolic changes and enhances its tolerance to abiotic and biotic stresses, thereby reducing mortality in the acclimatization and pre-nursery stages. Understanding the mechanisms is, therefore crucial for gaining insights into in vitro plant-microbe interactions. Studies of biochemical activities and compound identifications are always essential to evaluate in vitro plant-microbe interactions. Given the importance of biotization in promoting in vitro plant material growth, this review aims to provide a brief overview of the in vitro oil palm plant-microbe symbiosis system.

Current Progress and Open Challenges for Combined Toxic Effects of Manufactured Nano-Sized Objects (MNO’s) on Soil Biota and Microbial Community

Soil is a porous matrix containing organic matter and minerals as well as living organisms that vary physically, geographically, and temporally. Plants choose a particular microbiome from a pool of soil microorganisms which helps them grow and stay healthy. Many ecosystem functions in agrosystems are provided by soil microbes just like the ecosystem of soil, the completion of cyclic activity of vital nutrients like C, N, S, and P is carried out by soil microorganisms. Soil microorganisms affect carbon nanotubes (CNTs), nanoparticles (NPs), and a nanopesticide; these are called manufactured nano-objects (MNOs), that are added to the environment intentionally or reach the soil in the form of contaminants of nanomaterials. It is critical to assess the influence of MNOs on important plant-microbe symbiosis including mycorrhiza, which are critical for the health, function, and sustainability of both natural and agricultural ecosystems. Toxic compounds are released into rural and urban ecosystems as a result of anthropogenic contamination from industrial processes, agricultural practices, and consumer products. Once discharged, these pollutants travel through the atmosphere and water, settling in matrices like sediments and groundwater, potentially rendering broad areas uninhabitable. With the rapid growth of nanotechnology, the application of manufactured nano-objects in the form of nano-agrochemicals has expanded for their greater potential or their appearance in products of users, raising worries about possible eco-toxicological impacts. MNOs are added throughout the life cycle and are accumulated not only in the soils but also in other components of the environment causing mostly negative impacts on soil biota and processes. MNOs interfere with soil physicochemical qualities as well as microbial metabolic activity in rhizospheric soils. This review examines the harmful effect of MNOs on soil, as well as the pathways used by microbes to deal with MNOs and the fate and behavior of NPs inside the soils.

Isotopic evidence for increased carbon and nitrogen exchanges between peatland plants and their symbiotic microbes with rising atmospheric CO2 concentrations since 15,000 cal. year BP.

Whether nitrogen (N) availability will limit plant growth and removal of atmospheric CO2 by the terrestrial biosphere this century is controversial. Studies have suggested that N could progressively limit plant growth, as trees and soils accumulate N in slowly cycling biomass pools in response to increases in carbon sequestration. However, a question remains over whether longer-term (decadal to century) feedbacks between climate, CO2 and plant N uptake could emerge to reduce ecosystem-level N limitations. The symbioses between plants and microbes can help plants to acquire N from the soil or from the atmosphere via biological N2 fixation-the pathway through which N can be rapidly brought into ecosystems and thereby partially or completely alleviate N limitation on plant productivity. Here we present measurements of plant N isotope composition (δ15 N) in a peat core that dates to 15,000 cal. year BP to ascertain ecosystem-level N cycling responses to rising atmospheric CO2 concentrations. We find that pre-industrial increases in global atmospheric CO2 concentrations corresponded with a decrease in the δ15 N of both Sphagnum moss and Ericaceae when constrained for climatic factors. A modern experiment demonstrates that the δ15 N of Sphagnum decreases with increasing N2 -fixation rates. These findings suggest that plant-microbe symbioses that facilitate N acquisition are, over the long term, enhanced under rising atmospheric CO2 concentrations, highlighting an ecosystem-level feedback mechanism whereby N constraints on terrestrial carbon storage can be overcome.

Plant–microbe symbiosis widens the habitability range of the Daisyworld

Plant–microbe symbiosis is pervasive in the Earth’s ecosystems and dates back to the early land colonisation by plants. Mutualistic partnership with rhizobia bacteria and mycorrhizal fungi promotes plant nutrition, growth and diversity, impacting important ecosystem functions. However, how the global behaviour and dynamical properties of an ecosystem are modified by plant–microbe symbiosis is still unclear. To tackle this theoretical question, we resorted to the Daisyworld as a toy model of the global ecosystem. We redesigned the original model to allow accounting for seed production, spreading, germination, and seedling development to mature seed-producing plants to describe how symbiotic and non-symbiotic daisy species differ in these key processes. Using the steady-state and bifurcation analysis of this model, we demonstrate that symbiosis with microbes broadens the habitability range of the Daisyworld by enhancing plant growth and/or facilitating plant access to otherwise uninhabitable nutrient-poor regions.

Draft Metagenome Sequences of the Sphagnum (Peat Moss) Microbiome from Ambient and Warmed Environments across Europe.

ABSTRACTWe present 49 metagenome assemblies of the microbiome associated with Sphagnum (peat moss) collected from ambient, artificially warmed, and geothermally warmed conditions across Europe. These data will enable further research regarding the impact of climate change on plant-microbe symbiosis, ecology, and ecosystem functioning of northern peatland ecosystems.

Ecological functions of plant-microbial symbioses and their role in the development of resource-saving biotechnologies

The possibility of using the polyfunctional properties of plant-microbial symbiosis in the development of resourcesaving technologies in crop production has been substantiated. An ecological assessment of the interaction of legume genotypes with rhizosphere microflora was carried out, and the role of plant-microbial systems in the accumulation of biological nitrogen was shown. The positive effect of plant-microbial interactions on soil biogenicity and plant adaptation to biotic stresses was revealed.

Soil nutritional status in KwaZulu-Natal drives symbiotic interactions and plant performance in

Context Cancer bush (Lessertia frutescens L.) is a multipurpose medicinal legume endemic to southern Africa, reported to grow in a variety of soils, from very poor to fertile ones. However, there is limited knowledge on how L. frutescens is able to thrive in diverse soils and, particularly, nothing has been reported on the benefits from the microbe symbiosis, plant growth and acclimation to low nutrient soils. Aims Therefore, this study examined the effect of soil nutrient deficiency in plant–microbe symbiosis, nitrogen (N) nutrition and associated plant performance of L. frutescens plants, growing in four different impoverished soils from the KwaZulu-Natal region. Methods Experimental soil samples collected from four geographical distinct KwaZulu-Natal (KZN) locations (Hluhluwe, Izingolweni, Bergville and Ashburton) representing grasslands and savanna were used as natural inoculum and growth substrate. Key results Soil analysis showed significant differences in soil pH, exchange acidity, total cations, organic carbon (C), phosphorus (P) and N related to differences in the soil provenance. L. frutescens root nodules were dominated by Bacillus sp. in all soil treatments, except in plants grown in Bergville soil that did not nodulate. In all, 68–90% of total plant N concentration was reduced from atmospheric N. L. frutescens plants also relied on soil-available N for growth. Hluhluwe and Ashburton soil-grown plants showed a significantly higher biomass than did other soil-grown plants. Conclusions These current findings demonstrated that L. frutescens root nodules were dominated by bacteria characterised as phospho-bacteria and N2-fixing bacteria in these impoverished soils. This enabled L. frutescens to fix atmospheric N and assimilate soil available N to reduce energy demand. Implications These strategies may collectively contribute to L. frutescens resilience in nutrient-deficient savanna and grassland ecosystems.