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Oxidative stress is encountered by fungi in almost all niches, resulting in fungal degeneration or even death. Fungal tolerance to oxidative stress has been extensively studied, but the current understanding of the mechanisms regulating oxidative stress tolerance in fungi remains limited. The entomopathogenic and endophytic fungus Metarhizium robertsii encounters oxidative stress when it infects insects and develops a symbiotic relationship with plants, and we found that host reactive oxygen species (ROSs) greatly limited fungal growth in both insects and plants. We identified a histone H3 deacetylase (HDAC3) that catalyzed the deacetylation of lysine 56 of histone H3. Deleting Hdac3 significantly reduced the tolerance of M. robertsii to oxidative stress from insects and plants, thereby decreasing fungal ability to colonize the insect hemocoel and plant roots. HDAC3 achieved this by regulating the expression of three genes in the ergosterol biosynthesis pathway, which includes the lanosterol synthase gene Las1. The deletion of Hdac3 or Las1 reduced the ergosterol content and impaired cell membrane integrity. This resulted in an increase in ROS accumulation in fungal cells that were thus more sensitive to oxidative stress. We further showed that HDAC3 regulated the expression of the three ergosterol biosynthesis genes in an indirect manner. Our work significantly advances insights into the epigenetic regulation of oxidative stress tolerance and the interactions between M. robertsii and its plant and insect hosts.IMPORTANCEOxidative stress is a common challenge encountered by fungi that have evolved sophisticated mechanisms underlying tolerance to this stress. Although fungal tolerance to oxidative stress has been extensively investigated, the current understanding of the mechanisms for fungi to regulate oxidative stress tolerance remains limited. In the model entomopathogenic and plant symbiotic fungus Metarhizium robertsii, we found that the histone H3 deacetylase HDAC3 regulates the production of ergosterol, an essential cell membrane component. This maintains the cell membrane integrity to resist the oxidative stress derived from the insect and plant hosts for successful infection of insects and development of symbiotic associates with plants. Our work provides significant insights into the regulation of oxidative stress tolerance in M. robertsii and its interactions with insects and plants.

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Background: Drought constitutes a major abiotic stress factor adversely affecting plant growth and productivity. Plant-microbe symbiotic associations have evolved regulatory mechanisms to adapt to environmental stress conditions. However, the interactive effects of different fungi on host growth and stress tolerance under drought conditions remain unclear. Objective: This study explored the effects of varying polyethylene glycol (PEG-6000) concentrations (0%, 15%, 25%, and 35%) on the growth and physiological responses of two ectomycorrhizal fungi (Suillus granulatus (Sg) and Pisolithus tinctorius (Pt)) and two dark septate endophytes (Pleotrichocladium opacum (Po) and Pseudopyrenochaeta sp. (Ps)) isolated from the root system of Pinus tabuliformis. Specifically, the study aimed to evaluate six inoculation treatments, including no inoculation (CK), single inoculations with Sg, Pt, Po, Ps, and a mixed inoculation (Sg: Pt : Po: Ps = 1:1:1:1), on the growth and physiological characteristics of P. tabuliformis seedlings under different water regimes: well-watered at 70% ± 5%, light drought at 50% ± 5%, and severe drought at 30% ± 5% of the maximum field water holding capacity. Results: All four fungi exhibited the capacity to cope with drought stress by enhancing antioxidant activities and regulating osmotic balance. Upon successful root colonization, they increased plant height, shoot biomass, root biomass, total biomass, and mycorrhizal growth response in P. tabuliformis seedlings. Under drought stress conditions, fungal inoculation improved seedling drought resistance by increasing superoxide dismutase and catalase activities, free proline and soluble protein contents, and promoting nitrogen and phosphorus uptake. Notably, mixed inoculation treatments significantly enhanced antioxidant capacity, osmotic adjustment, and nutrient acquisition abilities, leading to superior growth promotion effects under drought stress compared to single inoculation treatments. Conclusion: All four fungi tolerated PEG-induced drought stress, with increased antioxidant enzyme activities and osmotic adjustment substances and they promoted the growth and enhanced drought resistance of P. tabuliformis seedlings.

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Endophytic fungi are a diverse group of microorganisms that reside within plant tissues and play a crucial ecological role in the development of their hosts. Psidium cattleianum (Myrtales: Myrtaceae: 'Cattley guava') is a Brazilian native species with economic potential due to the diverse applications of its fruits, wood, and essential oils. Despite their significance, the diversity of endophytic fungi associated with P. cattleianum remains unexplored. Here, we investigated the diversity of endophytic fungi in the leaves of this plant using cultivation-dependent isolation methods, analysis of the macroscopic characters of the isolates, and phylogenetic analyses employing the ITS barcode marker. A total of 396 isolates, classified into 25 fungal taxa, were obtained, namely, Alternaria, Aspergillus, Cladosporium, Colletotrichum, Coprinellus, Coriolopsis, Diaporthe, Induratia, Mycosphaerella, Muyocoprom, Myrmecridium, Neofusicoccum, Pantospora, Paracamarosporium, Parapallidocercospora, Paraphaeosphaeria, Penicillium, Perenniporia, Phaeophleospora, Phyllosticta, Pseudofusicoccum, Talaromyces, Xylaria, Sordariomycetes, and Xylariomycetes. Our findings reveal a significant diversity of fungi associated with P. cattleianum leaves; however, our study suggests an even greater diversity of fungi associated with this plant species. Interestingly, although P. cattleianum shares endophytic fungi with other plants in the Myrtaceae family, this plant species harbors a unique fungal community. This distinction is evidenced by certain fungal genera and seven potentially new phylogenetic species, isolated in this study.

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In northeast China, the invasive woodwasp., Sirex noctilio, attacks Pinus sylvestris var. mongolica Litv and often shares habitat with native Sirex nitobei. Previous research showed that S. noctilio can utilize the volatiles from its symbiotic fungus (A. areolatum IGS-BD) to locate host trees. Consequently, symbiotic fungi (A. areolatum IGS-D and A. chailletii) carried by S. nitobei may influence the behavioral selection of S. noctilio. This study aimed to investigate the impact of fungal odor sources on S. noctilio's behavior in laboratory and field experiments. Our observations revealed that female woodwasps exhibited greater attraction toward the fungal volatiles of 14-day-old Amylostereum IGS-D in a "Y"-tube olfactometer and wind tunnel. When woodwasps were released into bolts inoculated separately with three strains in the field, females of S. noctilio exhibited a preference for those bolts pre-inoculated with A. areolatum IGS-BD. Gas chromatography-mass spectrometry (GC-MS) analysis revealed that the volatiles emitted by the two genotypes of A. areolatum were similar yet significantly distinct from those of Ampelopsis chailletii. Hence, we postulate that the existence of native A. areolatum IGS-D could potentially facilitate the colonization of S. noctilio in scenarios with minimal or no A. areolatum IGS-BD present in the host.

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Plant-derived sugars and lipids are key nutritional sources for plant associated fungi. However, the relationship between utilization of host-derived sugars and lipids during development of the symbiotic association remains unknown. Here we show that the fungus Metarhizium robertsii also needs plant-derived lipids to develop symbiotic relationship with plants. The fatty acid binding proteins FABP1 and FABP2 are important for utilization of plant-derived lipids as the deletion of Fabp1 and Fabp2 significantly reduced the ability of M. robertsii to colonize rhizoplane and rhizosphere of maize and Arabidopsis thaliana. Deleting Fabp1 and Fabp2 increased sugar utilization by upregulating six sugar transporters, and this explains why deleting the monosaccharide transporter gene Mst1, which plays an important role in utilization of plant-derived sugars, had no impact on the ability of the double-gene deletion mutant ΔFabp1::ΔFabp2 to colonize plant roots. FABP1 and FABP2 were also found in other plant-associated Metarhizium species, and they were highly expressed in the medium using the tomato root exudate as the sole carbon and nitrogen source, suggesting that they could be also important for these species to develop symbiotic relationship with plants. In conclusion, we discovered that utilization of plant-derived sugars and lipids are coupled during colonization of rhizoplane and rhizosphere by M. robertsii.

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Anoplophora glabripennis (Asian longhorned beetle) is a wood-boring pest that can inhabit a wide range of healthy deciduous host trees in native and non-native habitats. Lignocellulose degradation plays a major role in the acquisition of nutrients during the growth and development of A. glabripennis larvae. In this study, the lignocellulose degradation capacity of Fusarium solani, a fungal symbiont of A. glabripennis, was investigated in fermentation culture and in four host tree species. The impact of F. solani on larval growth and survival parameters was assessed. Fermentation culture demonstrated continuous and stable production of lignocellulolytic enzymes over the cultivation period. Furthermore, F. solani was able to degrade host tree lignocellulose, as shown by decreased soluble sugar and cellulose contents and an increase in protein content. No significant differences in larval survival were observed in larvae fed with or without F. solani. However, weight and head capsule width were higher in larvae fed on F. solani, and gut lignocellulose activities were elevated in fed larvae. Our results indicate a role for F. solani in the predigestion of lignocellulose during the colonization and parasitic stages of A. glabripennis larval development, and also the F. solani an important symbiotic partner to A. glabripennis, lowering barriers to colonization and development in a range of habitats.

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BACKGROUND: The true bugs (Heteroptera) occupy nearly all of the known ecological niches of insects. Among them, as a group containing more than 30,000 species, the phytophagous true bugs are making increasing impacts on agricultural and forestry ecosystems. Previous studies proved that symbiotic bacteria play important roles in these insects in fitting various habitats. However, it is still obscure about the evolutionary and ecological patterns of the microorganisms of phytophagous true bugs as a whole with comprehensive taxon sampling. RESULTS: Here, in order to explore the symbiotic patterns between plant-feeding true bugs and their symbiotic microorganisms, 209 species belonging to 32 families of 9 superfamilies had been sampled, which covered all the major phytophagous families of true bugs. The symbiotic microbial communities were surveyed by full-length 16S rRNA gene and ITS amplicons respectively for bacteria and fungi using the PacBio platform. We revealed that hosts mainly affect the dominant bacteria of symbiotic microbial communities, while habitats generally influence the subordinate ones. Thereafter, we carried out the ancestral state reconstruction of the dominant bacteria and found that dramatic replacements of dominant bacteria occurred in the early Cretaceous and formed newly stable symbiotic relationships accompanying the radiation of insect families. In contrast, the symbiotic fungi were revealed to be horizontally transmitted, which makes fungal communities distinctive in different habitats but not significantly related to hosts. CONCLUSIONS: Host and habitat determine microbial communities of plant-feeding true bugs in different roles. The symbiotic bacterial communities are both shaped by host and habitat but in different ways. Nevertheless, the symbiotic fungal communities are mainly influenced by habitat but not host. These findings shed light on a general framework for future microbiome research of phytophagous insects. Video Abstract.

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Armillaria members play important roles in the nutrient supply and growth modulation of Gastrodia elata Bl., and they will undergo severe competition with native soil organisms before colonization and become symbiotic with G. elata. Unraveling the response of soil microbial organisms to symbiotic fungi will open up new avenues to illustrate the biological mechanisms driving G. elata's benefit from Armillaria. For this purpose, Armillaria strains from four main G. elata production areas in China were collected, identified, and co-planted with G. elata in Guizhou Province. The result of the phylogenetic tree indicated that the four Armillaria strains shared the shortest clade with Armillaria gallica. The yields of G. elata were compared to uncover the potential role of these A. gallica strains. Soil microbial DNA was extracted and sequenced using Illumina sequencing of 16S and ITS rRNA gene amplicons to decipher the changes of soil bacterial and fungal communities arising from A. gallica strains. The yield of G. elata symbiosis with the YN strain (A. gallica collected from Yunnan) was four times higher than that of the GZ strain (A. gallica collected from Guizhou) and nearly two times higher than that of the AH and SX strains (A. gallica collected from Shanxi and Anhui). We found that the GZ strain induced changes in the bacterial community, while the YN strain mainly caused changes in the fungal community. Similar patterns were identified in non-metric multidimensional scaling analysis, in which the GZ strain greatly separated from others in bacterial structure, while the YN strain caused significant separation from other strains in fungal structure. This current study revealed the assembly and response of the soil microbial community to A. gallica strains and suggested that exotic strains of A. gallica might be helpful in improving the yield of G. elata by inducing changes in the soil fungal community.

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Nitrogen (N) enrichment is widely known to affect the root-associated arbuscular mycorrhizal fungal (AMF) community in different ways, for example, via altering soil properties and/or shifting host plant functional structure. However, empirical knowledge of their relative importance is still lacking. Using a long-term N addition experiment, we measured the AMF community taxonomic and phylogenetic diversity at the single plant species (roots of 15 plant species) and plant community (mixed roots) levels. We also measured four functional traits of 35 common plant species along the N addition gradient. We found divergent responses of AMF diversity to N addition for host plants with different innate heights (i.e. plant natural height under unfertilized treatment). Furthermore, our data showed that species-specific responses of AMF diversity to N addition were negatively related to the change in maximum plant height. When scaling up to the community level, N addition affected AMF diversity mainly through increasing the maximum plant height, rather than altering soil properties. Our results highlight the importance of plant height in driving AMF community dynamics under N enrichment at both species and community levels, thus providing important implications for understanding the response of AMF diversity to anthropogenic N deposition.

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Fungi live different lifestyles-including pathogenic and symbiotic-by interacting with living plants. Recently, there has been a substantial increase in the study of phytopathogenic fungi and their interactions with plants. Symbiotic relationships with plants appear to be lagging behind, although progressive. Phytopathogenic fungi cause diseases in plants and put pressure on survival. Plants fight back against such pathogens through complicated self-defense mechanisms. However, phytopathogenic fungi develop virulent responses to overcome plant defense reactions, thus continuing their deteriorative impacts. Symbiotic relationships positively influence both plants and fungi. More interestingly, they also help plants protect themselves from pathogens. In light of the nonstop discovery of novel fungi and their strains, it is imperative to pay more attention to plant-fungi interactions. Both plants and fungi are responsive to environmental changes, therefore construction of their interaction effects has emerged as a new field of study. In this review, we first attempt to highlight the evolutionary aspect of plant-fungi interactions, then the mechanism of plants to avoid the negative impact of pathogenic fungi, and fungal strategies to overcome the plant defensive responses once they have been invaded, and finally the changes of such interactions under the different environmental conditions.

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Genomic traits reflect the evolutionary processes that have led to ecological variation among extant organisms, including variation in how they acquire and use resources. Soil fungi have diverse nutritional strategies and exhibit extensive variation in fitness along resource gradients. We tested for trade-offs in genomic traits with mycelial nutritional traits and hypothesize that such trade-offs differ among fungal guilds as they reflect contrasting resource exploitation and habitat preferences. We found species with large genomes exhibited nutrient-poor mycelium and low GC content. These patterns were observed across fungal guilds but with varying explanatory power. We then matched trait data to fungal species observed in 463 Australian grassland, woodland and forest soil samples. Fungi with large genomes and lower GC content dominated in nutrient-poor soils, associated with shifts in guild composition and with species turnover within guilds. These findings highlight fundamental mechanisms that underpin successful ecological strategies for soil fungi.

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Ganoderma lucidum polysaccharides (GLP) attract growing attention due to their remarkable bioactivities, but the low content in raw materials remains a bottleneck severely restricting their application. We previously found a higher polysaccharides accumulation in Ganoderma lucidum cultured in continuous cropping soil, and soil symbiotic fungi are presumed as the key among many factors. Herein, 33 symbiotic fungi were isolated from the soil, and fungal elicitors were prepared to investigate their biotic eliciting effect on GLP biosynthesis. Most elicitors were found to significantly improve GLP production, among which the NO.16 molecularly identified as Penicillium citrinum, exhibited the optimum eliciting effect with GLP yield increasing by 3.4 times. Differences in the biosynthetic pathway genes expressions and the monosaccharide components of GLP were further analyzed. The transcriptions of the main genes of GLP biosynthetic pathway were up-regulated under PCE treatments, suggesting it improves GLP production by activating transcriptions of the biosynthetic pathway genes. Moreover, PCE eliciting significantly altered the monosaccharide compositions of GLP with Gal, Man, GalA, GlcA, and Fuc increasing by 8.17 %, 5.68 %, 5.41 %, 2.66 %, and 1.51 % respectively, but Glc decreased by 23.43 %, which may result in the activity change. It can serve as a new strategy to improve GLP production.

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Heritable fungal endosymbiosis is underinvestigated in plant biology and documented in only three plant families (Convolvulaceae, Fabaceae, and Poaceae). An estimated 40% of morning glory species in the tribe Ipomoeeae (Convolvulaceae) have associations with one of two distinct heritable, endosymbiotic fungi (Periglandula and Chaetothyriales) that produce the bioactive metabolites ergot alkaloids, indole diterpene alkaloids, and swainsonine, which have been of interest for their toxic effects on animals and potential medical applications. Here, we report the occurrence of ergot alkaloids, indole diterpene alkaloids, and swainsonine in the Convolvulaceae; and the fungi that produce them based on synthesis of previous studies and new indole diterpene alkaloid data from 27 additional species in a phylogenetic, geographic, and life-history context. We find that individual morning glory species host no more than one metabolite-producing fungal endosymbiont (with one possible exception), possibly due to costs to the host and overlapping functions of the alkaloids. The symbiotic morning glory lineages occur in distinct phylogenetic clades, and host species have significantly larger seed size than nonsymbiotic species. The distinct and widely distributed endosymbiotic relationships in the morning glory family and their alkaloids provide an accessible study system for understanding heritable plant-fungal symbiosis evolution and their potential functions for host plants.

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Symbiotic fungi mediate important energy and nutrient transfers in terrestrial ecosystems. Environmental change can lead to shifts in communities of symbiotic fungi, but the consequences of these shifts for nutrient dynamics among symbiotic partners are poorly understood. Here, we assessed variation in carbon (C), nitrogen (N) and phosphorus (P) in tissues of arbuscular mycorrhizal (AM) fungi and a host plant (Medicago sativa) in response to experimental warming and drought. We linked compositional shifts in AM fungal communities in roots and soil to variation in hyphal chemistry by using high-throughput DNA sequencing and joint species distribution modelling. Compared to plants, AM hyphae was 43% lower in (C) and 24% lower in (N) but more than nine times higher in (P), with significantly lower C:N, C:P and N:P ratios. Warming and drought resulted in increases in (P) and reduced C:P and N:P ratios in all tissues, indicating fungal P accumulation was exacerbated by climate-associated stress. Warming and drought modified the composition of AM fungal communities, and many of the AM fungal genera that were linked to shifts in mycelial chemistry were also negatively impacted by climate variation. Our study offers a unified framework to link climate change, fungal community composition, and community-level functional traits. Thus, our study provides insight into how environmental change can alter ecosystem functions via the promotion or reduction of fungal taxa with different stoichiometric characteristics and responses.

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AIM To study the secondary metabolites from symbiotic fungi Talaromyces amestolkiae of Syngnathus acus Linnaeus.METHODS The methanol extract from Talaromyces amestolkiae fermentation was isolated and purified by silica gel,Sephadex LH-20,TLC and preparative HPLC,then the structures of obtained compounds were identified by physicochemical properties and spectral data.RESULTS Ten compounds were isolated and identified as 2,4-bis(1,1-dimethylethyl)benzeneethanol(1),aspergillumarins A(2),peniciisocoumarins H(3),2-(2-hydroxypropyl)-5-methyl-7-hydroxychromone(4),6-demethylvermistatin(5),penicimarin B(6),penicimarin C(7),8-hydroxy-6-methoxy-3-methylisocoumarin(8),polygonolide(9),ganoderpurine(10).CONCLUSION Compound 1 is a new natural product.Compounds 3-5,8-10 are isolated from this fungi for the first time.

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Arsenic contamination causes numerous health problems for humans and wildlife via bioaccumulation in the food chain. Phytoremediation of arsenic-contaminated soils with the model arsenic hyperaccumulator Pteris vittata provides a promising way to reduce the risk, in which the growth and arsenic absorption ability of plants and the biotransformation of soil arsenic may be greatly affected by rhizosphere microorganisms. However, the microbial community composition in the rhizosphere of P. vittata and its functional role in arsenic phytoremediation are still poorly understood. To bridge this knowledge gap, we carried out a field investigation and pot experiment to explore the composition and functional implications of microbial communities in the rhizosphere of four P. vittata populations with a natural arsenic contamination gradient. Arsenic pollution significantly reduced bacterial and fungal diversity in the rhizosphere of P. vittata (p < 0.05) and played an important role in shaping the microbial community structure. The suitability of soil microbes for the growth of P. vittata gradually decreased following increased soil arsenic levels, as indicated by the increased abundance of pathogenic fungi and parasitic bacteria and the decrease in symbiotic fungi. The analysis of arsenic-related functional gene abundance with AsChip revealed the gradual enrichment of the microbial genes involved in As(III) oxidation, As(V) reduction, and arsenic methylation and demethylation in the rhizosphere of P. vittata following increased arsenic levels (p < 0.05). The regulation of indigenous soil microbes through the field application of fungicide, but not bactericide, significantly reduced the remediation efficiency of P. vittata grown under an arsenic contamination gradient, indicating the important role of indigenous fungal groups in the remediation of arsenic-contaminated soil. This study has important implications for the functional role and application prospects of soil microorganisms in the phytoremediation of arsenic-polluted soil.

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Soil aggregation and aggregate-associated carbon (C) play an essential function in soil health and C sequestration. Arbuscular mycorrhizal fungi (AMF) are considered to be primary soil aggregators due to the combined effect of extraradical hyphae and glomalin-related soil proteins (GRSPs). However, the effects of diversity and network complexity of AMF community on stability of soil aggregates and their associated C under long-term climate change (CC) and land-use conversion (LUC) in relatively high-latitude regions are largely unexplored. Therefore, an 8-year soil plot (with a 30-year cropping history) transplantation experiment was conducted to simulate CC and LUC from cropland to fallow land. The results showed that Glomus, Paraglomus, and Archaeospora were the most abundant genera. The diversity of AMF community in fallow land was higher than cropland and increased with increasing of mean annual temperature (MAT) and mean annual precipitation (MAP). Fallow land enhanced the network complexity of AMF community. The abundance families (Glomeraceae and Paraglomeraceae) exhibited higher values of topological features and were more often located in central ecological positions. Long-term fallow land had a significantly higher hyphal length density, GRSP, mean weight diameter (MWD), geometric mean diameter (GMD), and C concentration of GRSP (C-GRSP) than the cropland. The soil aggregate associated soil organic carbon (SOC) was 16.8, 18.6, and 13.8% higher under fallow land compared to that under cropland at HLJ, JL, and LN study sites, respectively. The structural equation model and random forest regression revealed that AMF diversity, network complexity, and their secreted GRSP mediate the effects of CC and LUC on C-GRSP and aggregate-associated SOC. This study elucidates the climate sensitivity of C within GRSP and soil aggregates which response symmetry to LUC and highlights the potential importance of AMF in C sequestration and climate change mitigation.

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With the rapid development of industrialization and urbanization, soil contamination with heavy metal (HM) has gradually become a global environmental problem. Lead (Pb) is one of the most abundant toxic metals in soil and high concentrations of Pb can inhibit plant growth, harm human health, and damage soil properties, including quality and stability. Arbuscular mycorrhizal fungi (AMF) are a type of obligate symbiotic soil microorganism forming symbiotic associations with most terrestrial plants, which play an essential role in the remediation of HM-polluted soils. In this study, we investigated the effects of AMF on the stability of soil aggregates under Pb stress in a pot experiment. The results showed that the hyphal density (HLD) and spore density (SPD) of the AMF in the soil were significantly reduced at Pb stress levels of 1000 mg kg−1 and 2000 mg kg−1. AMF inoculation strongly improved the concentration of glomalin-related soil protein (GRSP). The percentage of soil particles >2 mm and 2−1 mm in the AMF-inoculation treatment was higher than that in the non-AMF-inoculation treatment, while the Pb stress increased the percentage of soil particles <0.053 mm and 0.25−0.53 mm. HLD, total glomalin-related soil protein (T-GRSP), and easily extractable glomalin-related soil protein (EE-GRSP) were the three dominant factors regulating the stability of the soil aggregates, based on the random forest model analysis. Furthermore, the structural equation modeling analysis indicated that the Pb stress exerted an indirect effect on the soil-aggregate stability by regulating the HLD or the GRSP, while only the GRSP had a direct effect on the mean weight diameter (MWD) and geometric mean diameter (GMD). The current study increases the understanding of the mechanism through which soil degradation is caused by Pb stress, and emphasizes the crucial importance of glomalin in maintaining the soil-aggregate stability in HM-contaminated ecosystems.

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Historically, Hyaloscypha s. lat. (Hyaloscyphaceae, Helotiales) included various saprobes with small apothecia formed on decaying plant matter, usually wood, that were defined by chemical and (ultra)structural aspects. However, recent molecular phylogenetic and resynthesis studies have narrowed the concept of the genus and shown that it contains several widely distributed species with unknown sexual morphs that form ectomycorrhizae, ericoid mycorrhizae, and mycothalli and also grow endophytically in plant roots and hypogeous ectomycorrhizal (EcM) fruitbodies (i.e., the historical Hymenoscyphus ericae aggregate). Hence, some of the sexually reproducing saprobic Hyaloscypha s. lat. and the symbionts belong to the monophyletic Hyaloscypha s. str. Here, we introduce two new root-symbiotic Hyaloscypha s. str. species, i.e., H. gabretae and H. gryndleri spp. nov. While the former was isolated only from ericaceous hosts (Vaccinium myrtillus from Southern Bohemia, Czechia and Calluna vulgaris from England, UK), the latter was obtained from a basidiomycetous EcM root tip of Picea abies (Pinaceae), roots of Pseudorchis albida (Orchidaceae), and hair roots of V. myrtillus from Southern Bohemia and C. vulgaris from England. Hyaloscypha gryndleri comprises two closely related lineages, suggesting ongoing speciation, possibly connected with the root-symbiotic life-style. Fungal isolates from ericaceous roots with sequences similar to H. gabretae and H. gryndleri have been obtained in Japan and in Canada and Norway, respectively, suggesting a wide and scattered distribution across the Northern Hemisphere. In a series of in vitro experiments, both new species failed to form orchid mycorrhizal structures in roots of P. albida and H. gryndleri repeatedly formed what morphologically corresponds to the ericoid mycorrhizal (ErM) symbiosis in hair roots of V. myrtillus, whereas the ErM potential of H. gabretae remained unresolved. Our results highlight the symbiotic plasticity of root-associated hyaloscyphoid mycobionts as well as our limited knowledge of their diversity and distribution, warranting further ecophysiological and taxonomic research of these important and widespread fungi.

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