plant-AMF Interactions Research Articles

Mitigating gadolinium toxicity in guar (Cyamopsis tetragonoloba L.) through the symbiotic associations with arbuscular mycorrhizal fungi: physiological and biochemical insights

BackgroundGadolinium (Gd) is an increasingly found lanthanide element in soil; thus, understanding its impact on plant physiology, biochemistry, and molecular responses is crucial. Here, we aimed to provide a comprehensive understanding of Gd (150 mg kg− 1) impacts on guar (Cyamopsis tetragonoloba L.) plant yield and metabolism and whether the symbiotic relationship with arbuscular mycorrhizal fungi (AMF) can mitigate Gd toxicity of soil contamination.ResultsAMF treatment improved mineral nutrient uptake and seed yield by 38–41% under Gd stress compared to non-inoculated stressed plants. Metabolic analysis unveiled the defense mechanisms adopted by AMF-treated plants, revealing carbon and nitrogen metabolism adaptations to withstand Gd contamination. This included an increase in the synthesis of primary metabolites, such as total sugar (+ 39% compared to control), soluble sugars (+ 29%), starch (+ 30%), and some main amino acids like proline (+ 57%) and phenylalanine (+ 87%) in the seeds of AMF-treated plants grown under Gd contamination. Furthermore, fatty acid and organic acid profile changes were accompanied by the production of secondary metabolites, including tocopherols, polyamines, phenolic acids, flavones, and anthocyanins.ConclusionsOverall, the coordinated synthesis of these compounds underscores the intricate regulatory mechanisms underlying plant-AMF interactions and highlights the potential of AMF to modulate plant secondary metabolism for enhanced Gd stress tolerance.

Plant-Mycorrhizal Fungi Interactions in Phytoremediation of Geogenic Contaminated Soils.

Soil contamination by geogenic contaminants (GCs) represents an imperative environmental problem. Various soil remediation methods have been successfully employed to ameliorate the health risks associated with GCs. Phytoremediation is considered as an eco-friendly and economical approach to revegetate GC-contaminated soils. However, it is a very slow process, as plants take a considerable amount of time to gain biomass. Also, the process is limited only to the depth and surface area of the root. Inoculation of arbuscular mycorrhizal fungi (AMF) with remediating plants has been found to accelerate the phytoremediation process by enhancing plant biomass and their metal accumulation potential while improving the soil physicochemical and biological characteristics. Progress in the field application is hindered by a lack of understanding of complex interactions between host plant and AMF that contribute to metal detoxification/(im)mobilization/accumulation/translocation. Thus, this review is an attempt to reveal the underlying mechanisms of plant-AMF interactions in phytoremediation.

Global negative effects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality.

Despite widespread anthropogenic nutrient enrichment, it remains unclear how nutrient enrichment influences plant-arbuscular mycorrhizal fungi (AMF) symbiosis and ecosystem multifunctionality at the global scale. Here, we conducted a meta-analysis to examine the worldwide effects of nutrient enrichment on AMF and plant diversity and ecosystem multifunctionality using data of field experiments from 136 papers. Our analyses showed that nutrient addition simultaneously decreased AMF diversity and abundance belowground and plant diversity aboveground at the global scale. The decreases in AMF diversity and abundance associated with nutrient addition were more pronounced with increasing experimental duration, mean annual temperature (MAT) and mean annual precipitation (MAP). Nutrient addition-induced changes in soil pH and available phosphorus (P) predominantly regulated the responses of AMF diversity and abundance. Furthermore, AMF diversity correlated with ecosystem multifunctionality under nutrient addition worldwide. Our findings identify the negative effects of nutrient enrichment on AMF and plant diversity and suggest that AMF diversity is closely linked with ecosystem function. This study offers an important advancement in our understanding of plant-AMF interactions and their likely responses to ongoing global change.

An arbuscular mycorrhizal fungus alters switchgrass growth, root architecture, and cell wall chemistry across a soil moisture gradient.

The abiotic environment can dictate the relative costs and benefits of plant-arbuscular mycorrhizal fungi (AMF) symbioses. While the effects of varying light or soil nutrient conditions are well studied, outcomes of plant-AMF interactions along soil moisture gradients are not fully understood. It is predicted that mycorrhizal associations may become parasitic in extreme soil moisture conditions. Under low soil moisture stress, costs of maintaining a mycorrhizal symbiont may outweigh benefits for the host plant, whereas under high soil moisture stress, the host plant may not need the symbiont. In a factorial growth chamber study, we investigated the effects of a plant-arbuscular mycorrhizal fungus symbiosis along a soil moisture gradient on growth, cell wall chemistry, and root architecture of a biofuel crop, Panicum virgatum (switchgrass). Regardless of soil moisture conditions, we found an increase in the number of tillers, number of leaves, root biomass, and amount of cellulose and hemicellulose in response to root colonization by the arbuscular mycorrhizal fungus. The fungus also increased aboveground biomass and changed several root architectural traits, but only under low soil moisture conditions, indicating a reduction in benefits of the mycorrhizal association under high soil moisture. Results from this study indicate that an arbuscular mycorrhizal fungus can increase some key measures of plant growth and cell wall chemistry regardless of soil moisture conditions but is most beneficial in low soil moisture conditions.

Fungal Facilitation in Rangelands: Do Arbuscular Mycorrhizal Fungi Mediate Resilience and Resistance in Sagebrush Steppe?

Arbuscular mycorrhizal fungi (AMF) may exert profound influences on ecosystem resilience and invasion resistance in rangelands. Maintenance of plant community structure through ecological feedback mechanisms such as facilitation of nutrient cycling and uptake by host plants, physical and chemical contributions to soil structural stability, and mediation of plant competition suggest AMF may be important facilitators in stressful arid environments. Plant-AMF interactions could influence succession by increasing native plant community resilience to drought, grazing, and fire and resistance to exotic plant invasion. However, invasive exotic plants may benefit from associations with, as well as alter, native AMF communities. Furthermore, questions remain on the role of AMF in stressful environments, specifically the mycorrhizal dependency of sagebrush (Artemisia spp.) steppe plant species. Here, we review scientific literature relevant to AMF in rangelands, with specific focus on impacts of land management, disturbance, and invasion on AMF communities in sagebrush steppe. We highlight the nature of AMF ecology as it relates to rangelands and discuss the methods used to measure mycorrhizal responsiveness. Our review found compelling evidence that AMF mediation of resilience to disturbance and resistance to invasion varies with plant and fungal community composition, including plant mycorrhizal host status, plant functional guild, and physiological adaptations to disturbance in both plants and fungi. We conclude by outlining a framework to advance knowledge of AMF in rangeland invasion ecology. Understanding the role of AMF in semiarid sagebrush steppe ecosystems will likely require multiple study approaches due to the highly variable nature of plant-AMF interactions, the complex mechanisms of resilience conference, and the unknown thresholds for responses to environmental stressors. This may require shifting away from the plant biomass paradigm of assessing mycorrhizal benefits in order to obtain a more holistic view of plant dependency on AMF, or lack thereof, in sagebrush steppe and other semiarid ecosystems.

Arbuscular mycorrhizal colonization of selected herbaceous plants under arid protected area in Tunisia

ABSTRACT Arbuscular mycorrhizal fungi (AMF) play an important role in plants growth and soils dynamic in all most ecosystems. The main objective of the present study was to evaluate the plant-AMF interactions on soil functions under arid protected area ‘Zarat-Gabès’ in Tunisia. AMF colonization was evaluated by visual observation of AMF in fine roots of eight herbaceous plants. The level of mycorrhizal colonization varied between plants. Astragalus corrugatus and Hippocrepis areolata showed the highest mycorrhizal performance. The relative spore number was significantly different across rhizosphere soils. Statistical analysis showed a clearly positive correlation between the number of spores and plant-mycorrhizal intensity. For microbiological parameters, our results showed that mycorrhizal plants improved significantly the various microbiological parameters. Rhizosphere soils of Astragalus corrugatus and Hippocrepis areolata presented the necessary microbial densities and microorganisms more stable compared to unplanted soil. This study allowed obtaining a new result that challenges us about the need for efficient management of natural resources in the objective of nature conservation.

Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi.

High-through-put (HTP) screening for functional arbuscular mycorrhizal fungi (AMF)-associations is challenging because roots must be excavated and colonization evaluated by transcript analysis or microscopy. Here we show that specific leaf-metabolites provide broadly applicable accurate proxies of these associations, suitable for HTP-screens. With a combination of untargeted and targeted metabolomics, we show that shoot accumulations of hydroxy- and carboxyblumenol C-glucosides mirror root AMF-colonization in Nicotiana attenuata plants. Genetic/pharmacologic manipulations indicate that these AMF-indicative foliar blumenols are synthesized and transported from roots to shoots. These blumenol-derived foliar markers, found in many di- and monocotyledonous crop and model plants (Solanum lycopersicum, Solanum tuberosum, Hordeum vulgare, Triticum aestivum, Medicago truncatula and Brachypodium distachyon), are not restricted to particular plant-AMF interactions, and are shown to be applicable for field-based QTL mapping of AMF-related genes.

High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis.

Arbuscular mycorrhizal fungi (AMF) are known to improve plant fitness through the establishment of mycorrhizal symbioses. Genetic and phenotypic variations among closely related AMF isolates can significantly affect plant growth, but the genomic changes underlying this variability are unclear. To address this issue, we improved the genome assembly and gene annotation of the model strain Rhizophagus irregularis DAOM197198, and compared its gene content with five isolates of R.irregularis sampled in the same field. All isolates harbor striking genome variations, with large numbers of isolate-specific genes, gene family expansions, and evidence of interisolate genetic exchange. The observed variability affects all gene ontology terms and PFAM protein domains, as well as putative mycorrhiza-induced small secreted effector-like proteins and other symbiosis differentially expressed genes. High variability is also found in active transposable elements. Overall, these findings indicate a substantial divergence in the functioning capacity of isolates harvested from the same field, and thus their genetic potential for adaptation to biotic and abiotic changes. Our data also provide a first glimpse into the genome diversity that resides within natural populations of these symbionts, and open avenues for future analyses of plant-AMF interactions that link AMF genome variation with plant phenotype and fitness.

What drives differences in arbuscular mycorrhizal fungal communities among plant species?

Abstract Plant species can influence communities of arbuscular mycorrhizal fungi (AMF) by hosting different AMF taxon identities and/or richness. We used presence/absence data from a recent global survey of AMF communities to assess how often AMF communities differ among plant species, and to explore whether differences result from dissimilarities in AMF taxon identity or richness. We found that AMF communities clustered among plant species in 24% of sites, and that plant species were more likely to differ in AMF taxon richness (23% of sites) than the particular taxa with which they associate (5% of sites). Overall though, the variation in both AMF richness and identity was often as great within as between plant species, suggesting that plant species identity may be less important for structuring local AMF communities than other factors, such as environmental conditions, fungal interactions or even stochastic distributions of AMF. This has implications for how we should view plant-AMF interactions and community patterns.

Virus-Induced Gene Silencing Using Tobacco Rattle Virus as a Tool to Study the Interaction between Nicotiana attenuata and Rhizophagus irregularis.

Most land plants live in a symbiotic association with arbuscular mycorrhizal fungi (AMF) that belong to the phylum Glomeromycota. Although a number of plant genes involved in the plant-AMF interactions have been identified by analyzing mutants, the ability to rapidly manipulate gene expression to study the potential functions of new candidate genes remains unrealized. We analyzed changes in gene expression of wild tobacco roots (Nicotiana attenuata) after infection with mycorrhizal fungi (Rhizophagus irregularis) by serial analysis of gene expression (SuperSAGE) combined with next generation sequencing, and established a virus-induced gene-silencing protocol to study the function of candidate genes in the interaction. From 92,434 SuperSAGE Tag sequences, 32,808 (35%) matched with our in-house Nicotiana attenuata transcriptome database and 3,698 (4%) matched to Rhizophagus genes. In total, 11,194 Tags showed a significant change in expression (p<0.05, >2-fold change) after infection. When comparing the functions of highly up-regulated annotated Tags in this study with those of two previous large-scale gene expression studies, 18 gene functions were found to be up-regulated in all three studies mainly playing roles related to phytohormone metabolism, catabolism and defense. To validate the function of identified candidate genes, we used the technique of virus-induced gene silencing (VIGS) to silence the expression of three putative N. attenuata genes: germin-like protein, indole-3-acetic acid-amido synthetase GH3.9 and, as a proof-of-principle, calcium and calmodulin-dependent protein kinase (CCaMK). The silencing of the three plant genes in roots was successful, but only CCaMK silencing had a significant effect on the interaction with R. irregularis. Interestingly, when a highly activated inoculum was used for plant inoculation, the effect of CCaMK silencing on fungal colonization was masked, probably due to trans-complementation. This study demonstrates that large-scale gene expression studies across different species induce of a core set of genes of similar functions. However, additional factors seem to influence the overall pattern of gene expression, resulting in high variability among independent studies with different hosts. We conclude that VIGS is a powerful tool with which to investigate the function of genes involved in plant-AMF interactions but that inoculum strength can strongly influence the outcome of the interaction.

Evidence for phylogenetic correlation of plant-AMF assemblages?

Specificity in biotic interactions is mediated' by functional traits inducing shifts in the community species composition. Functional traits are often evolutionarily conserved, resulting in closely related species tending to interact with similar species. This tendency may initially shape the phylogenetic composition of coexisting guilds, but other intraguild ecological processes may either blur or promote the mirroring of the phylogenetic compositions between guilds. The roles of intra- and interguild interactions in shaping the phylogenetic community composition are largely unknown, beyond the mere selectivity in the interguild interactions. Plant facilitation is a phylogenetically structured species-specific process involving interactions not only between the same guild of plants, but also between plants and other guilds such as arbuscular mycorrhizal fungi (AMF). In this study it is hypothesized that reciprocal plant-AMF interactions will leave an interdependent phylogenetic signal in the community composition of both plants and AMF. A correlation was used to test for a relationship between the phylogenetic composition of plant and AMF assemblages in a patchy xeric shrubland environment shaped by plant facilitation. In addition, a null model was used to test whether this correlation can be solely explained by selectivity in plant-AMF interactions. A significant correlation was observed between the phylogenetic composition of plant and AMF assemblages. Plant phylogenetic composition in a patch was related to the predominance of plant species with high nursery quality that can influence the community assembly. AMF phylogenetic composition was related to the AMF phylogenetic diversity in each patch. This study shows that shifts in the phylogenetic composition of plants and AMF assemblages do not occur independently. It is suggested that besides selectivity in plant-AMF interactions, inter-related succession dynamics of plants and AMF within patches could be an ecological mechanism driving community assembly. Future lines of research might explore whether interlinked above- and below-ground dynamics could be occurring across multiple guilds simultaneously.

Foliar Spray with Vermiwash Modifies the Arbuscular Mycorrhizal Dependency and Nutrient Stoichiometry of Bhut Jolokia (Capsicum assamicum)

Vermiwash (VW), a liquid extract obtained from vermicomposting beds, is used as an organic fertilizer for crop plants. The current study investigated the effect of a vermiwash foliar spray on the response of bhut jolokia (Capsicum assamicum) exposed to two different arbuscular mycorrhizal fungi (AMF: Rhizophagus irregularis, RI and G. mosseae, GM) in acidic soil under naturally ventilated greenhouse conditions. The VW spray significantly influenced the growth of plants receiving the dual treatment of AMF+VW. Plant growth was more prominent in the GM+VW treatment group than that in the RI+VW treatment group. The plant-AMF interactions in relation to growth and nutrient requirements were also significantly influenced by the application of VW. Interestingly, the VW treatment appeared to contribute more N to plants when compared to that under the AMF treatment, which led to changes in the C:N:P stoichiometry in plant shoots. Furthermore, the increased potassium dependency, as observed in the case of the dual treatments, suggests the significance of such treatments for improving crop conditions under salt stress. Overall, our study shows that the VW foliar spray modifies the response of a crop to inoculations of different AMF with regard to growth and nutrient utilization, which has implications for the selection of an efficient combination of nutrient source for improving crop growth.

Diversity of arbuscular mycorrhizal fungal spore communities and its relations to plants under increased temperature and precipitation in a natural grassland

Arbuscular mycorrhizal fungi (AMF) form mutualisms with most plant species, and therefore, understanding how AMF communities will respond to climate change is essential for predictions of changes in plant communities. To evaluate the impact of global climate change on AMFs and plant-AMF interactions in a natural grassland in Inner Mongolia, both artificial warming and watering treatments were assigned to experimental plots. Our results indicate that (1) warming and precipitation significantly affected the relative spore abundance of abundant sporulating AMF species; (2) the relative abundance of weak sporulating AMF species and AMF diversity decreased under experimental warming; (3) evidence was found that the composition of the AMF community in a given year might be correlated with plant community composition in the following year; and (4) grasses and forbs showing different preferences to Claroideoglomus etunicatum or Ambispora gerdemannii dominated plots. Our results imply that climate change appears to induce changes in AMF assemblages with knock-on effects on grassland plant communities. AMF communities may play a much more important role than we have thought in the responses of ecosystem to global climate changes. global warming, precipitation increase, Arbuscular mycorrhiza, plant-AMF relations, grassland ecosystem

Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi

Complementary beneficial effects of different arbuscular mycorrhizal fungi (AMF) can result in a more efficient exploitation of the soil nutrients available, thus influencing plant communities. Here, we hypothesize that plant-AMF specificity is mediated by phylogenetic constraints defining possible interactions, and that plant-AMF interaction patterns can influence plant-plant facilitation specificity. We reanalyzed previous data describing plant-plant and plant-AMF interaction at the community level to specifically test for a phylogenetic signal on plant and AMF interactions and for a relationship between plant-plant facilitation specificity and plant species differences in their AMF associates. Closely related AMF operational taxonomical units (OTUs) tend to interact with the same plant species, but there is not a significant signal in the interaction through the plant phylogeny. This indicates that the similarity in the AMF associates of two plant species is independent of their phylogenetic relatedness. Interestingly, plant-AMF interactions match plant facilitation specificity, with pairs of plant species recruiting more frequently under each other tending to have different AMF associates. An increment of AMF diversity in the rhizosphere, as a result of plant-AMF and plant-plant selectivity, is suggested as a potential driver of plant-plant facilitation. This study highlights the role of plant-AMF interactions in shaping plant community assemblages.

Arbuscular mycorrhizal fungal community differs between a coexisting native shrub and introduced annual grass

Arbuscular mycorrhizal fungi (AMF) have been implicated in non-native plant invasion success and persistence. However, few studies have identified the AMF species associating directly with plant invaders, or how these associations differ from those of native plant species. Identifying changes to the AMF community due to plant invasion could yield key plant-AMF interactions necessary for the restoration of native plant communities. This research compared AMF associating with coexisting Bromus tectorum, an invasive annual grass, and Artemisia tridentata, the dominant native shrub in western North America. At three sites, soil and root samples from Bromus and Artemisia were collected. Sporulation was induced using trap cultures, and spores were identified using morphological characteristics. DNA was extracted from root and soil subsamples and amplified. Sequences obtained were aligned and analyzed to compare diversity, composition, and phylogenetic distance between hosts and sites. Richness of AMF species associated with Artemisia in cultures was higher than AMF species associated with Bromus. Gamma diversity was similar and beta diversity was higher in AMF associated with Bromus compared to Artemisia. AMF community composition differed between hosts in both cultures and roots. Two AMF species (Archaeospora trappei and Viscospora viscosum) associated more frequently with Artemisia than Bromus across multiple sites. AMF communities in Bromus roots were more phylogenetically dispersed than in Artemisia roots, indicating a greater competition for resources within the invasive grass. Bromus associated with an AMF community that differed from Artemisia in a number of ways, and these changes could restrict native plant establishment.

Serpentine and non‐serpentine ecotypes of Collinsia sparsiflora associate with distinct arbuscular mycorrhizal fungal assemblages

Although plant adaptation to serpentine soils has been studied for several decades, the mechanisms of plant adaptation to edaphic extremes are still poorly understood. Arbuscular mycorrhizal fungi (AMF) are common root symbionts that can increase the plant hosts' establishment and growth in stressful environments. However, little is known about the role plant-AMF interactions play in plant adaptation to serpentine. As a first step towards understanding this role, we examined the AMF assemblages associated with field populations of serpentine and non-serpentine ecotypes of California native plant Collinsia sparsiflora. We sampled roots of C. sparsiflora from three serpentine and three non-serpentine sites in close proximity (110 m to 1.94 km between sites) and analysed the small subunit ribosomal DNA gene amplified from root DNA extracts using AMF-specific primers. A total of 1952 clones from 24 root samples (four from each site) were sequenced. We used sequence similarity and phylogenetic analysis to determine operational taxonomic units (OTU) resulting in 19 OTUs representing taxa from six AMF genera, including one serpentine-specific OTU. We used Bray-Curtis similarity, multidimensional scaling and analysis of similarity to compare root sample AMF assemblages. These analyses clearly showed that plant ecotypes associated with distinct AMF assemblages; an Acaulospora OTU-dominated serpentine, and a Glomus OTU-dominated non-serpentine assemblages. Species diversity and evenness were significantly higher in serpentine assemblages. Finally, relate analysis showed a relationship between ecotype AMF assemblages and soil nutrients. This study reveals a strong relationship between AMF associates and plant adaptation to edaphic extremes.