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1.  An aboveground pathogen inhibits belowground rhizobia and arbuscular mycorrhizal fungi in Phaseolus vulgaris 
BMC Plant Biology  2014;14(1):321.
Induced aboveground plant defenses against pathogens can have negative effects on belowground microbial symbionts. While a considerable number of studies have utilized chemical elicitors to experimentally induce such defenses, there is surprisingly little evidence that actual aboveground pathogens affect root-associated microbes. We report here that an aboveground fungal pathogen of common bean (Phaseolus vulgaris) induces a defense response that inhibits both the belowground formation of root nodules elicited by rhizobia and the colonization with arbuscular mycorrhizal fungi (AMF).
Foliage of plants inoculated with either rhizobia or AMF was treated with both live Colletotrichum gloeosporioides—a generalist hemibiotrophic plant pathogen—and C. gloeosporioides fragments. Polyphenol oxidase (PPO), chitinase and β-1,3-glucanase activity in leaves and roots, as well as the number of rhizobia nodules and the extent of AMF colonization, were measured after pathogen treatments. Both the live pathogen and pathogen fragments significantly increased PPO, chitinase and β-1,3-glucanase activity in the leaves, but only PPO activity was increased in roots. The number of rhizobia nodules and the extent of AMF colonization was significantly reduced in treatment plants when compared to controls.
We demonstrate that aboveground fungal pathogens can affect belowground mutualism with two very different types of microbial symbionts—rhizobia and AMF. Our results suggest that systemically induced PPO activity is functionally involved in this above-belowground interaction. We predict that the top-down effects we show here can drastically impact plant performance in soils with limited nutrients and water; abiotic stress conditions usually mitigated by microbial belowground mutualists.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0321-4) contains supplementary material, which is available to authorized users.
PMCID: PMC4248430  PMID: 25429887
Colletotrichum gloeosporioides; Induced response; Plant defense; Plant–pathogen interaction; Polyphenol oxidase; Tradeoff
2.  Combined inoculation with Glomus intraradices and Rhizobium tropici CIAT899 increases phosphorus use efficiency for symbiotic nitrogen fixation in common bean (Phaseolus vulgaris L.) 
This study compared the response of common bean (Phaseolus vulgaris L.) to arbuscular mycorrhizal fungi (AMF) and rhizobia strain inoculation. Two common bean genotypes i.e. CocoT and Flamingo varying in their effectiveness for nitrogen fixation were inoculated with Glomus intraradices and Rhizobium tropici CIAT899, and grown for 50 days in soil–sand substrate in glasshouse conditions. Inoculation of common bean plants with the AM fungi resulted in a significant increase in nodulation compared to plants without inoculation. The combined inoculation of AM fungi and rhizobia significantly increased various plant growth parameters compared to simple inoculated plants. In addition, the combined inoculation of AM fungi and rhizobia resulted in significantly higher nitrogen and phosphorus accumulation in the shoots of common bean plants and improved phosphorus use efficiency compared with their controls, which were not dually inoculated. It is concluded that inoculation with rhizobia and arbuscular mycorrhizal fungi could improve the efficiency in phosphorus use for symbiotic nitrogen fixation especially under phosphorus deficiency.
PMCID: PMC3730892  PMID: 23961175
Arbuscular mycorrhizal fungi; Glomus intraradices; Nitrogen fixation; Phaseolus vulgaris; Phosphorus; Rhizobia; Symbiosis
3.  Isolate Identity Determines Plant Tolerance to Pathogen Attack in Assembled Mycorrhizal Communities 
PLoS ONE  2013;8(4):e61329.
Arbuscular mycorrhizal fungi (AMF) are widespread soil microorganisms that associate mutualistically with plant hosts. AMF receive photosynthates from the host in return for various benefits. One of such benefits is in the form of enhanced pathogen tolerance. However, this aspect of the symbiosis has been understudied compared to effects on plant growth and its ability to acquire nutrients. While it is known that increased AMF species richness positively correlates with plant productivity, the relationship between AMF diversity and host responses to pathogen attack remains obscure. The objective of this study was to test whether AMF isolates can differentially attenuate the deleterious effects of a root pathogen on plant growth, whether the richest assemblage of AMF isolates provides the most tolerance against the pathogen, and whether AMF-induced changes to root architecture serve as a mechanism for improved plant disease tolerance. In a growth chamber study, we exposed the plant oxeye daisy (Leucanthemum vulgare) to all combinations of three AMF isolates and to the plant root pathogen Rhizoctonia solani. We found that the pathogen caused an 81% reduction in shoot and a 70% reduction in root biomass. AMF significantly reduced the highly deleterious effect of the pathogen. Mycorrhizal plants infected with the pathogen produced 91% more dry shoot biomass and 72% more dry root biomass relative to plants solely infected with R. solani. AMF isolate identity was a better predictor of AMF-mediated host tolerance to the pathogen than AMF richness. However, the enhanced tolerance response did not result from AMF-mediated changes to root architecture. Our data indicate that AMF communities can play a major role in alleviating host pathogen attack but this depends primarily on the capacity of individual AMF isolates to provide this benefit.
PMCID: PMC3631226  PMID: 23620744
4.  Arbuscular mycorrhizal fungi reduce effects of physiological integration in Trifolium repens 
Annals of Botany  2009;104(2):335-344.
Background and Aims
One of the special properties of clonal plants is the capacity for physiological integration, which can increase plant performance through mechanisms such as resource sharing and co-ordinated phenotypic plasticity when plants grow in microsites with contrasting resource availabilities. However, many clonal plants are colonized by arbuscular mycorrhizal fungi (AMF). Since AMF are likely to reduce contrasts in effective resource levels, they could also reduce these effects of clonal integration on plasticity and performance in heterogeneous environments.
To test this hypothesis, pairs of connected and disconnected ramets of the stoloniferous herb Trifolium repens were grown. One ramet in a pair was given high light and low nutrients while the other ramet was given high nutrients and low light. The pairs were inoculated with zero, one or five species of AMF.
Key Results
Pairs of ramets grown without AMF developed division of labour and benefited from resource sharing, as indicated by effects of connection on allocation to roots, accumulation of mass, and ramet production. Inoculation with five species of AMF significantly reduced these effects of connection, both by inhibiting them in ramets given high nutrients and inducing them in ramets given high light. Inoculation with one species of AMF also reduced some effects of connection, but generally to a lesser degree.
The results show that AMF can significantly modify the effects of clonal integration on the plasticity and performance of clonal plants in heterogeneous environments. In particular, AMF may partly replace the effects and benefits of clonal integration in low-nutrient habitats, possibly more so where species richness of AMF is high. This provides the first test of interaction between colonization by AMF and physiological integration in a clonal plant, and a new example of how biotic and abiotic factors could interact to determine the ecological importance of clonal growth.
PMCID: PMC2710896  PMID: 19493856
Arbuscular mycorrhizal fungi; biomass allocation; clonal plant; division of labour; environmental heterogeneity; light availability; nutrients; white clover
5.  Effect of Arbuscular Mycorrhizal Fungi on Plant Biomass and the Rhizosphere Microbial Community Structure of Mesquite Grown in Acidic Lead/Zinc Mine Tailings 
The Science of the total environment  2011;409(6):1009-1016.
Mine tailings in arid and semi-arid environments are barren of vegetation and subject to eolian dispersion and water erosion. Revegetation is a cost-effective strategy to reduce erosion processes and has wide public acceptance. A major cost of revegetation is the addition of amendments, such as compost, to allow plant establishment. In this paper we explore whether arbuscular mycorrhizal fungi (AMF) can help support plant growth in tailings at a reduced compost concentration. A greenhouse experiment was performed to determine the effects of three AMF inocula on biomass, shoot accumulation of heavy metals, and changes in the rhizosphere microbial community structure of the native plant Prosopis juliflora (mesquite). Plants were grown in an acidic lead/zinc mine tailings amended with 10% (w/w) compost amendment, which is slightly sub-optimal for plant growth in these tailings. After two months, AMF-inoculated plants showed increased dry biomass and root length (p < 0.05) and effective AMF colonization compared to controls grown in uninoculated compost-amended tailings. Mesquite shoot tissue lead and zinc concentrations did not exceed domestic animal toxicity limits regardless of whether AMF inoculation was used. The rhizosphere microbial community structure was assessed using denaturing gradient gel electrophoresis (DGGE) profiles of the small subunit RNA gene for bacteria and fungi. Canonical correspondence analysis (CCA) of DGGE profiles showed that the rhizosphere fungal community structure at the end of the experiment was significantly different from the community structure in the tailings, compost, and AMF inocula prior to planting. Further, CCA showed that AMF inoculation significantly influenced the development of both the fungal and bacterial rhizosphere community structures after two months. The changes observed in the rhizosphere microbial community structure may be either a direct effect of the AMF inocula, caused by changes in plant physiology induced by AMF, or a combination of both mechanisms.
PMCID: PMC3030643  PMID: 21211826
Prosopis juliflora; phytostabilization; DGGE; mycorrhizal fungi; mine tailing
6.  Meta-Analysis of Interactions between Arbuscular Mycorrhizal Fungi and Biotic Stressors of Plants 
The Scientific World Journal  2014;2014:746506.
Naturally, simultaneous interactions occurred among plants, herbivores, and soil biota, that is, arbuscular mycorrhizal fungi (AMF), nematodes, and fungal pathogens. These multiple interactions play fundamental roles in driving process, structure, and functioning of ecosystems. In this study, we conducted a meta-analysis with 144 papers to investigate the interactions between AMF and plant biotic stressors and their effects on plant growth performance. We found that AMF enhanced plant tolerance to herbivores, nematodes, and fungal pathogens. We also found reciprocal inhibition between AMF and nematodes as well as fungal pathogens, but unidirectional inhibition for AMF on herbivores. Negative effects of AMF on biotic stressors of plants depended on herbivore feeding sites and actioning modes of fungal pathogens. More performance was reduced in root-feeding than in shoot-feeding herbivores and in rotting- than in wilt-fungal pathogens. However, no difference was found for AMF negative effects between migratory and sedentary nematodes. In return, nematodes and fungal pathogens generated more reduction of root colonization in Non-Glomeraceae than in Glomeraceae. Our results suggested that AMF positive effects on plants might be indirectly mediated by competitive inhibition with biotic stressors of plants. These positive and negative interactions make potential contributions to maintaining ecosystem stability and functioning.
PMCID: PMC3914602  PMID: 24558327
7.  Influence of Habitat and Climate Variables on Arbuscular Mycorrhizal Fungus Community Distribution, as Revealed by a Case Study of Facultative Plant Epiphytism under Semiarid Conditions 
Applied and Environmental Microbiology  2013;79(23):7203-7209.
In semiarid Mediterranean ecosystems, epiphytic plant species are practically absent, and only some species of palm trees can support epiphytes growing in their lower crown area, such as Phoenix dactylifera L. (date palm). In this study, we focused on Sonchus tenerrimus L. plants growing as facultative epiphytes in P. dactylifera and its terrestrial forms growing in adjacent soils. Our aim was to determine the possible presence of arbuscular mycorrhizal fungi (AMF) in these peculiar habitats and to relate AMF communities with climatic variations. We investigated the AMF community composition of epiphytic and terrestrial S. tenerrimus plants along a temperature and precipitation gradient across 12 localities. Epiphytic roots were colonized by AMF, as determined by microscopic observation; all of the epiphytic and terrestrial samples analyzed showed AMF sequences from taxa belonging to the phylum Glomeromycota, which were grouped in 30 AMF operational taxonomic units. The AMF community composition was clearly different between epiphytic and terrestrial root samples, and this could be attributable to dispersal constraints and/or the contrasting environmental and ecophysiological conditions prevailing in each habitat. Across sites, the richness and diversity of terrestrial AMF communities was positively correlated with rainfall amount during the most recent growing season. In contrast, there was no significant correlation between climate variables and AMF richness and diversity for epiphytic AMF communities, which suggests that the composition of AMF communities in epiphytic habitats appears to be largely determined by the availability and dispersion of fungal propagules from adjacent terrestrial habitats.
PMCID: PMC3837746  PMID: 24038687
8.  Hypericin and pseudohypericin concentrations of a valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal fungi 
Mycorrhiza  2011;22(2):149-156.
Hypericum perforatum L. (St. John’s-wort, Hypericaceae) is a valuable medicinal plant species cultivated for pharmaceutical purposes. Although the chemical composition and pharmacological activities of H. perforatum have been well studied, no data are available concerning the influence of arbuscular mycorrhizal fungi (AMF) on this important herb. A laboratory experiment was therefore conducted in order to test three AMF inocula on H. perforatum with a view to show whether AMF could influence plant vitality (biomass and photosynthetic activity) and the production of the most valuable secondary metabolites, namely anthraquinone derivatives (hypericin and pseudohypericin) as well as the prenylated phloroglucinol—hyperforin. The following treatments were prepared: (1) control—sterile soil without AMF inoculation, (2) Rhizophagus intraradices (syn. Glomus intraradices), (3) Funneliformis mosseae (syn. Glomus mosseae), and (4) an AMF Mix which contained: Funneliformis constrictum (syn. Glomus constrictum), Funneliformis geosporum (syn. Glomus geosporum), F. mosseae, and R. intraradices. The application of R. intraradices inoculum resulted in the highest mycorrhizal colonization, whereas the lowest values of mycorrhizal parameters were detected in the AMF Mix. There were no statistically significant differences in H. perforatum shoot mass in any of the treatments. However, we found AMF species specificity in the stimulation of H. perforatum photosynthetic activity and the production of secondary metabolites. Inoculation with the AMF Mix resulted in higher photosynthetic performance index (PItotal) values in comparison to all the other treatments. The plants inoculated with R. intraradices and the AMF Mix were characterized by a higher concentration of hypericin and pseudohypericin in the shoots. However, no differences in the content of these metabolites were detected after the application of F. mosseae. In the case of hyperforin, no significant differences were found between the control plants and those inoculated with any of the AMF applied. The enhanced content of anthraquinone derivatives and, at the same time, better plant vitality suggest that the improved production of these metabolites was a result of the positive effect of the applied AMF strains on H. perforatum. This could be due to improved mineral nutrition or to AMF-induced changes in the phytohormonal balance. Our results are promising from the biotechnological point of view, i.e. the future inoculation of H. perforatum with AMF in order to improve the quality of medicinal plant raw material obtained from cultivation.
PMCID: PMC3261393  PMID: 21626142
AMF species specificity; Anthraquinone derivatives; Arbuscular mycorrhiza; Hyperforin; Photosynthetic performance index; St. John’s-wort
9.  Communities of Arbuscular Mycorrhizal Fungi in Pyrus pyrifolia var. culta (Japanese pear) and an Understory Herbaceous Plant Plantago asiatica 
Microbes and Environments  2013;28(2):204-210.
We investigated communities of arbuscular mycorrhizal fungi (AMF) in the fine roots of Pyrus pyrifolia var. culta, and Plantago asiatica to consider the relationship between orchard trees and herbaceous plants in AMF symbioses. The AMF communities were analyzed on the basis of the partial fungal DNA sequences of the nuclear small subunit ribosomal RNA gene (SSU rDNA), which were amplified using the AMF-specific primers AML1 and AML2. Phylogenetic analysis showed that the obtained AMF sequences were divided into 23 phylotypes. Among them, 12 phylotypes included AMF from both host plants, and most of the obtained sequences (689/811) were affiliated to them. Canonical correspondence analysis showed that the host plant species did not have a significant effect on the distribution of AMF phylotypes, whereas the effects of sampling site, soil total C, soil total N and soil-available P were significant. It was also found that the mean observed overlaps of AMF phylotypes between the paired host plants in the same soil cores (27.1% of phylotypes shared) were significantly higher than the mean 1,000 simulated overlaps (14.2%). Furthermore, the same AMF sequences (100% sequence identity) were detected from both host plants in 8/12 soil cores having both roots. Accordingly, we concluded that Py. pyrifolia and Pl. asiatica examined shared some AMF communities, which suggested that understory herbaceous plants may function as AMF inoculum sources for orchard trees.
PMCID: PMC4070674  PMID: 23614902
AML1-AML2; canonical correspondence analysis (CCA); correspondence analysis (CA); Orchard; SSU rDNA
10.  A Fungal Symbiont of Plant-Roots Modulates Mycotoxin Gene Expression in the Pathogen Fusarium sambucinum 
PLoS ONE  2011;6(3):e17990.
Fusarium trichothecenes are fungal toxins that cause disease on infected plants and, more importantly, health problems for humans and animals that consume infected fruits or vegetables. Unfortunately, there are few methods for controlling mycotoxin production by fungal pathogens. In this study, we isolated and characterized sixteen Fusarium strains from naturally infected potato plants in the field. Pathogenicity tests were carried out in the greenhouse to evaluate the virulence of the strains on potato plants as well as their trichothecene production capacity, and the most aggressive strain was selected for further studies. This strain, identified as F. sambucinum, was used to determine if trichothecene gene expression was affected by the symbiotic Arbuscular mycorrhizal fungus (AMF) Glomus irregulare. AMF form symbioses with plant roots, in particular by improving their mineral nutrient uptake and protecting plants against soil-borne pathogens. We found that that G. irregulare significantly inhibits F. sambucinum growth. We also found, using RT-PCR assays to assess the relative expression of trichothecene genes, that in the presence of the AMF G. irregulare, F. sambucinum genes TRI5 and TRI6 were up-regulated, while TRI4, TRI13 and TRI101 were down-regulated. We conclude that AMF can modulate mycotoxin gene expression by a plant fungal pathogen. This previously undescribed effect may be an important mechanism for biological control and has fascinating implications for advancing our knowledge of plant-microbe interactions and controlling plant pathogens.
PMCID: PMC3063790  PMID: 21455305
11.  Effects of Inoculum Additions in the Presence of a Preestablished Arbuscular Mycorrhizal Fungal Community 
Applied and Environmental Microbiology  2013;79(20):6507-6515.
Communities of arbuscular mycorrhizal fungi (AMF) are crucial for promoting plant productivity in most terrestrial systems, including anthropogenically managed ecosystems. Application of AMF inocula has therefore become a widespread practice. It is, however, pertinent to understand the mechanisms that govern AMF community composition and their performance in order to design successful manipulations. Here we assess whether the composition and plant growth-promotional effects of a synthetic AMF community can be altered by inoculum additions of the isolates forming the community. This was determined by following the effects of three AMF isolates, each inoculated in two propagule densities into a preestablished AMF community. Fungal abundance in roots and plant growth were evaluated in three sequential harvests. We found a transient positive response in AMF abundance to the intraspecific inoculation only in the competitively weakest isolate. The other two isolates responded negatively to intra- and interspecific inoculations, and in some cases plant growth was also reduced. Our results suggest that increasing the AMF density may lead to increased competition among fungi and a trade-off with their ability to promote plant productivity. This is a key ecological aspect to consider when introducing AMF into soils.
PMCID: PMC3811198  PMID: 23956395
12.  Genetic analysis of the interaction between Allium species and arbuscular mycorrhizal fungi 
The response of Alliumcepa, A. roylei, A. fistulosum, and the hybrid A. fistulosum × A. roylei to the arbuscular mycorrhizal fungus (AMF) Glomus intraradices was studied. The genetic basis for response to AMF was analyzed in a tri-hybrid A. cepa × (A. roylei × A. fistulosum) population. Plant response to mycorrhizal symbiosis was expressed as relative mycorrhizal responsiveness (R′) and absolute responsiveness (R). In addition, the average performance (AP) of genotypes under mycorrhizal and non-mycorrhizal conditions was determined. Experiments were executed in 2 years, and comprised clonally propagated plants of each genotype grown in sterile soil, inoculated with G. intraradices or non-inoculated. Results were significantly correlated between both years. Biomass of non-mycorrhizal and mycorrhizal plants was significantly positively correlated. R′ was negatively correlated with biomass of non-mycorrhizal plants and hence unsuitable as a breeding criterion. R and AP were positively correlated with biomass of mycorrhizal and non-mycorrhizal plants. QTLs contributing to mycorrhizal response were located on a linkage map of the A. roylei × A. fistulosum parental genotype. Two QTLs from A. roylei were detected on chromosomes 2 and 3 for R, AP, and biomass of mycorrhizal plants. A QTL from A. fistulosum was detected on linkage group 9 for AP (but not R), biomass of mycorrhizal and non-mycorrhizal plants, and the number of stem-borne roots. Co-segregating QTLs for plant biomass, R and AP indicate that selection for plant biomass also selects for enhanced R and AP. Moreover, our findings suggest that modern onion breeding did not select against the response to AMF, as was suggested before for other cultivated species. Positive correlation between high number of roots, biomass and large response to AMF in close relatives of onion opens prospects to combine these traits for the development of more robust onion cultivars.
Electronic supplementary material
The online version of this article (doi:10.1007/s00122-010-1501-8) contains supplementary material, which is available to authorized users.
PMCID: PMC3043257  PMID: 21222096
13.  Community Analysis of Arbuscular Mycorrhizal Fungi in Roots of Poncirus trifoliata and Citrus reticulata Based on SSU rDNA 
The Scientific World Journal  2014;2014:562797.
Morphological observation of arbuscular mycorrhizal fungi (AMF) species in rhizospheric soil could not accurately reflect the actual AMF colonizing status in roots, while molecular identification of indigenous AMF colonizing citrus rootstocks at present was rare in China. In our study, community of AMF colonizing trifoliate orange (Poncirus trifoliata L. Raf.) and red tangerine (Citrus reticulata Blanco) were analyzed based on small subunit of ribosomal DNA genes. Morphological observation showed that arbuscular mycorrhizal (AM) colonization, spore density, and hyphal length did not differ significantly between two rootstocks. Phylogenetic analysis showed that 173 screened AMF sequences clustered in at least 10 discrete groups (GLO1~GLO10), all belonging to the genus of Glomus Sensu Lato. Among them, GLO1 clade (clustering with uncultured Glomus) accounting for 54.43% clones was the most common in trifoliate orange roots, while GLO6 clade (clustering with Glomus intraradices) accounting for 35.00% clones was the most common in red tangerine roots. Although, Shannon-Wiener indices exhibited no notable differences between both rootstocks, relative proportions of observed clades analysis revealed that composition of AMF communities colonizing two rootstocks varied severely. The results indicated that native AMF species in citrus rhizosphere had diverse colonization potential between two different rootstocks in the present orchards.
PMCID: PMC4138779  PMID: 25162057
14.  The intercropping partner affects arbuscular mycorrhizal fungi and Fusarium oxysporum f. sp. lycopersici interactions in tomato 
Mycorrhiza  2013;23(7):543-550.
Arbuscular mycorrhizal fungi (AMF) and their bioprotective aspects are of great interest in the context of sustainable agriculture. Combining the benefits of AMF with the utilisation of plant species diversity shows great promise for the management of plant diseases in environmentally compatible agriculture. In the present study, AMF were tested against Fusarium oxysporum f. sp. lycopersici with tomato intercropped with either leek, cucumber, basil, fennel or tomato itself. Arbuscular mycorrhizal (AM) root colonisation of tomato was clearly affected by its intercropping partners. Tomato intercropped with leek showed even a 20 % higher AM colonisation rate than tomato intercropped with tomato. Positive effects of AMF expressed as an increase of tomato biomass compared to the untreated control treatment could be observed in root as well as in shoot weights. A compensation of negative effects of F. oxysporum f. sp. lycopersici on tomato biomass by AMF was observed in the tomato/leek combination. The intercropping partners leek, cucumber, basil and tomato had no effect on F. oxysporum f. sp. lycopersici disease incidence or disease severity indicating no allelopathic suppression; however, tomato co-cultivated with tomato clearly showed a negative effect on one plant/pot with regard to biomass and disease severity of F. oxysporum f. sp. lycopersici. Nonetheless, bioprotective effects of AMF resulting in the decrease of F. oxysporum f. sp. lycopersici disease severity were evident in treatments with AMF and F. oxysporum f. sp. lycopersici co-inoculation. However, these bioprotective effects depended on the intercropping partner since these effects were only observed in the tomato/leek and tomato/basil combination and for the better developed plant of tomato/tomato. In conclusion, the effects of the intercropping partner on AMF colonisation of tomato are of great interest for crop plant communities and for the influences on each other. The outcome of the bioprotective effects of AMF resulting in the decrease on F. oxysporum f. sp. lycopersici disease severity and/or compensation of plant biomass does not depend on the degree of AM colonisation but more on the intercropping partner.
PMCID: PMC3778835  PMID: 23549903
AM fungi; Fusarium oxysporum f. sp. lycopersici; Intercropping; Solanum lycopersicum; Biological control
15.  A Common Garden Test of Host-Symbiont Specificity Supports a Dominant Role for Soil Type in Determining AMF Assemblage Structure in Collinsia sparsiflora 
PLoS ONE  2013;8(2):e55507.
Specialization in plant host-symbiont-soil interactions may help mediate plant adaptation to edaphic stress. Our previous field study showed ecological evidence for host-symbiont specificity between serpentine and non-serpentine adapted ecotypes of Collinsia sparsiflora and arbuscular mycorrrhizal fungi (AMF). To test for adapted plant ecotype-AMF specificity between C. sparsiflora ecotypes and field AMF taxa, we conducted an AMF common garden greenhouse experiment. We grew C. sparsiflora ecotypes individually in a common pool of serpentine and non-serpentine AMF then identified the root AMF by amplifying rDNA, cloning, and sequencing and compared common garden AMF associates to serpentine and non-serpentine AMF controls. Mixing of serpentine and non-serpentine AMF soil inoculum resulted in an intermediate soil classified as non-serpentine soil type. Within this common garden both host ecotypes associated with AMF assemblages that resembled those seen in a non-serpentine soil. ANOSIM analysis and MDS ordination showed that common garden AMF assemblages differed significantly from those in the serpentine-only controls (R = 0.643, P<0.001), but were similar the non-serpentine-only control AMF assemblages (R = 0.081, P<0.31). There was no evidence of adapted host ecotype-AMF specificity. Instead soil type accounted for most of the variation AM fungi association patterns, and some differences between field and greenhouse behavior of individual AM fungi were found.
PMCID: PMC3564749  PMID: 23393588
16.  Contrasting the Community Structure of Arbuscular Mycorrhizal Fungi from Hydrocarbon-Contaminated and Uncontaminated Soils following Willow (Salix spp. L.) Planting 
PLoS ONE  2014;9(7):e102838.
Phytoremediation is a potentially inexpensive alternative to chemical treatment of hydrocarbon-contaminated soils, but its success depends heavily on identifying factors that govern the success of root-associated microorganisms involved in hydrocarbon degradation and plant growth stimulation. Arbuscular mycorrhizal fungi (AMF) form symbioses with many terrestrial plants, and are known to stimulate plant growth, although both species identity and the environment influence this relationship. Although AMF are suspected to play a role in plant adaptation to hydrocarbon contamination, their distribution in hydrocarbon-contaminated soils is not well known. In this study, we examined how AMF communities were structured within the rhizosphere of 11 introduced willow cultivars as well as unplanted controls across uncontaminated and hydrocarbon-contaminated soils at the site of a former petrochemical plant. We obtained 69 282 AMF-specific 18S rDNA sequences using 454-pyrosequencing, representing 27 OTUs. Contaminant concentration was the major influence on AMF community structure, with different AMF families dominating at each contaminant level. The most abundant operational taxonomic unit in each sample represented a large proportion of the total community, and this proportion was positively associated with increasing contamination, and seemingly, by planting as well. The most contaminated soils were dominated by three phylotypes closely related to Rhizophagus irregularis, while these OTUs represented only a small proportion of sequences in uncontaminated and moderately contaminated soils. These results suggest that in situ inoculation of AMF strains could be an important component of phytoremediation treatments, but that strains should be selected from the narrow group that is both adapted to contaminant toxicity and able to compete with indigenous AMF species.
PMCID: PMC4102571  PMID: 25032685
17.  Can Arbuscular Mycorrhizal Fungi Reduce the Growth of Agricultural Weeds? 
PLoS ONE  2011;6(12):e27825.
Arbuscular mycorrhizal fungi (AMF) are known for their beneficial effects on plants. However, there is increasing evidence that some ruderal plants, including several agricultural weeds, respond negatively to AMF colonization. Here, we investigated the effect of AMF on the growth of individual weed species and on weed-crop interactions.
Methodology/Principal Findings
First, under controlled glasshouse conditions, we screened growth responses of nine weed species and three crops to a widespread AMF, Glomus intraradices. None of the weeds screened showed a significant positive mycorrhizal growth response and four weed species were significantly reduced by the AMF (growth responses between −22 and −35%). In a subsequent experiment, we selected three of the negatively responding weed species – Echinochloa crus-galli, Setaria viridis and Solanum nigrum – and analyzed their responses to a combination of three AMF (Glomus intraradices, Glomus mosseae and Glomus claroideum). Finally, we tested whether the presence of a crop (maize) enhanced the suppressive effect of AMF on weeds. We found that the growth of the three selected weed species was also reduced by a combination of AMF and that the presence of maize amplified the negative effect of AMF on the growth of E. crus-galli.
Our results show that AMF can negatively influence the growth of some weed species indicating that AMF have the potential to act as determinants of weed community structure. Furthermore, mycorrhizal weed growth reductions can be amplified in the presence of a crop. Previous studies have shown that AMF provide a number of beneficial ecosystem services. Taken together with our current results, the maintenance and promotion of AMF activity may thereby contribute to sustainable management of agroecosystems. However, in order to further the practical and ecological relevance of our findings, additional experiments should be performed under field conditions.
PMCID: PMC3229497  PMID: 22164216
18.  Inoculation of tomato seedlings with Trichoderma Harzianum and Arbuscular Mycorrhizal Fungi and their effect on growth and control of wilt in tomato seedlings 
Brazilian Journal of Microbiology  2011;42(2):508-513.
A green house study was conducted to investigate the ability of an isolate of Trichoderma harzianum (P52) and arbuscular mycorrhizal fungi (AMF) in enhancing growth and control of a wilt pathogen caused by Fusarium oxysporum f. sp. lycopersici in tomato seedlings. The plants were grown in plastic pots filled with sterilized soils. There were four treatments applied as follows; P52, AMF, AMF + P52 and a control. A completely randomized design was used and growth measurements and disease assessment taken after 3, 6 and 9 weeks. Treatments that significantly (P < 0.05) enhanced heights and root dry weights were P52, AMF and a treatment with a combination of both P52 and AMF when compared the control. The treatment with both P52 and AMF significantly (P < 0.05) enhanced all growth parameters (heights; shoot and root dry weight) investigated compared to the control. Disease severity was generally lower in tomato plants grown with isolate P52 and AMF fungi either individually or when combined together, though the effect was not statistically significant (P≥ 0.05). A treatment combination of P52 + AMF had less trend of severity as compared to each individual fungus. T. harzianum and AMF can be used to enhance growth in tomato seedlings.
PMCID: PMC3769820  PMID: 24031662
Arbuscular mycorrhizal Fungi (AMF); Trichoderma harzianum (P52); Disease severity
19.  Enhancement of the efficacy of a carbamate nematicide against the potato cyst nematode, Globodera pallida, through mycorrhization in commercial potato fields 
Journal of Nematology  2010;42(1):22-32.
Two experiments were conducted over 2 years in commercial potato fields in Shropshire, UK, to evaluate the compatibility of the nematicide aldicarb with commercial inocula of arbuscular mycorrhizal fungi (AMF) in the control of the potato cyst nematode Globodera pallida. The AMF used were Vaminoc (mixed-AMF inoculum), Glomus intraradices (BioRize BB-E) and G. mosseae (isolate BEG 12). In the absence of AMF, the in-soil hatch of G. pallida increased 30% (P < 0.01) from wk-2 to wk-4 after planting. Inoculation of physiologically-aged potato (cv. Golden Wonder) tubers with AMF eliminated this delay in G. pallida hatch by stimulating a mean increase of 32% (P < 0.01) in hatch within 2 wk after planting. In the aldicarb-treated plots in Experiment 1, G. pallida multiplication rate was 38% lower (P < 0.05) in roots of AMF-inoculated than noninoculated plants, but in Experiment 2, this effect was slightly lower (P = 0.07). In these plots, the single AMF inocula showed also a weak trend (P = 0.10) towards greater tuber yields relative to their noninoculated counterparts. Mycorrhization therefore appears to enhance the efficacy of carbamate nematicides against G. pallida and consequently more research is proposed to validate these findings and fully explore the potential of this model.
PMCID: PMC3380507  PMID: 22736833
integrated pest management; potato cyst nematode; Globodera pallida; arbuscular mycorrhizal fungi; Glomus spp.; interaction; aldicarb; hatch; multiplication; Solanum tuberosum
20.  Influence of the Size of Indigenous Rhizobial Populations on Establishment and Symbiotic Performance of Introduced Rhizobia on Field-Grown Legumes † 
Indigenous rhizobia in soil present a competition barrier to the establishment of inoculant strains, possibly leading to inoculation failure. In this study, we used the natural diversity of rhizobial species and numbers in our fields to define, in quantitative terms, the relationship between indigenous rhizobial populations and inoculation response. Eight standardized inoculation trials were conducted at five well-characterized field sites on the island of Maui, Hawaii. Soil rhizobial populations ranged from 0 to over 3.5 × 104 g of soil-1 for the different legumes used. At each site, no less than four but as many as seven legume species were planted from among the following: soybean (Glycine max), lima bean (Phaseolus lunatus), cowpea (Vigna unguiculata), bush bean (Phaseolus vulgaris), peanut (Arachis hypogaea), Leucaena leucocephala, tinga pea (Lathyrus tingeatus), alfalfa (Medicago sativa), and clover (Trifolium repens). Each legume was (i) inoculated with an equal mixture of three effective strains of homologous rhizobia, (ii) fertilized at high rates with urea, or (iii) left uninoculated. For soybeans, a nonnodulating isoline was used in all trials as the rhizobia-negative control. Inoculation increased economic yield for 22 of the 29 (76%) legume species-site combinations. While the yield increase was greater than 100 kg ha-1 in all cases, in only 11 (38%) of the species-site combinations was the increase statistically significant (P ≤ 0.05). On average, inoculation increased yield by 62%. Soybean (G. max) responded to inoculation most frequently, while cowpea (V. unguiculata) failed to respond in all trials. Inoculation responses in the other legumes were site dependent. The response to inoculation and the competitive success of inoculant rhizobia were inversely related to numbers of indigenous rhizobia. As few as 50 rhizobia g of soil-1 eliminated inoculation response. When fewer than 10 indigenous rhizobia g of soil-1 were present, economic yield was significantly increased 85% of the time. Yield was significantly increased in only 6% of the observations when numbers of indigenous rhizobia were greater than 10 cells g of soil-1. A significant response to N application, significant increases in nodule parameters, and greater than 50% nodule occupancy by inoculant rhizobia did not necessarily coincide with significant inoculation responses. No less than a doubling of nodule mass and 66% nodule occupancy by inoculant rhizobia were required to significantly increase the yield of inoculated crops over that of uninoculated crops. However, lack of an inoculation response was common even when inoculum strains occupied the majority of nodules. In these trials, the symbiotic yield of crops was, on average, only 88% of the maximum yield potential, as defined by the fertilizer N treatment. The difference between the yield of N-fertilized crops and that of N2-fixing crops indicates a potential for improving inoculation technology, the N2 fixation capacity of rhizobial strains, and the efficiency of symbiosis. In this study, we show that the probability of enhancing yield with existing inoculation technology decreases dramatically with increasing numbers of indigenous rhizobia.
PMCID: PMC182659  PMID: 16348393
21.  Root Interactions in a Maize/Soybean Intercropping System Control Soybean Soil-Borne Disease, Red Crown Rot 
PLoS ONE  2014;9(5):e95031.
Within-field multiple crop species intercropping is well documented and used for disease control, but the underlying mechanisms are still unclear. As roots are the primary organ for perceiving signals in the soil from neighboring plants, root behavior may play an important role in soil-borne disease control.
Principal Findings
In two years of field experiments, maize/soybean intercropping suppressed the occurrence of soybean red crown rot, a severe soil-borne disease caused by Cylindrocladium parasiticum (C. parasiticum). The suppressive effects decreased with increasing distance between intercropped plants under both low P and high P supply, suggesting that root interactions play a significant role independent of nutrient status. Further detailed quantitative studies revealed that the diversity and intensity of root interactions altered the expression of important soybean PR genes, as well as, the activity of corresponding enzymes in both P treatments. Furthermore, 5 phenolic acids were detected in root exudates of maize/soybean intercropped plants. Among these phenolic acids, cinnamic acid was released in significantly greater concentrations when intercropped maize with soybean compared to either crop grown in monoculture, and this spike in cinnamic acid was found dramatically constrain C. parasiticum growth in vitro.
To the best of our knowledge, this study is the first report to demonstrate that intercropping with maize can promote resistance in soybean to red crown rot in a root-dependent manner. This supports the point that intercropping may be an efficient ecological strategy to control soil-borne plant disease and should be incorporated in sustainable agricultural management practices.
PMCID: PMC4014482  PMID: 24810161
22.  Arbuscular mycorrhizal fungi alter above- and below-ground chemical defense expression differentially among Asclepias species 
Below-ground (BG) symbionts of plants can have substantial influence on plant growth and nutrition. Recent work demonstrates that mycorrhizal fungi can affect plant resistance to herbivory and the performance of above- (AG) and BG herbivores. Although these examples emerge from diverse systems, it is unclear if plant species that express similar defensive traits respond similarly to fungal colonization, but comparative work may inform this question. To examine the effects of arbuscular mycorrhizal fungi (AMF) on the expression of chemical resistance, we inoculated 8 species of Asclepias (milkweed)—which all produce toxic cardenolides—with a community of AMF. We quantified plant biomass, foliar and root cardenolide concentration and composition, and assessed evidence for a growth-defense tradeoff in the presence and absence of AMF. As expected, total foliar and root cardenolide concentration varied among milkweed species. Importantly, the effect of mycorrhizal fungi on total foliar cardenolide concentration also varied among milkweed species, with foliar cardenolides increasing or decreasing, depending on the plant species. We detected a phylogenetic signal to this variation; AMF fungi reduced foliar cardenolide concentrations to a greater extent in the clade including A. curassavica than in the clade including A. syriaca. Moreover, AMF inoculation shifted the composition of cardenolides in AG and BG plant tissues in a species-specific fashion. Mycorrhizal inoculation changed the relative distribution of cardenolides between root and shoot tissue in a species-specific fashion, but did not affect cardenolide diversity or polarity. Finally, a tradeoff between plant growth and defense in non-mycorrhizal plants was mitigated completely by AMF inoculation. Overall, we conclude that the effects of AMF inoculation on the expression of chemical resistance can vary among congeneric plant species, and ameliorate tradeoffs between growth and defense.
PMCID: PMC3776932  PMID: 24065971
plant–herbivore interactions; mycorrhizal fungi; plant defense; above-below-ground interactions; growth-defense tradeoff; root defense; phylogenetic signal
23.  Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression 
Annals of Botany  2010;106(5):791-802.
Background and Aims
It is increasingly evident that plant tolerance to stress is improved by mycorrhiza. Thus, suitable plant–fungus combinations may also contribute to the success of phytoremediation of heavy metal (HM)-polluted soil. Metallothioneins (MTs) and polyamines (PAs) are implicated in the response to HM stress in several plant species, but whether the response is modulated by arbuscular mycorrhizal fungi (AMF) remains to be clarified. The aim of the present study was to check whether colonization by AMF could modify growth, metal uptake/translocation, and MT and PA gene expression levels in white poplar cuttings grown on HM-contaminated soil, and to compare this with plants grown on non-contaminated soil.
In this greenhouse study, plants of a Populus alba clone were pre-inoculated, or not, with either Glomus mosseae or G. intraradices and then grown in pots containing either soil collected from a multimetal- (Cu and Zn) polluted site or non-polluted soil. The expression of MT and PA biosynthetic genes was analysed in leaves using quantitative reverse transcription–PCR. Free and conjugated foliar PA concentrations were determined in parallel.
On polluted soil, AMF restored plant biomass despite higher Cu and Zn accumulation in plant organs, especially roots. Inoculation with the AMF caused an overall induction of PaMT1, PaMT2, PaMT3, PaSPDS1, PaSPDS2 and PaADC gene expression, together with increased free and conjugated PA levels, in plants grown on polluted soil, but not in those grown on non-polluted soil.
Mycorrhizal plants of P. alba clone AL35 exhibit increased capacity for stabilization of soil HMs, together with improved growth. Their enhanced stress tolerance may derive from the transcriptional upregulation of several stress-related genes, and the protective role of PAs.
PMCID: PMC2958786  PMID: 20810743
Arbuscular mycorrhizal fungi; contaminated soil; heavy metals; metallothioneins; polyamines; Populus alba; white poplar
24.  Assessment of arbuscular mycorrhizal fungi on the phytoremediation potential of Ipomoea aquatica on cadmium uptake 
3 Biotech  2012;2(3):193-198.
The phytoremedial potential of Ipomoea aquatica and role of arbuscular mycorrhizal fungi (AMF) during Cadmium uptake was studied under two different soils i.e., soil inoculated with and without AMF. The plants were treated with different concentrations of Cd(NO)3 starting from 0, 5, 10, 25, 50, and 100 ppm in three replicate design in soil with and without AMF inoculation. Results showed that AMF enhanced accumulation of cadmium in plant tissues at all concentrations. Plants in AMF exhibited tolerance for Cd up to 100 mg/l and accumulated 88.07% in its tissues with no visual symptoms of toxicity, whereas those in non-AMF showed marked growth reduction at the same concentration with a metal accumulation of 73.2%. A significant variation of antioxidant enzymes under different environments evaluated the defense pathways of plants during uptake of Cd. Physiological changes and nutrient uptake showed that plants inoculated in AMF were more unwavering during stress conditions. The study established that phytoremedial potential of I. aquatica depends on rhizospheric conditions which enhanced Cd uptake. Finally, it was established that AMF was able to maintain an efficient symbiosis with I. aquatica in soil moderately contaminated by Cd, viable due to relation between fungus and plant.
PMCID: PMC3433885
Phytoremediation; Cadmium; AMF; Ipomoea aquatica; Antioxidant enzymes
25.  Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence 
The ISME Journal  2013;7(11):2137-2146.
Arbuscular mycorrhizal fungi (AMF) form symbioses with most plant species. They are ecologically important determinants of plant growth and diversity. Considerable genetic variation occurs in AMF populations. Thus, plants are exposed to AMF of varying relatedness to each other. Very little is known about either the effects of coexisting AMF on plant growth or which factors influence intraspecific AMF coexistence within roots. No studies have addressed whether the genetics of coexisting AMF, and more specifically their relatedness, influences plant growth and AMF coexistence. Relatedness is expected to influence coexistence between individuals, and it has been suggested that decreasing ability of symbionts to coexist can have negative effects on the growth of the host. We tested the effect of a gradient of AMF genetic relatedness on the growth of two plant species. Increasing relatedness between AMFs lead to markedly greater plant growth (27% biomass increase with closely related compared to distantly related AMF). In one plant species, closely related AMF coexisted in fairly equal proportions but decreasing relatedness lead to a very strong disequilibrium between AMF in roots, indicating much stronger competition. Given the strength of the effects with such a shallow relatedness gradient and the fact that in the field plants are exposed to a steeper gradient, we consider that AMF relatedness can have a strong role in plant growth and the ability of AMF to coexist. We conclude that AMF relatedness is a driver of plant growth and that relatedness is also a strong driver of intraspecific coexistence of these ecologically important symbionts.
PMCID: PMC3806264  PMID: 23823490
Rhizophagus irregularis; intraspecific competition; coexistence; symbiosis; mycorrhiza

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