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1.  Soil sand content can alter effects of different taxa of mycorrhizal fungi on plant biomass production of grassland species 
European Journal of Soil Biology  2011;47(3):175-181.
In this greenhouse experiment we tested whether (i) ubiquitous arbuscular mycorrhizal fungi (AMF) taxa (Glomus claroideum, Glomus geosporum, Glomus intraradices, Glomus mosseae) singly and in a mixture differently affect growth and biomass production of four co-occurring grassland species (grass: Arrhenatherum elatius, non-leguminous forbs: Plantago lanceolata, Salvia pratensis and leguminous forb Trifolium pratense), and (ii) different soil sand contents alter AMF influence. We hypothesized that AMF effects on plants will increase with an increased AMF diversity and with increasing sand content. Percent AMF colonization of roots differed between plant species and AMF taxa and was higher with higher sand content. Plant growth responses to AMF were species-specific both regarding plants and AMF. Generally, biomass production of the non-leguminous forbs was the most responsive, the grass species the least and the legume intermediate both for AMF treatments and sand content. Across species, AMF influence on plant biomass increased with increasing soil sand content. Plant species growing in soil containing a mix of four AMF taxa showed similar growth responses than species in soil containing only one AMF taxon. These results suggest that both interference among AMF taxa and soil sand content can trigger the influence of AMF on plant production in grassland species.
Highlights
► Ubiquitous AMF taxa of the Glomus group differently affected plant growth.► Plant growth responses were not affected by the diversity of the AMF taxa in the inoculum. ► Shoot and root growth was differently affected by different AMF taxa. ► Relative contribution of grass, forb and legume species was affected by AMF taxa. ► AMF influence on plant growth increased with increasing soil sand content.
doi:10.1016/j.ejsobi.2011.03.001
PMCID: PMC4461177  PMID: 26109837
AMF inoculation; AMF taxa; Biomass allocation; Plant biomass production; Grassland; Soil texture; Plant growth responses; Root growth; Shoot growth
2.  Earthworm-Mycorrhiza Interactions Can Affect the Diversity, Structure and Functioning of Establishing Model Grassland Communities 
PLoS ONE  2011;6(12):e29293.
Both earthworms and arbuscular mycorrhizal fungi (AMF) are important ecosystem engineers co-occurring in temperate grasslands. However, their combined impacts during grassland establishment are poorly understood and have never been studied. We used large mesocosms to study the effects of different functional groups of earthworms (i.e., vertically burrowing anecics vs. horizontally burrowing endogeics) and a mix of four AMF taxa on the establishment, diversity and productivity of plant communities after a simulated seed rain of 18 grassland species comprising grasses, non-leguminous forbs and legumes. Moreover, effects of earthworms and/or AMF on water infiltration and leaching of ammonium, nitrate and phosphate were determined after a simulated extreme rainfall event (40 l m−2). AMF colonisation of all three plant functional groups was altered by earthworms. Seedling emergence and diversity was reduced by anecic earthworms, however only when AMF were present. Plant density was decreased in AMF-free mesocosms when both anecic and endogeic earthworms were active; with AMF also anecics reduced plant density. Plant shoot and root biomass was only affected by earthworms in AMF-free mesocosms: shoot biomass increased due to the activity of either anecics or endogeics; root biomass increased only when anecics were active. Water infiltration increased when earthworms were present in the mesocosms but remained unaffected by AMF. Ammonium leaching was increased only when anecics or a mixed earthworm community was active but was unaffected by AMF; nitrate and phosphate leaching was neither affected by earthworms nor AMF. Ammonium leaching decreased with increasing plant density, nitrate leaching decreased with increasing plant diversity and density. In order to understand the underlying processes of these interactions further investigations possibly under field conditions using more diverse belowground communities are required. Nevertheless, this study demonstrates that belowground-aboveground linkages involving earthworms and AMF are important mediators of the diversity, structure and functioning of plant communities.
doi:10.1371/journal.pone.0029293
PMCID: PMC3247237  PMID: 22216236
3.  Interrelated effects of mycorrhiza and free-living nitrogen fixers cascade up to aboveground herbivores 
Ecology and Evolution  2015;5(17):3756-3768.
Aboveground plant performance is strongly influenced by belowground microorganisms, some of which are pathogenic and have negative effects, while others, such as nitrogen-fixing bacteria and arbuscular mycorrhizal fungi, usually have positive effects. Recent research revealed that belowground interactions between plants and functionally distinct groups of microorganisms cascade up to aboveground plant associates such as herbivores and their natural enemies. However, while functionally distinct belowground microorganisms commonly co-occur in the rhizosphere, their combined effects, and relative contributions, respectively, on performance of aboveground plant-associated organisms are virtually unexplored. Here, we scrutinized and disentangled the effects of free-living nitrogen-fixing (diazotrophic) bacteria Azotobacter chroococcum (DB) and arbuscular mycorrhizal fungi Glomus mosseae (AMF) on host plant choice and reproduction of the herbivorous two-spotted spider mite Tetranychus urticae on common bean plants Phaseolus vulgaris. Additionally, we assessed plant growth, and AMF and DB occurrence and density as affected by each other. Both AMF alone and DB alone increased spider mite reproduction to similar levels, as compared to the control, and exerted additive effects under co-occurrence. These effects were similarly apparent in host plant choice, that is, the mites preferred leaves from plants with both AMF and DB to plants with AMF or DB to plants grown without AMF and DB. DB, which also act as AMF helper bacteria, enhanced root colonization by AMF, whereas AMF did not affect DB abundance. AMF but not DB increased growth of reproductive plant tissue and seed production, respectively. Both AMF and DB increased the biomass of vegetative aboveground plant tissue. Our study breaks new ground in multitrophic belowground–aboveground research by providing first insights into the fitness implications of plant-mediated interactions between interrelated belowground fungi–bacteria and aboveground herbivores.
doi:10.1002/ece3.1654
PMCID: PMC4567878  PMID: 26380703
Aboveground–belowground interactions; arbuscular mycorrhiza; fitness; multitrophic interactions; nitrogen fixation; spider mites
4.  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.
doi:10.1371/journal.pone.0061329
PMCID: PMC3631226  PMID: 23620744
5.  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.
doi:10.1007/s00572-013-0495-x
PMCID: PMC3778835  PMID: 23549903
AM fungi; Fusarium oxysporum f. sp. lycopersici; Intercropping; Solanum lycopersicum; Biological control
6.  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.
doi:10.1007/s00572-011-0391-1
PMCID: PMC3261393  PMID: 21626142
AMF species specificity; Anthraquinone derivatives; Arbuscular mycorrhiza; Hyperforin; Photosynthetic performance index; St. John’s-wort
7.  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.
doi:10.1016/j.scitotenv.2010.11.020
PMCID: PMC3030643  PMID: 21211826
Prosopis juliflora; phytostabilization; DGGE; mycorrhizal fungi; mine tailing
8.  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.
doi:10.3389/fpls.2013.00361
PMCID: PMC3776932  PMID: 24065971
plant–herbivore interactions; mycorrhizal fungi; plant defense; above-below-ground interactions; growth-defense tradeoff; root defense; phylogenetic signal
9.  Metabolomics Suggests That Soil Inoculation with Arbuscular Mycorrhizal Fungi Decreased Free Amino Acid Content in Roots of Durum Wheat Grown under N-Limited, P-Rich Field Conditions 
PLoS ONE  2015;10(6):e0129591.
Arbuscular mycorrhizal fungi (AMF) have a major impact on plant nutrition, defence against pathogens, a plant’s reaction to stressful environments, soil fertility, and a plant’s relationship with other microorganisms. Such effects imply a broad reprogramming of the plant’s metabolic activity. However, little information is available regarding the role of AMF and their relation to other soil plant growth—promoting microorganisms in the plant metabolome, especially under realistic field conditions. In the present experiment, we evaluated the effects of inoculation with AMF, either alone or in combination with plant growth–promoting rhizobacteria (PGPR), on the metabolome and changes in metabolic pathways in the roots of durum wheat (Triticum durum Desf.) grown under N-limited agronomic conditions in a P-rich environment. These two treatments were compared to infection by the natural AMF population (NAT). Soil inoculation with AMF almost doubled wheat root colonization by AMF and decreased the root concentrations of most compounds in all metabolic pathways, especially amino acids (AA) and saturated fatty acids, whereas inoculation with AMF+PGPR increased the concentrations of such compounds compared to inoculation with AMF alone. Enrichment metabolomics analyses showed that AA metabolic pathways were mostly changed by the treatments, with reduced amination activity in roots most likely due to a shift from the biosynthesis of common AA to γ-amino butyric acid. The root metabolome differed between AMF and NAT but not AMF+PGPR and AMF or NAT. Because the PGPR used were potent mineralisers, and AMF can retain most nitrogen (N) taken as organic compounds for their own growth, it is likely that this result was due to an increased concentration of mineral N in soil inoculated with AMF+PGPR compared to AMF alone.
doi:10.1371/journal.pone.0129591
PMCID: PMC4466249  PMID: 26067663
10.  Subsurface earthworm casts can be important soil microsites specifically influencing the growth of grassland plants 
Biology and Fertility of Soils  2013;49(8):1097-1107.
Earthworms (Annelida: Oligochaeta) deposit several tons per hectare of casts enriched in nutrients and/or arbuscular mycorrhizal fungi (AMF) and create a spatial and temporal soil heterogeneity that can play a role in structuring plant communities. However, while we begin to understand the role of surface casts, it is still unclear to what extent plants utilize subsurface casts. We conducted a greenhouse experiment using large mesocosms (volume 45 l) to test whether (1) soil microsites consisting of earthworm casts with or without AMF (four Glomus taxa) affect the biomass production of 11 grassland plant species comprising the three functional groups grasses, forbs, and legumes, (2) different ecological groups of earthworms (soil dwellers—Aporrectodea caliginosa vs. vertical burrowers—Lumbricus terrestris) alter potential influences of soil microsites (i.e., four earthworms × two subsurface microsites × two AMF treatments). Soil microsites were artificially inserted in a 25-cm depth, and afterwards, plant species were sown in a regular pattern; the experiment ran for 6 months. Our results show that minute amounts of subsurface casts (0.89 g kg−1 soil) decreased the shoot and root production of forbs and legumes, but not that of grasses. The presence of earthworms reduced root biomass of grasses only. Our data also suggest that subsurface casts provide microsites from which root AMF colonization can start. Ecological groups of earthworms did not differ in their effects on plant production or AMF distribution. Taken together, these findings suggest that subsurface earthworm casts might play a role in structuring plant communities by specifically affecting the growth of certain functional groups of plants.
doi:10.1007/s00374-013-0808-4
PMCID: PMC4459550  PMID: 26069355
Aboveground–belowground interactions; Grassland ecology; Mesocosm experiment; Plant–animal–fungi interaction; Polymerase chain reaction (PCR); Vesicular-arbuscular mycorrhizal fungi (AMF)
11.  Grassland invaders and their mycorrhizal symbionts: a study across climate and invasion gradients 
Ecology and Evolution  2014;4(6):794-805.
Controlled experiments show that arbuscular mycorrhizal fungi (AMF) can increase competitiveness of exotic plants, potentially increasing invasion success. We surveyed AMF abundance and community composition in Centaurea stoebe and Potentilla recta invasions in the western USA to assess whether patterns were consistent with mycorrhizal-mediated invasions. We asked whether (1) AMF abundance and community composition differ between native and exotic forbs, (2) associations between native plants and AMF shift with invading exotic plants, and (3) AMF abundance and/or community composition differ in areas where exotic plants are highly invasive and in areas where they are not. We collected soil and roots from invaded and native forb communities along invasion gradients and in regions with different invasion densities. We used AMF root colonization as a measure of AMF abundance and characterized AMF communities in roots using 454-sequencing of the LSU-rDNA region. All plants were highly colonized (>60%), but exotic forbs tended to be more colonized than natives (P < 0.001). We identified 30 AMF operational taxonomic units (OTUs) across sites, and community composition was best predicted by abiotic factors (soil texture, pH). Two OTUs in the genera Glomus and Rhizophagus dominated in most communities, and their dominance increased with invasion density (r = 0.57, P = 0.010), while overall OTU richness decreased with invasion density (r = −0.61, P = 0.006). Samples along P. recta invasion gradients revealed small and reciprocal shifts in AMF communities with >45% fungal OTUs shared between neighboring native and P. recta plants. Overall, we observed significant, but modest, differences in AMF colonization and communities between co-occurring exotic and native forbs and among exotic forbs across regions that differ in invasion pressure. While experimental manipulations are required to assess functional consequences, the observed patterns are not consistent with those expected from strong mycorrhizal-mediated invasions.
doi:10.1002/ece3.917
PMCID: PMC3967904  PMID: 24683461
454-sequencing; arbuscular mycorrhizal fungi; Centaurea stoebe; community structure; plant invasion; plant–soil interactions; Potentilla recta
12.  Co-Inoculation with Rhizobia and AMF Inhibited Soybean Red Crown Rot: From Field Study to Plant Defense-Related Gene Expression Analysis 
PLoS ONE  2012;7(3):e33977.
Background
Soybean red crown rot is a major soil-borne disease all over the world, which severely affects soybean production. Efficient and sustainable methods are strongly desired to control the soil-borne diseases.
Principal Findings
We firstly investigated the disease incidence and index of soybean red crown rot under different phosphorus (P) additions in field and found that the natural inoculation of rhizobia and arbuscular mycorrhizal fungi (AMF) could affect soybean red crown rot, particularly without P addition. Further studies in sand culture experiments showed that inoculation with rhizobia or AMF significantly decreased severity and incidence of soybean red crown rot, especially for co-inoculation with rhizobia and AMF at low P. The root colony forming unit (CFU) decreased over 50% when inoculated by rhizobia and/or AMF at low P. However, P addition only enhanced CFU when inoculated with AMF. Furthermore, root exudates of soybean inoculated with rhizobia and/or AMF significantly inhibited pathogen growth and reproduction. Quantitative RT-PCR results indicated that the transcripts of the most tested pathogen defense-related (PR) genes in roots were significantly increased by rhizobium and/or AMF inoculation. Among them, PR2, PR3, PR4 and PR10 reached the highest level with co-inoculation of rhizobium and AMF.
Conclusions
Our results indicated that inoculation with rhizobia and AMF could directly inhibit pathogen growth and reproduction, and activate the plant overall defense system through increasing PR gene expressions. Combined with optimal P fertilization, inoculation with rhizobia and AMF could be considered as an efficient method to control soybean red crown rot in acid soils.
doi:10.1371/journal.pone.0033977
PMCID: PMC3307780  PMID: 22442737
13.  The Influence of Rhizobium and Arbuscular Mycorrhizal Fungi on Nitrogen and Phosphorus Accumulation by Vicia faba 
Annals of Botany  2004;94(2):251-258.
• Background and Aims The aim of this study was to investigate the effects of the interactions between the microbial symbionts, Rhizobium and arbuscular mycorrhizal fungi (AMF) on N and P accumulation by broad bean (Vicia faba) and how increased N and P content influence biomass production, leaf area and net photosynthetic rate.
• Methods A multi-factorial experiment consisting of four different legume–microbial symbiotic associations and two nitrogen treatments was used to investigate the influence of the different microbial symbiotic associations on P accumulation, total N accumulation, biomass, leaf area and net photosynthesis in broad bean grown under low P conditions.
• Key Results AMF promoted biomass production and photosynthetic rates by increasing the ratio of P to N accumulation. An increase in P was consistently associated with an increase in N accumulation and N productivity, expressed in terms of biomass and leaf area. Photosynthetic N use efficiency, irrespective of the inorganic source of N (e.g. NO3− or N2), was enhanced by increased P supply due to AMF. The presence of Rhizobium resulted in a significant decline in AMF colonization levels irrespective of N supply. Without Rhizobium, AMF colonization levels were higher in low N treatments. Presence or absence of AMF did not have a significant effect on nodule mass but high N with or without AMF led to a significant decline in nodule biomass. Plants with the Rhizobium and AMF symbiotic associations had higher photosynthetic rates per unit leaf area.
• Conclusions The results indicated that the synergistic or additive interactions among the components of the tripartite symbiotic association (Rhizobium–AMF–broad bean) increased plant productivity.
doi:10.1093/aob/mch135
PMCID: PMC4242160  PMID: 15205177
Arbuscular mycorrhizal fungi (AMF); nitrogen; phosphorus; Rhizobium; Vicia faba
14.  Herbivory of an invasive slug in a model grassland community can be affected by earthworms and mycorrhizal fungi 
Biology and Fertility of Soils  2013;50(1):13-23.
Invasion of non-native species is among the top threats for the biodiversity and functioning of native and agricultural ecosystems worldwide. We investigated whether the herbivory of the slug Arion vulgaris (formerly Arion lusitanicus; Gastropoda), that is listed among the 100 worst alien species in Europe, is affected by soil organisms commonly present in terrestrial ecosystems (i.e. earthworms—Annelida: Lumbricidae and arbuscular mycorrhizal fungi—AMF, Glomerales). We hypothesized that slug herbivory would be affected by soil organisms via altered plant nutrient availability and plant quality. In a greenhouse experiment, we created a simple plant community consisting of a grass, a forb, and a legume species and inoculated these systems with either two earthworm species and/or four AMF taxa. Slugs were introduced after plants were established. Earthworms significantly reduced total slug herbivory in AMF-inoculated plant communities (P = 0.013). Across plant species, earthworms increased leaf total N and secondary metabolites, AMF decreased leaf thickness. Mycorrhizae induced a shift in slug feeding preference from non-legumes to legumes; the grass was generally avoided by slugs. AMF effects on legume herbivory can partly be explained by the AMF-induced increase in total N and decrease in C/N ratio; earthworm effects are less clear as no worm-induced alterations of legume plant chemistry were observed. The presence of earthworms increased average AMF colonization of plant roots by 140 % (P < 0.001). Total shoot mass was significantly increased by AMF (P < 0.001). These data suggest that the feeding behavior of this invasive slug is altered by a belowground control of plant chemical quality and community structure.
doi:10.1007/s00374-013-0827-1
PMCID: PMC4459544  PMID: 26069356
Aboveground–belowground interactions; Gastropods; Invasive species; Lumbricidae; Neobiota; Plant–soil interactions; Soil ecology; Symbiotic fungi
15.  Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat 
In a field experiment conducted in a Mediterranean area of inner Sicily, durum wheat was inoculated with plant growth-promoting rhizobacteria (PGPR), with arbuscular mycorrhizal fungi (AMF), or with both to evaluate their effects on nutrient uptake, plant growth, and the expression of key transporter genes involved in nitrogen (N) and phosphorus (P) uptake. These biotic associations were studied under either low N availability (unfertilized plots) and supplying the soil with an easily mineralizable organic fertilizer. Regardless of N fertilization, at the tillering stage, inoculation with AMF alone or in combination with PGPR increased the aboveground biomass yield compared to the uninoculated control. Inoculation with PGPR enhanced the aboveground biomass yield compared to the control, but only when N fertilizer was added. At the heading stage, inoculation with all microorganisms increased the aboveground biomass and N. Inoculation with PGPR and AMF+PGPR resulted in significantly higher aboveground P compared to the control and inoculation with AMF only when organic N was applied. The role of microbe inoculation in N uptake was elucidated by the expression of nitrate transporter genes. NRT1.1, NRT2, and NAR2.2 were significantly upregulated by inoculation with AMF and AMF+PGPR in the absence of organic N. A significant down-regulation of the same genes was observed when organic N was added. The ammonium (NH4+) transporter genes AMT1.2 showed an expression pattern similar to that of the NO3- transporters. Finally, in the absence of organic N, the transcript abundance of P transporters Pht1 and PT2-1 was increased by inoculation with AMF+PGPR, and inoculation with AMF upregulated Pht2 compared to the uninoculated control. These results indicate the soil inoculation with AMF and PGPR (alone or in combination) as a valuable option for farmers to improve yield, nutrient uptake, and the sustainability of the agro-ecosystem.
doi:10.3389/fpls.2015.00815
PMCID: PMC4591488  PMID: 26483827
mediterranean; organic N uptake; plant growth promotion; Gene Expression Regulation; field experiments; arbuscular mycorrhizal fungi (AMF); plant growth-promoting rhizobacteria
16.  Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil 
The ISME Journal  2013;8(6):1336-1345.
N2O is a potent greenhouse gas involved in the destruction of the protective ozone layer in the stratosphere and contributing to global warming. The ecological processes regulating its emissions from soil are still poorly understood. Here, we show that the presence of arbuscular mycorrhizal fungi (AMF), a dominant group of soil fungi, which form symbiotic associations with the majority of land plants and which influence a range of important ecosystem functions, can induce a reduction in N2O emissions from soil. To test for a functional relationship between AMF and N2O emissions, we manipulated the abundance of AMF in two independent greenhouse experiments using two different approaches (sterilized and re-inoculated soil and non-mycorrhizal tomato mutants) and two different soils. N2O emissions were increased by 42 and 33% in microcosms with reduced AMF abundance compared to microcosms with a well-established AMF community, suggesting that AMF regulate N2O emissions. This could partly be explained by increased N immobilization into microbial or plant biomass, reduced concentrations of mineral soil N as a substrate for N2O emission and altered water relations. Moreover, the abundance of key genes responsible for N2O production (nirK) was negatively and for N2O consumption (nosZ) positively correlated to AMF abundance, indicating that the regulation of N2O emissions is transmitted by AMF-induced changes in the soil microbial community. Our results suggest that the disruption of the AMF symbiosis through intensification of agricultural practices may further contribute to increased N2O emissions.
doi:10.1038/ismej.2013.224
PMCID: PMC4030222  PMID: 24351937
agriculture; greenhouse gas; arbuscular mycorrhizal fungi; nitrous oxide; symbiosis; tomato mutants
17.  Effect of Rice Cultivation Systems on Indigenous Arbuscular Mycorrhizal Fungal Community Structure 
Microbes and Environments  2013;28(3):316-324.
Arbuscular mycorrhizal fungi (AMF) in an agricultural ecosystem are necessary for proper management of beneficial symbiosis. Here we explored how the patterns of the AMF community in rice roots were affected by rice cultivation systems (the system of rice intensification [SRI] and the conventional rice cultivation system [CS]), and by compost application during growth stages. Rice plants harvested from SRI-managed plots exhibited considerably higher total biomass, root dry weight, and seed fill than those obtained from conventionally managed plots. Our findings revealed that all AMF sequences observed from CS plots belonged (only) to the genus Glomus, colonizing in rice roots grown under this type of cultivation, while rice roots sown in SRI showed sequences belonging to both Glomus and Acaulospora. The AMF community was compared between the different cultivation types (CS and SRI) and compost applications by principle component analysis. In all rice growth stages, AMF assemblages of CS management were not separated from those of SRI management. The distribution of AMF community composition based on T-RFLP data showed that the AMF community structure was different among four cultivation systems, and there was a gradual increase of Shannon-Weaver indices of diversity (H′) of the AMF community under SRI during growth stages. The results of this research indicated that rice grown in SRI-managed plots had more diverse AMF communities than those grown in CS plots.
doi:10.1264/jsme2.ME13011
PMCID: PMC4070969  PMID: 23719585
arbuscular mycorrhizal fungi; compost application; cultivation systems; Oryza sativa; terminal restriction fragment length polymorphism (T-RFLP)
18.  Impact of an invasive nitrogen-fixing tree on arbuscular mycorrhizal fungi and the development of native species 
AoB Plants  2016;8:plw018.
This study contributes to knowledge on the effect of the invasive N2-fixing tree, Acacia dealbata, on soil microbial communities and consequences on plant species that are dependent on symbiotic relationships as in the case of Plantago lanceolata. The main results of this work indicate that Acacia dealbata modifies the structure of arbuscular mycorrhizal fungi in the invaded shrublands and consequently the growth and development of plants that depend on AMF. Plantago lanceolata showed a substantial reduction in growth, biomass, fungal colonization and P content in the absence of native AMF species.
Arbuscular mycorrhizal fungi (AMF) are obligate soil biotrophs that establish intimate relationships with 80 % of terrestrial plant families. Arbuscular mycorrhizal fungi obtain carbon from host plants and contribute to the acquisition of mineral nutrients, mainly phosphorus. The presence of invasive plants has been identified as a soil disturbance factor, often conditioning the structure and function of soil microorganisms. Despite the investigation of many aspects related to the invasion of Acacia dealbata, the effect produced on the structure of AMF communities has never been assessed. We hypothesize that A. dealbata modifies the structure of AMF community, influencing the establishment and growth of plants that are dependent on these mutualisms. To validate our hypothesis, we carried out denaturing gradient gel electrophoresis (DGGE) analysis and also grew plants of Plantago lanceolata in pots using roots of native shrublands or from A. dealbata, as inoculum of AMF. Cluster analyses from DGGE indicated an alteration in the structure of AMF communities in invaded soils. After 15 weeks, we found that plants grown in pots containing native roots presented higher stem and root growth and also produced higher biomass in comparison with plants grown with A. dealbata inoculum. Furthermore, plants that presented the highest biomass and growth exhibited the maximum mycorrhizal colonization and phosphorus content. Moreover, fluorescence measurements indicated that plants grown with A. dealbata inoculum even presented higher photosynthetic damage. Our results indicate that the presence of the invader A. dealbata modify the composition of the arbuscular fungal community, conditioning the establishment of native plants.
doi:10.1093/aobpla/plw018
PMCID: PMC4823375  PMID: 26984185
Acacia dealbata; DGGE; microbial community structure; plant invasion; Plantago lanceolata; root inoculum; soil sterilization
19.  Arbuscular Mycorrhizal Fungi as Natural Biofertilizers: Let's Benefit from Past Successes 
Arbuscular Mycorrhizal Fungi (AMF) constitute a group of root obligate biotrophs that exchange mutual benefits with about 80% of plants. They are considered natural biofertilizers, since they provide the host with water, nutrients, and pathogen protection, in exchange for photosynthetic products. Thus, AMF are primary biotic soil components which, when missing or impoverished, can lead to a less efficient ecosystem functioning. The process of re-establishing the natural level of AMF richness can represent a valid alternative to conventional fertilization practices, with a view to sustainable agriculture. The main strategy that can be adopted to achieve this goal is the direct re-introduction of AMF propagules (inoculum) into a target soil. Originally, AMF were described to generally lack host- and niche-specificity, and therefore suggested as agriculturally suitable for a wide range of plants and environmental conditions. Unfortunately, the assumptions that have been made and the results that have been obtained so far are often worlds apart. The problem is that success is unpredictable since different plant species vary their response to the same AMF species mix. Many factors can affect the success of inoculation and AMF persistence in soil, including species compatibility with the target environment, the degree of spatial competition with other soil organisms in the target niche and the timing of inoculation. Thus, it is preferable to take these factors into account when “tuning” an inoculum to a target environment in order to avoid failure of the inoculation process. Genomics and transcriptomics have led to a giant step forward in the research field of AMF, with consequent major advances in the current knowledge on the processes involved in their interaction with the host-plant and other soil organisms. The history of AMF applications in controlled and open-field conditions is now long. A review of biofertilization experiments, based on the use of AMF, has here been proposed, focusing on a few important factors that could increase the odds or jeopardize the success of the inoculation process.
doi:10.3389/fmicb.2015.01559
PMCID: PMC4717633  PMID: 26834714
arbuscular mycorrhizal fungi (AMF); abiotic and biotic stress; plant nutrition; inoculation; transcriptomics
20.  Short-term temporal variation in sporulation dynamics of arbuscular mycorrhizal (AM) fungi and physico-chemical edaphic properties of wheat rhizosphere 
In this study, we investigated the pattern of short-term temporal variation in the arbuscular mycorrhizal (AM) fungi and physico-chemical edaphic properties of some wheat growing areas of the Bundelkhand region, Central India. Rhizospheric soil samples were collected every month from December 2007 to May 2008 from four wheat growing sites around Jhansi (Bundelkhand region). AM fungal root colonization, sporulation and physico-chemical edaphic properties during this period were determined and compared to evaluate the dynamics of response of wheat towards the AMF along crop maturation. Maximum AMF root colonization recorded was 54.3% indicating that AMF, particularly in low phosphorus (P) soils, can be important even in case of less responsive crop like wheat. In the two out of four sites studied, the AMF spore density increased with the increase in soil temperature. Absence of this type of pattern in remaining two sites indicated that site-specific environmental and agricultural conditions may affect the degree of wheat response to AMF. It also suggested that AMF communities inhabiting agroecosystems may exhibit considerable temporal sporulation patterns. The maximum AMF colonization was observed during February–March 2008, whereas maximum AMF sporulation was noticed during March–April 2008. Statistically significant negative correlation of AMF spore density with pH, organic carbon (OC) and available P was observed in the one of the sites studied. Overall assessment of the data indicated that season and location significantly affected the interaction of AM fungi with winter wheat necessitating the further need to understand the ecology of AMF populations with reference to specific host species under different micro-climatic conditions of Bundelkhand region.
doi:10.1016/j.sjbs.2010.12.012
PMCID: PMC3730808  PMID: 23961131
Arbuscular mycorrhizal fungi; Sporulation dynamics; Edaphic properties; Temporal variation; Wheat; Rhizosphere
21.  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.
doi:10.1038/ismej.2013.112
PMCID: PMC3806264  PMID: 23823490
Rhizophagus irregularis; intraspecific competition; coexistence; symbiosis; mycorrhiza
22.  Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem 
Plants interact with a variety of other community members that have the potential to indirectly influence each other through a shared host plant. Arbuscular mycorrhizal fungi (AMF) are generally considered plant mutualists because of their generally positive effects on plant nutrient status and growth. AMF may also have important indirect effects on plants by altering interactions with other community members. By influencing plant traits, AMF can modify aboveground interactions with both mutualists, such as pollinators, and antagonists, such as herbivores. Because herbivory and pollination can dramatically influence plant fitness, comprehensive assessment of plant–AMF interactions should include these indirect effects. To determine how AMF affect plant–insect interactions, we grew Cucumis sativus (Cucurbitaceae) under five AMF inoculum treatments and control. We measured plant growth, floral production, flower size, and foliar nutrient content of half the plants, and transferred the other half to a field setting to measure pollinator and herbivore preference of wild insects. Mycorrhizal treatment had no effect on plant biomass or floral traits but significantly affected leaf nutrients, pollinator behavior, and herbivore attack. Although total pollinator visitation did not vary with AMF treatment, pollinators exhibited taxon-specific responses, with honey bees, bumble bees, and Lepidoptera all responding differently to AMF treatments. Flower number and size were unaffected by treatments, suggesting that differences in pollinator preference were driven by other floral traits. Mycorrhizae influenced leaf K and Na, but these differences in leaf nutrients did not correspond to variation in herbivore attack. Overall, we found that AMF indirectly influence both antagonistic and mutualistic insects, but impacts depend on the identity of both the fungal partner and the interacting insect, underscoring the context-dependency of plant–AMF interactions.
doi:10.3389/fpls.2013.00338
PMCID: PMC3763484  PMID: 24046771
aboveground–belowground; arbuscular mycorrhizal fungi; Cucumis sativus; herbivore; indirect interaction; pollinator
23.  Effect of combined microbes on plant tolerance to Zn–Pb contaminations 
The presence and composition of soil microbial communities has been shown to have a large impact on plant–plant interactions and consequently plant diversity and composition. The goal of the present study was to evaluate impact of arbuscular mycorrhizal fungi (AMF) and nitrogen-fixing bacteria, which constitutes an essential link between the soil and the plant’s roots. A greenhouse pot experiment was conducted to evaluate the feasibility of using selected microbes to improve Hieracium pilosella and Medicago sativa growth on Zn–Pb-rich site. Results of studies revealed that biomass, the dry mass of shoots and roots, increased significantly when plants were inoculated with mycorrhizal fungi and nitrogen-fixing bacteria. The addition of Azospirillum sp. and Nostoc edaphicum without mycorrhiza suppressed plant growth. Single bacterial inoculation alone does not have a positive effect on M. sativa growth, while co-inoculation with AMF improved plant growth. Plant vitality (expressed by the performance index) was improved by the addition of microbes. However, our results indicated that even dry heat sterilization of the substratum created imbalanced relationships between soil-plant and plants and associated microorganisms. The studies indicated that AMF and N2-fixers can improve revegetation of heavy metal-rich industrial sites, if the selection of interacting symbionts is properly conducted.
Electronic supplementary material
The online version of this article (doi:10.1007/s11356-015-5094-2) contains supplementary material, which is available to authorized users.
doi:10.1007/s11356-015-5094-2
PMCID: PMC4669377  PMID: 26250813
Plant/microbial interactions; Arbuscular mycorrhizal fungi (AMF); N2-fixing bacteria; Cyanobacteria; Co-cropping; Plant vitality
24.  Precipitation shapes communities of arbuscular mycorrhizal fungi in Tibetan alpine steppe 
Scientific Reports  2016;6:23488.
Tibetan Plateau is one of the largest and most unique habitats for organisms including arbuscular mycorrhizal fungi (AMF). However, it remains unclear how AMF communities respond to key environmental changes in this harsh environment. To test if precipitation could be a driving force in shaping AMF community structures at regional scale, we examined AMF communities associated with dominant plant species along a precipitation gradient in Tibetan alpine steppe. Rhizosphere soils were collected from five sites with annual precipitation decreasing from 400 to 50 mm. A total of 31 AMF operational taxonomic units (OTUs) were identified. AMF community composition varied significantly among sites, whereas AMF community composition did not vary among plant species. Path analysis revealed that precipitation directly affected AMF hyphal length density, and indirectly influenced AMF species richness likely through the mediation of plant coverage. Our results suggested that water availability could drive the changes of AMF communities at regional scale. Given the important roles AMF could play in the dynamics of plant communities, exploring the changes of AMF communities along key environmental gradients would help us better predict the ecosystem level responses of the Tibetan vegetation to future climate change.
doi:10.1038/srep23488
PMCID: PMC4802204  PMID: 27002188
25.  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.
doi:10.1007/s00122-010-1501-8
PMCID: PMC3043257  PMID: 21222096

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