Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids

The effects of arbuscular mycorrhizal colonization of Leucanthemum vulgare on parasitism of a leaf‐mining insect was studied in a field and a laboratory experiment. In the field, parasitism of Chromatomyia syngenesiae by Diglyphus isaea was lower on mycorrhizal plants, compared with plants where the association was reduced. A laboratory experiment, in which L. vulgare was inoculated with three species of AM fungi, showed that the effects on parasitism rates were mycorrhizal species‐dependent. Some fungal combinations increased parasitism, some decreased it, while others had no effect. It is concluded that the most likely cause of these differences is plant size, with parasitoid searching efficiency being reduced on the larger plants, resulting from certain mycorrhizal species combinations. However, a mycorrhizal effect on herbivore‐produced plant volatiles cannot be ruled out.     

Life history plasticity and fitness in a caddisfly in response to proximate cues of pond-drying

The majority of plants are involved in symbioses with arbuscular mycorrhizal fungi (AMF), and these associations are known to have a strong influence on the performance of both plants and insect herbivores. Little is known about the impact of AMF on complex trophic chains, although such effects are conceivable. In a greenhouse study we examined the effects of two AMF species, Glomus intraradices and G. mosseae on trophic interactions between the grass Phleum pratense, the aphid Rhopalosiphum padi, and the parasitic wasp Aphidius rhopalosiphi. Inoculation with AMF in our study system generally enhanced plant biomass (+5.2%) and decreased aphid population growth (−47%), but there were no fungal species-specific effects. When plants were infested with G. intraradices, the rate of parasitism in aphids increased by 140% relative to the G. mosseae and control treatment. When plants were associated with AMF, the developmental time of the parasitoids decreased by 4.3% and weight at eclosion increased by 23.8%. There were no clear effects of AMF on the concentration of nitrogen and phosphorus in plant foliage. Our study demonstrates that the effects of AMF go beyond a simple amelioration of the plants’ nutritional status and involve rather more complex species-specific cascading effects of AMF in the food chain that have a strong impact not only on the performance of plants but also on higher trophic levels, such as herbivores and parasitoids.     

Nitrogen limitation impairs plant control over the arbuscular mycorrhizal symbiosis in response to phosphorus and shading in two European sand dune species

The symbiosis of plants with arbuscular mycorrhizal fungi (AMF) may become parasitic if the cost:benefit ratio (carbon:phosphorus ratio) increases. In case of mycorrhizal parasitism, a plant may prevent growth depression through the reduction of root colonization as a form of control over the symbiosis. In this greenhouse study, we attempted to manipulate the cost:benefit ratio of the arbuscular mycorrhizal symbiosis by shading and/or phosphorus (P) fertilization in the differentially mycotrophic plant species Hieracium pilosella and Corynephorus canescens. By repeated sampling of soil cores, we assessed the temporal progress of plant investment towards mycorrhizal structures as a measure of plant control over the AMF. Unexpectedly, we found no obvious treatment effects on mycorrhizal growth dependency (MGD), most likely caused by constant N-limitation in AM plants being enhanced by P-fertilization and shade probably not exacerbating plant C-budget for AMF. This highlights the importance of N:P:C stoichiometry for the outcome of the symbiosis. Nevertheless, we found possible control mechanisms in shaded H. pilosella, with considerably higher resource investments into root than into hyphal growth, while root colonization was only marginally suppressed. This control only manifested after 4 weeks of growth under potentially detrimental conditions, emphasizing the importance of time in plant control over the arbuscular mycorrhizal symbiosis. In contrast, the less mycotrophic C. canescens did not exhibit obvious changes in mycorrhizal investments in reaction to shading and P-fertilization, possibly because the low mycotrophy and AMF colonization already imposes a functioning control mechanism in this species. Our study suggests that highly mycotrophic plants may have a stronger need to keep AMF in check than less mycotrophic plants, which may have implications for the role of mycotrophy in the outcome of symbiotic interactions in natural situations.     

Evidence for leaf endophyte regulation of root symbionts: effect of <Emphasis Type="Italic">Neotyphodium</Emphasis> endophytes on the pre-infective state of mycorrhizal fungi

Neotyphodium endophytes and arbuscular mycorrhizal (AM) fungi are common constituents of natural grasslands. The plant–endophyte symbiosis can introduce changes in soil conditions that affect the density and activity of different functional groups of soil organisms. In the present work we performed in vitro assays to evaluate the effect of root and endophyte exudates on the pre-infective state of mycorrhizal fungi (Gigaspora margarita and G. rosea). Plant roots of Bromus setifolius from populations of Patagonia, and four strains of Neotyphodium were used to obtain the exudates. Root exudates of infected plants, at a high concentration, significantly increased AMF hyphal branches and length relative to exudates from naturally endophyte free plants. The effect of Neotyphodium endophyte exudates on AMF mycelial length varied depending on strain and the concentration used, suggesting a differential interaction between endophyte and AMF species. AMF hyphal branches were increased by Neotyphodium fungal exudates in both mycorrhizal species. A few previous studies have suggested that Neotyphodium endophytes can reduce mycorrhizal sporulation and colonization of host roots in commonly-cultivated agronomic hosts. In this study we report the opposite effect in B. setifolius. This study reports the direct and positive effect of root exudates from plants in symbiosis with Neotyphodium, on AMF pre-infective state. Further, identical effects were detected using exudates from Neotyphodium endophytes.     

Direct and indirect influences of arbuscular mycorrhizal fungi on phosphorus uptake by two root hemiparasitic Pedicularis species: do the fungal partners matter at low colonization levels?

Background and Aims

Because most parasitic plants do not form mycorrhizal associations, the nutritional roles of arbuscular mycorrhizal (AM) fungi in them have hardly been tested. Some facultative root hemiparasitic Pedicularis species form AM associations and hence are ideal for testing both direct and indirect effects of AM fungi on their nutrient acquisition. The aim of this study was to test the influence of AM inoculation on phosphorus (P) uptake by Pedicularis rex and P. tricolor.

Methods

³²P labelling was used in compartmented pots to assess the contribution of the AM pathway and the influence of AM inoculation on P uptake from a host plant into the root hemiparasites. Laboratory isolates of fungal species (Glomus mosseae and G. intraradices) and the host species (Hordeum vulgare ‘Fleet’) to which the two Pedicularis species showed obvious responses in haustorium formation and growth in previous studies were used.

Key Results

The AM colonization of both Pedicularis spp. was low (<15 % root length) and only a very small proportion of total plant P (<1 %) was delivered from the soil via the AM fungus. In a separate experiment, inoculation with AM fungi strongly interfered with P acquisition by both Pedicularis species from their host barley, almost certainly because the numbers of haustoria formed by the parasite were significantly reduced in AM plants.

Conclusions

Roles of AM fungi in nutrient acquisition by root parasitic plants were quantitatively demonstrated for the first time. Evidence was obtained for a novel mechanism of preventing root parasitic plants from overexploiting host resources through AM fungal-induced suppression of the absorptive structures in the parasites.     

Infection by mycorrhizal fungi increases natural enemy abundance on tobacco (Nicotiana rustica)

The presence of arbuscular mycorrhizal fungi (AMF) influences plant nutrient uptake, growth, and plant defensive chemistry, thereby directly influencing multi-trophic interactions. Different fungal isolates (genotypes of the same fungal species) have been shown to differ in nutrient uptake ability. Plants infected with different AMF genotypes may vary in foliar nutrient or defensive chemical levels, potentially influencing multi-trophic interactions. Using a completely randomized design, we compared the effect of two isolates of the mycorrhizal fungus Glomus etunicatum W. N. Becker & Gerdemann on silver leaf whitefly (Bemisia argentifolii Bellows & Perring) (Hemiptera: Aleyrodidae) and parasitic wasp (Eretmocerus eremicus Rose & Zolnerowich) (Hymenoptera: Aphelinidae) abundance. Whitefly populations were not influenced by AMF infection. Parasite populations were higher on plants infected with the isolate collected from Georgia, even after controlling for whitefly abundance and plant architecture. We propose that AMF indirectly influences parasite abundance and parasitism through a change in leaf surface chemicals that affect parasitic wasps. Because of the ubiquity of and genetic variation in AMF, multi-trophic interactions are likely to be strongly influenced by belowground processes.     

Context‐dependent effects of mycorrhizae on herbivore density and parasitism in a tritrophic coastal study system

1. Stressful abiotic conditions and mycorrhizal fungi have both been shown to influence plant quality significantly, yet the interactive effects of these factors on relationships among plants, herbivores, and natural enemies remain unclear. 2. In this study, the results of a factorial field experiment are reported in which the effects of plant stress and mycorrhizae on density and parasitism of three herbivores of Baccharis halimifolia L. were examined. 3. Plant stress was increased by adding salt to the soil, and association with mycorrhizal fungi was increased by inoculating plant roots. 4. Inoculation with mycorrhizal fungi resulted in increased density of all three herbivore species, but the effects of mycorrhizae on parasitism varied by species and with soil salinity levels. For the gall maker Neolasioptera lathami Gagne, mycorrhizae decreased parasitism regardless of soil salinity levels. For the leaf miners Amauromyza maculosa Malloch and Liriomyza trifolii Burgess, mycorrhizae effectively negated the decrease in parasitism resulting from increased salinity. 5. The results of this study show that the effects of mycorrhizae on parasitism may be context dependent, and can be positive or negative depending upon species and environmental conditions.     

Mycorrhiza‐mediated interference between cover crop and weed in organic winter cereal agroecosystems: The mycorrhizal colonization intensity indicator

The mycorrhizal fungi are symbiotic organisms able to provide many benefits to crop production by supplying a set of ecosystem functions. A recent ecological approach based on the ability of the fungi community to influence plant–plant interactions by extraradical mycelium development may be applied to diversified, herbaceous agroecosystems. Our hypothesis is that the introduction of a winter cereal cover crop (CC) as arbuscular mycorrhizal fungi (AMF)–host plant in an organic rotation can boosts the AMF colonization of the other plants, influencing crop–weed interference. In a 4‐years organic rotation, the effect of two winter cereal CC, rye and spelt, on weed density and AMF colonization was evaluated. The AMF extraradical mycelium on CC and weeds roots was observed by scanning electron microscopy analysis. By joining data of plant density and mycorrhization, we built the mycorrhizal colonization intensity of the Agroecosystem indicator (MA%). Both the CC were colonized by soil AMF, being the mycorrhizal colonization intensity (M%) affected by environmental conditions. Under CC, the weed density was reduced, due to the increase of the reciprocal competition in favor of CC, which benefited from mycorrhizal colonization and promoted the development of AMF extraradical mycelium. Even though non‐host plants, some weed species showed an increased mycorrhizal colonization in presence of CC respect to the control. Under intense rainfall, the MA% was less sensitive to the CC introduction. On the opposite, under highly competitive conditions, both the CC boosted significantly the mycorrhization of coexistent plants in the agroecosystem. The proposed indicator measured the agroecological service provided by the considered CCs in promoting or inhibiting the overall AMF colonization of the studied agroecosystems, as affected by weed selection and growth: It informs about agroecosystem resilience and may be profitably applied to indicate the extent of the linkage of specific crop traits to agroecosystem services, contributing to further develop the functional biodiversity theory.     

Arbuscular mycorrhiza‐mediated resistance in tomato against Cladosporium fulvum‐induced mould disease

Root colonization with arbuscular mycorrhizal fungi (AMF) enhances plant resistance particularly against soil‐borne pathogenic fungi. In this study, mycorrhizal inoculation with Glomus mosseae (Gm) significantly alleviated tomato mould disease caused by the air‐borne fungal pathogen, Cladosporium fulvum (Cf). The disease index (DI) in local leaves (receiving pathogen inoculation) and systemic leaves (just above the local leaf without pathogen inoculation) was 36.4% and 11.7% in mycorrhizal plants, respectively, whereas DI was 59.6% and 36.4% in the corresponding leaves of AMF non‐inoculated plants, after 50 days of Gm inoculation, corresponding to 15 days after Cf inoculation by leaf infiltration. Foliar spray inoculation with Cf also revealed that AMF pre‐inoculated plants had a higher resistance against subsequent pathogen infection, where the DI was 41.3% in mycorrhizal plants vs. 64.4% in AMF non‐inoculated plants. AMF‐inoculated plants showed significantly higher fresh and dry weight than non‐inoculated plants under both control (without pathogen) and pathogen treatments. AMF‐inoculated plants exhibited significant increases in activities of superoxide dismutase and peroxidase, along with decreases in levels of H₂O₂ and malondialdehyde, compared with non‐inoculated plants after pathogen inoculation. AMF inoculation led to increases in total chlorophyll contents and net photosynthesis rate as compared with non‐inoculated plants under control and pathogen infection. Pathogen infection on AMF non‐inoculated plants led to decreases in chlorophyll fluorescence parameters. However, pathogen infection did not affect these parameters in mycorrhizal plants. Taken together, these results indicate that AMF colonization may play an important role in plant resistance against air‐borne pathogen infection by maintaining redox poise and photosynthetic activity.     

Interrelated effects of mycorrhiza and free‐living nitrogen fixers cascade up to aboveground herbivores

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.     

Parasitism of arbuscular mycorrhizal fungi: reviewing the evidence.

In order to understand the functioning of mycorrhizal fungi in ecosystems it is necessary to consider the full suite of possible biotic interactions in the soil. While a number of such interactions have recently been shown to be crucially important, parasitism is a highly neglected feature in the ecology of arbuscular mycorrhizal fungi (AMF). A number of studies have classified some interactions between populations of bacteria and fungi with AMF as parasitism, generating discussion about its consequences at both 'parasite' and host population levels. This paper reviews these various publications, and based on a set of criteria that are necessary to demonstrate parasitism, it was concluded that parasitism has not been conclusively shown to exist in AMF, even though some data are highly suggestive of such a relationship. The difficulties in gathering data supportive of parasitism were discussed, and hypotheses for defense were offered. This paper concludes by presenting potential consequences of AMF parasitism at the population/community levels and by discussing applied aspects.     

Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference

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Mycorrhizal and dark septate endophytic fungi of <Emphasis Type="Italic">Pedicularis</Emphasis> species from northwest of Yunnan Province,China

Colonization of mycorrhizal and root endophytic fungi in 14 Pedicularis species from northwest of Yunnan Province, southwest China, was examined. These species included: Pedicularis gracilis Wall., Pedicularis longipes Maxim., Pedicularis axillaris Franch., Pedicularis cephalantha Franch., Pedicularis tenuisecta Franch., Pedicularis tapaoensis Tsoong, Pedicularis likiangensis Franch., Pedicularis dichotoma Bonati, Pedicularis yui Li, Pedicularis rhinanthoides Schrenk, Pedicularis rex C.B. Clarke, Pedicularis longiflora Rudolph., Pedicularis siphonantha Don, and Pedicularis oxycarpa Franch., among which nine are endemic to China (one to Yunnan). Three types of potentially beneficial fungi associated with roots of these species were observed, namely, arbuscular mycorrhizal fungi, ectomycorrhizal fungi, and dark septate endophytic fungi (DSEF), with DSEF as the most common colonizers. An unexpected high colonization level was detected in this hemiparasitic genus. Of the 19 sampling sites examined, 10 gave colonization frequency of above 50% and 6 showed a colonization index of above 50. Heavy colonization suggested a significant ecological role of these fungi and their potential to be applied to successful cultivation of these intractable plants.     

Which role can arbuscular mycorrhizal fungi play in the facilitation of Ambrosia artemisiifolia L. invasion in France?

Ambrosia artemisiifolia L. (common ragweed), an annual invasive plant, was introduced more than 100 years ago from North America to Europe. Like the majority of other invasive plants in Europe, it develops in open, disturbed areas such as fields, wastelands, roadsides, and riverbanks. Recently, arbuscular mycorrhizal fungi (AMF) have been suspected to play a role in some plant invasion processes. As the common ragweed is known to be colonized by AMF in its native range, the intensity of mycorrhizal root colonization was studied in 35 natural populations in eastern France. About 94% of the A. artemisiifolia populations sampled were mycorrhizal. Root colonization levels varied from 1 to 40% depending on the ecological sites, with lower levels for agricultural habitats and higher levels in disturbed sites, such as wastelands or roadsides. A subsequent greenhouse experiment showed positive impacts of AMF on the growth and development of A. artemisiifolia. It is proposed that the spread of this invasive plant species could be facilitated by AMF, underlining the need to integrate symbiotic interactions in future work on invasive plant processes.     

Differential host plant performance as a function of soil arbuscular mycorrhizal fungal communities: experimentally manipulating co-occurring Glomus species

In order to evaluate host plant performance relative to different soil arbuscular mycorrhizal fungal (AMF) communities, Andropogon gerardii seedlings were grown with nine different AMF communities. The communities consisted of 0, 10, or 20 spores of Glomus etunicatum and 0, 10, or 20 spores of Glomus intraradices in all possible combinations. Spores were produced by fungal cultures originating on A. gerardii in a serpentine plant community; seeds of A. gerardii were collected at the same site. The experiment was performed in the greenhouse using a mixture of sterilized serpentine soil and sand to which naturally occurring non-mycorrhizal microbes were added. There was no difference in root AMF colonization rates between single species communities of either G. etunicatum or G. intraradices, but G. intraradices enhanced plant growth and G. etunicatum did not. However, plants grew larger with some combinations of G.␣intraradices plus G. etunicatum than with the same quantity of G. intraradices alone. These results suggest the potential for niche complementarity in the mycorrhizal fungi. That G. etunicatum only increased plant growth in the presence of G. intraradices could be illustrative of why AMF that appear to be parasitic or benign when examined in isolation are maintained within multi-species mycorrhizal communities in nature.     

Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi

Interactions between arbuscular mycorrhizal fungal (AMF) species cocolonizing the same host plant are still little understood in spite of major ecological significance of mycorrhizal symbiosis and widespread occurrence of these fungi in communities rather than alone. Furthermore, shifting the composition of AMF communities has demonstrated consequences for the provision of symbiotic benefits to the host as well as for the qualities of ecosystem services. Therefore, here we addressed the nature and strength of interactions between three different AMF species in all possible two‐species combinations on a gradient of inoculation densities. Fungal communities were established in pots with Medicago truncatula plants, and their composition was assessed with taxon‐specific real‐time PCR markers. Nature of interactions between the fungi was varying from competition to facilitation and was influenced by both the identity and relative abundance of the coinoculated fungi. Plants coinoculated with Claroideoglomus and Rhizophagus grew bigger and contained more phosphorus than with any of these two fungi separately, although these fungi obviously competed for root colonization. On the other hand, plants coinoculated with Gigaspora and Rhizophagus, which facilitated each other's root colonization, grew smaller than with any of these fungi separately. Our results point to as yet little understood complexity of interactions in plant‐associated symbiotic fungal communities, which, depending on their composition, can induce significant changes in plant host growth and/or phosphorus acquisition in either direction.     

不同强度盐胁迫下AM真菌对羊草生长的影响

不同浓度NaCl盐处理下,AM真菌对羊草(Leymus chinensis)的侵染能力和对植物生长的影响,从植物形态和离子含量角度探讨了AM真菌提高羊草耐盐性的作用机理。结果表明,在高盐胁迫下,AM真菌显著降低了盐胁迫效应,提高了羊草生物量,菌根效应明显。菌根化羊草的根茎比显著增加,并且N、P浓度较高,Na~+和Cl~-离子浓度较低,表明AM真菌即促进羊草对营养元素的吸收,又减少了离子毒害。菌根化羊草的Ca~(2+)和K~+离子浓度,以及P/Na~+和K~+/Na~+比高于非菌根化羊草,表明AM真菌可通过调节渗透势以避免或减缓盐胁迫造成的生理缺水。随着盐胁迫的增加,菌根化羊草对磷的依赖性逐渐转换为对钾的依赖性。研究结果有助于揭示AM真菌提高植物耐盐能力的作用机理,并对应用菌根技术修复盐化草地具有理论指导意义。     

Mycorrhizal Fungal Effects on Growth,Antioxidant Capacity,and Medicine Quality of <i>Paris polyphylla</i> var. <i>yunnanensis</i>

A field experiment was conducted to determine the effects of two commercial strains composed of mulple arbuscular mycorrhizal fungi (AMF) species on plant growth, antioxidant capacity, and medicine quality of Paris polyphylla var. yunnanensis in three subtropical soils from Wanzhou, Anshun and Baoshan in fields. The results showed that AMF inoculation enhanced the fungal colonization rate and activities of both succinate dehydrogenase and alkaline phosphatase, thereby, enhancing the mycorrhizal viability of P. polyphylla var. yunnanensis. The concentrations of photosynthetic pigments (chlorophyll a, b, a+b and carotenoids), soluble sugar, soluble protein and photosynthetic capacity were higher in AMF-inoculated plants than in non-AMF-treated plants in field. AMFtreated plants recorded higher activities of catalase, peroxidase and superoxide dismutase, and caused the reduction in malondialdehyde content, indicating lower oxidative damage, compared with non-AMF plants. Polyphyllin I, Polyphyllin II, Polyphyllin III, Polyphyllin IV and total polyphyllin contents were increased by AMF treatment. In conclusion, AMF improved the plant growth, antioxidant capacity and medicinal quality of P. polyphylla var. yunnanensis seedlings. Hereinto, AMF effects on the soil from Wanzhou was relatively greater than on other soils.     

Moderate drought influences the effect of arbuscular mycorrhizal fungi as biocontrol agents against Verticillium-induced wilt in pepper

Previous studies have shown that the arbuscular mycorrhizal fungus (AMF) Glomus deserticola (Trappe, Bloss and Menge) can diminish the negative effect of Verticillium dahliae Kleb. on pepper yield. On the other hand, it is known that AMF can be more beneficial for plant growth and physiology under dry conditions than when soil moisture is plentiful. Therefore, our objective was to assess if a moderate water deficit imposed on pepper plants before their inoculation with V. dahliae could improve the effectiveness of G. deserticola as biocontrol agent. In the present experiment, the delay in disease development in Verticillium-inoculated plants associated with AMF did not occur under well watered conditions. In addition, the establishment of mycorrhizal symbiosis and the development of structures by AMF were delayed when both symbiotic and pathogenic fungi infected the same root. Therefore, it is suggested that the equilibrium between pepper plant, G. deserticola and V. dahliae is so complex that small changes in competition between symbiotic and pathogenic fungi for host resources can modify the efficiency of AMF as a biocontrol agent. On the other hand, water deficit enhanced the deleterious effect of V. dahliae on fruit set and yield only when pepper plants were not associated with G. deserticola, which reinforces the idea that AMF may be more important for host plants subjected to stressful conditions. However, comparing well watered non-mycorrhizal and predroughted mycorrhizal plants, we found that moderate water deficit imposed before inoculation with V. dahliae did not improve the effectiveness of G. deserticola as a biocontrol agent.