Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions

Complex relationships occur among plants, mycorrhizal fungi, and herbivores. By altering plant nutrient status, mycorrhizas may alter herbivory or plant tolerance to herbivory via compensatory regrowth. We examined these interactions by assessing grasshopper preference and plant growth and fungal colonization responses to herbivory under mycorrhizal and non‐mycorrhizal conditions within tallgrass prairie microcosms. Mycorrhizal symbiosis increased plant regrowth following defoliation, and some strongly mycotrophic plant species showed overcompensation in response to herbivory when they were mycorrhizal. Although grasshoppers spent more time on mycorrhizal plants, herbivory intensity did not differ between mycorrhizal and non‐mycorrhizal plants. Aboveground herbivory by grasshoppers significantly increased mycorrhizal fungal colonization of plant roots. Thus mycorrhizas may greatly benefit plants subjected to herbivory by stimulating compensatory growth, and herbivores, in turn, may increase the development of the symbiosis. Our results also indicate strong interspecific differences among tallgrass prairie plant species in their responses to the interaction of aboveground herbivores and mycorrhizal symbionts.     

Root fungal symbionts interact with mammalian herbivory, soil nutrient availability and specific habitat conditions

Herbivory, competition and soil fertility interactively shape plant communities and exhibit an important role in modifying conditions for host-dependent fungal symbionts. However, field studies on the combined impacts of natural herbivory, competition and soil fertility on root fungal symbionts are rare. We asked how mammalian herbivory, fertilization, liming and plant–plant competition affect the root colonization of arbuscular mycorrhizal fungi (AMF) and dark septate endophytic (DSE) fungi of the dicot herb, Solidago virgaurea. The 2-year full-factorial experiment was conducted in two contrasting habitats: non-acidic and acidic mountain tundra. We found that herbivory increased arbuscular colonization (i.e. the site of resource exchange) at fertile non-acidic sites, where vegetation was rich in species having AMF symbionts, whereas at infertile acidic sites, where plants having AMF symbiont are scarce, the response was the opposite. Herbivory of the host plant negatively affected DSE hyphal and sclerotial colonization in unfertilized plots, possibly due to reduced carbon flow from the host plant while there was no effect of herbivory in fertilized plots. DSE colonization was highest in unfertilized exclosures where soil nutrient concentrations were also lowest. Liming had a negative effect on DSE hyphal colonization, and its effect also interacted with herbivory and the habitat. Biomass removal of the neighboring plants did not affect the root colonization percent of either arbuscules or DSE. Our results show that the impacts of aboveground mammalian herbivory, soil nutrient availability and specific habitat conditions on belowground root fungal symbionts are highly dependent on each other. Arbuscule response to herbivory appeared to be regulated by specific habitat conditions possibly caused by differences in the AMF availability in the soil while DSE response was associated with availability of host-derived carbon. Our result of the relationship between herbivory and soil nutrients suggests an important role of DSE in ecosystem processes.     

Plant Kin Recognition Enhances Abundance of Symbiotic Microbial Partner

Background

The stability of cooperative interactions among different species can be compromised by cheating. In the plant-mycorrhizal fungi symbiosis, a single mycorrhizal network may interact with many plants, providing the opportunity for individual plants to cheat by obtaining nutrients from the fungi without donating carbon. Here we determine whether kin selection may favour plant investment in the mycorrhizal network, reducing the incentive to cheat when relatives interact with a single network.

Methodology/Principal Findings

We show that mycorrhizal network size and root colonization were greater when Ambrosia artemisiifolia L. was grown with siblings compared to strangers. Soil fungal abundance was positively correlated with group leaf nitrogen, and increased root colonization was associated with a reduced number of pathogen-induced root lesions, indicating greater benefit to plants grown with siblings.

Conclusions/Significance

Plants can benefit their relatives through investment in mycorrhizal fungi, and kin selection in plants could promote the persistence of the mycorrhizal symbiosis.     

Do compensatory shoot growth and mycorrhizal symbionts act as competing above- and below-ground sinks after simulated grazing?

Since mycorrhizal symbionts are dependent on host carbon availability, shading and grazing of the host plant often decrease mycorrhizal colonization in host roots. We conducted field experiments on an intensively mycorrhizal host, Autumn gentian, Gentianella amarella to investigate the effects of neighbor removal and simulated grazing on host growth and reproduction as well as mycorrhizal colonization. In the neighbor removal experiment, we manually removed the above-ground parts of companion plants of gentians. Reduced competition tended to improve the performance of both the host and the symbionts. Total fungal as well as arbuscular, hyphal, and coiled hyphal colonizations were higher in gentians with neighbors removed. Simulated grazing (clipping off 50% of shoot height) reduced host shoot and seed biomass, whereas the responses of the root symbionts were most often positive or neutral. In the first experiment (with late-flowering plants), clipping increased arbuscular, hyphal, and total colonizations but decreased dark septate endophyte colonization. In the second experiment (with both early- and late-flowering plants), clipping did not affect total mycorrhizal colonization. Higher arbuscular, hyphal, and total colonizations were found in late-flowering gentians compared to early-flowering ones. Early-flowering plants, on the other hand, tolerated simulated grazing better compared to late-flowering plants, which may indicate a higher cost of the symbionts for the late-flowering plants. Above-ground herbivory tends to increase carbon limitation, and under these conditions, regrowing shoots and the fungal symbionts may appear as alternative, competing sinks for the host’s limited carbon reserves.     

Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply

Considered to play an important role in plant mineral nutrition, arbuscular mycorrhizal (AM) symbiosis is a common relationship between the roots of a great majority of plant species and glomeromycotan fungi. Its effects on the plant host are highly context dependent, with the greatest benefits often observed in phosphorus (P)‐limited environments. Mycorrhizal contribution to plant nitrogen (N) nutrition is probably less important under most conditions. Moreover, inasmuch as both plant and fungi require substantial quantities of N for their growth, competition for N could potentially reduce net mycorrhizal benefits to the plant under conditions of limited N supply. Further compounded by increased belowground carbon (C) drain, the mycorrhizal costs could outweigh the benefits under severe N limitation. Using a field AM fungal community or a laboratory culture of Rhizophagus irregularis as mycorrhizal inoculants, we tested the contribution of mycorrhizal symbiosis to the growth, C allocation, and mineral nutrition of Andropogon gerardii growing in a nutrient‐poor substrate under variable N and P supplies. The plants unambiguously competed with the fungi for N when its supply was low, resulting in no or negative mycorrhizal growth and N‐uptake responses under such conditions. The field AM fungal communities manifested their potential to improve plant P nutrition only upon N fertilization, whereas the R. irregularis slightly yet significantly increased P uptake of its plant host (but not the host's growth) even without N supply. Coincident with increasing levels of root colonization by the AM fungal structures, both inoculants invariably increased nutritional and growth benefits to the host with increasing N supply. This, in turn, resulted in relieving plant P deficiency, which was persistent in non‐mycorrhizal plants across the entire range of nutrient supplies.     

Defoliation increases carbon limitation in ectomycorrhizal symbiosis of <Emphasis Type="Italic">Betula pubescens</Emphasis>

Boreal forest trees are highly dependent on root-colonizing mycorrhizal fungi. Since the maintenance of mycorrhizal symbiosis implies a significant carbon cost for the host plant, the loss of photosynthetic leaf area due to herbivory is expected to reduce the host investment in mycorrhizae. We tested this hypothesis in a common garden experiment by exposing ectomycorrhizal white birch (Betula pubescens Ehrh.) seedlings to simulated insect defoliation of 50 or 100% intensity during either the previous or the current summer or repeatedly during both seasons before harvest. The shoot and root growth of the seedlings were distinctly reduced by both 100% defoliation and repeated 50% defoliation, and they were more strongly affected by previous-year than current-year defoliation. The root to shoot ratio significantly decreased after 100% defoliation, indicating reduced proportional allocation to the roots. Ergosterol concentration (i.e. fungal biomass) in the fine roots decreased by 100% defoliation conducted either in the year of harvest or in both years. No such decrease occurred following the 100% defoliation conducted in the previous year, indicating the importance of current photosynthates for fungal symbionts. The trend was similar in the colonization percentage of thick-mantled mycorrhizae in the roots, the most marked decline occurring in the repeatedly defoliated seedlings. The present results thus support the prediction that the plant investment in ectomycorrhizae may decline as a response to foliage loss. Moreover, the colonization percentage of thick-mantled mycorrhizae correlated positively with the ratio of leaf to heterotrophic plant biomass in the defoliated birch seedlings, but not in the control ones. This tends to indicate a stronger carbon limitation of ectomycorrhizal colonization in defoliated seedlings.     

Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa

Individual plants typically interact with multiple mutualists and enemies simultaneously. Plant roots encounter both arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi, while the leaves are exposed to herbivores. AMF are usually beneficial symbionts, while the functional role of DSE is largely unknown. Leaf herbivory may have a negative effect on root symbiotic fungi due to decreased carbon availability. However, evidence for this is ambiguous and no inoculation-based experiment on joint effects of herbivory on AM and DSE has been done to date. We investigated how artificial defoliation impacts root colonization by AM (Glomus intraradices) and DSE (Phialocephala fortinii) fungi and growth of Medicago sativa host in a factorial laboratory experiment. Defoliation affected fungi differentially, causing a decrease in arbuscular colonization and a slight increase in DSE-type colonization. However, the presence of one fungal species had no effect on colonization by the other or on plant growth. Defoliation reduced plant biomass, with this effect independent of the fungal treatments. Inoculation by either fungal species reduced root/shoot ratios, with this effect independent of the defoliation treatments. These results suggest AM colonization is limited by host carbon availability, while DSE may benefit from root dieback or exudation associated with defoliation. Reductions in root allocation associated with fungal inoculation combined with a lack of effect of fungi on plant biomass suggest DSE and AMF may be functional equivalent to the plant within this study. Combined, our results indicate different controls of colonization, but no apparent functional consequences between AM and DSE association in plant roots in this experimental setup.     

Continental‐scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks

Most tree roots on Earth form a symbiosis with either ecto‐ or arbuscular mycorrhizal fungi. Nitrogen fertilization is hypothesized to favor arbuscular mycorrhizal tree species at the expense of ectomycorrhizal species due to differences in fungal nitrogen acquisition strategies, and this may alter soil carbon balance, as differences in forest mycorrhizal associations are linked to differences in soil carbon pools. Combining nitrogen deposition data with continental‐scale US forest data, we show that nitrogen pollution is spatially associated with a decline in ectomycorrhizal vs. arbuscular mycorrhizal trees. Furthermore, nitrogen deposition has contrasting effects on arbuscular vs. ectomycorrhizal demographic processes, favoring arbuscular mycorrhizal trees at the expense of ectomycorrhizal trees, and is spatially correlated with reduced soil carbon stocks. This implies future changes in nitrogen deposition may alter the capacity of forests to sequester carbon and offset climate change via interactions with the forest microbiome.     

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.     

Early Root Herbivory Impairs Arbuscular Mycorrhizal Fungal Colonization and Shifts Defence Allocation in Establishing Plantago lanceolata

Research into plant-mediated indirect interactions between arbuscular mycorrhizal (AM) fungi and insect herbivores has focussed on those between plant shoots and above-ground herbivores, despite the fact that only below-ground herbivores share the same part of the host plant as AM fungi. Using Plantago lanceolata L., we aimed to characterise how early root herbivory by the vine weevil (Otiorhynchus sulcatus F.) affected subsequent colonization by AM fungi (Glomus spp.) and determine how the two affected plant growth and defensive chemistry. We exposed four week old P. lanceolata to root herbivory and AM fungi using a 2×2 factorial design (and quantified subsequent effects on plant biomass and iridoid glycosides (IGs) concentrations. Otiorhynchus sulcatus reduced root growth by c. 64%, whereas plant growth was unaffected by AM fungi. Root herbivory reduced extent of AM fungal colonization (by c. 61%). O. sulcatus did not influence overall IG concentrations, but caused qualitative shifts in root and shoot IGs, specifically increasing the proportion of the more toxic catalpol. These changes may reflect defensive allocation in the plant against further attack. This study demonstrates that very early root herbivory during plant development can shape future patterns of AM fungal colonization and influence defensive allocation in the plant.     

Interactions between aboveground herbivores and the mycorrhizal mutualists of plants

Plant growth, reproduction and survival can be affected both by mycorrhizal fungi and aboveground herbivores, but few studies have examined the interactive effects of these factors on plants. Most of the available data suggest that severe herbivory reduces root colonization by vesicular-arbuscular and ectomycorrhizal fungi. However, the reverse interaction has also been documented - mycorrhizal fungi deter herbivores and interact with fungal endophytes to influence herbivory. Although consistent patterns and mechanistic explanations are yet to emerge, it is likely that aboveground herbivore-mycorrhiza interactions have important implications for plant populations and communities.     

Resource allocation in an annual herb: Effects of light,mycorrhizal fungi,and defoliation

Concurrent interactions and the availability of resources (e.g., light) affect the cost/benefit balance during mutualistic and antagonistic interactions, as well as plant resource allocation patterns. Mycorrhizal interactions and herbivory concur in most plants, where mycorrhizae can enhance the uptake of soil nutrients by plants as well as consuming a large fraction of the plant's carbon, and defoliation usually reduces light interception and photosynthesis, thereby causing direct losses to the hosts of mycorrhizal fungi. Both types of interactions affect the carbon budget of their host plants and thus we predict that the relative costs of herbivory and mycorrhizal colonization will increase when photosynthesis is reduced, for instance in light limited environments. We conducted a greenhouse experiment using Datura stramonium to investigate the effects of defoliation and mycorrhizal inoculation on the resource allocation patterns in two different light environments. Defoliated plants overcompensated in terms of leaf mass in both light environments, but total seed mass per fruit was negatively affected by defoliation in both light environments. Mycorrhizal inoculation had a positive effect on vegetative growth and the leaf nitrogen content, but defoliation negates the benefit of mycorrhizal interactions in terms of the leaf nitrogen content. In general, D. stramonium compensated for the relative costs of concurrent mycorrhizal interactions and defoliation; plants that lacked both interactions exhibited the same performance as plants with both types of interactions.     

菌根真菌与植物共生营养交换机制研究进展

菌根是陆地生态系统普遍存在的、由土壤中的菌根真菌侵染宿主植物根系形成的联合共生体.菌根的建立是以共生体双方的营养交换为基础的:菌根真菌从土壤中吸收氮、磷等营养物质并转运给宿主植物,供其生长;作为交换,植物则以脂质或糖的形式向菌根真菌提供其生长所必需的碳水化合物.近年来,菌根真菌与宿主植物间的营养交换机制一直是研究的热点,国内外对菌根真菌介导的植物营养物质吸收和转运机制的研究也取得了巨大进展.本文综述了丛枝和外生两种菌根真菌与宿主植物间营养交换的最新研究进展,尤其是碳、氮、磷等几种重要营养物质的吸收与双向转运机制,以及营养交换在菌根形成中的潜在调控作用,并对目前存在的关键问题和未来研究方向进行了分析和展望,这对菌根模型的建立及菌根效益的优化具有重要意义.     

Phosphorus and Nitrogen Regulate Arbuscular Mycorrhizal Symbiosis in Petunia hybrida

Phosphorus and nitrogen are essential nutrient elements that are needed by plants in large amounts. The arbuscular mycorrhizal symbiosis between plants and soil fungi improves phosphorus and nitrogen acquisition under limiting conditions. On the other hand, these nutrients influence root colonization by mycorrhizal fungi and symbiotic functioning. This represents a feedback mechanism that allows plants to control the fungal symbiont depending on nutrient requirements and supply. Elevated phosphorus supply has previously been shown to exert strong inhibition of arbuscular mycorrhizal development. Here, we address to what extent inhibition by phosphorus is influenced by other nutritional pathways in the interaction between Petunia hybrida and R. irregularis. We show that phosphorus and nitrogen are the major nutritional determinants of the interaction. Interestingly, the symbiosis-promoting effect of nitrogen starvation dominantly overruled the suppressive effect of high phosphorus nutrition onto arbuscular mycorrhiza, suggesting that plants promote the symbiosis as long as they are limited by one of the two major nutrients. Our results also show that in a given pair of symbiotic partners (Petunia hybrida and R. irregularis), the entire range from mutually symbiotic to parasitic can be observed depending on the nutritional conditions. Taken together, these results reveal complex nutritional feedback mechanisms in the control of root colonization by arbuscular mycorrhizal fungi.     

Fertilization and forb:graminoid ratio affect arbuscular mycorrhiza in seedlings but not adult plants of Plantago lanceolata

Aims

Nutrients play a key role in arbuscular mycorrhizal (AM) symbiosis. We quantified the response of AM symbiosis of seedlings and adult plants of Plantago lanceolata to fertilization under field conditions in managed grasslands differing in nutrient availability and soil moisture.

Methods

The AM symbiosis was measured as the total extent of AM fungal colonization and frequency of arbuscules or vesicles, and as the relative proportions of morphotypes. We further examined the effects of the surrounding vegetation upon AM symbiosis.

Results

Fertilization decreased total AM colonization and relative arbuscular frequency of the whole mycorrhizal community and of Acaulospora and “fine endophyte” morphotypes in seedling roots, but it had no effect upon the mycorrhiza in adult plants. The decline in arbuscular frequency in seedling roots due to fertilization was greater at the sites with higher nutrient availability and lower N:P ratio. Seedlings surrounded by more forbs had a greater total AM colonization and higher vesicular frequency.

Conclusions

Increased nutrient availability in the initial stages of seedling development has a prominent effect upon AM symbiosis development, but these effects seem to diminish over the long term, as evidenced by the results obtained for adult plants and from the limited effects of parameters characterizing long-term nutrient availability.     

Tracking plant preference for higher‐quality mycorrhizal symbionts under varying CO2 conditions over multiple generations

The symbiosis between plants and root‐colonizing arbuscular mycorrhizal (AM) fungi is one of the most ecologically important examples of interspecific cooperation in the world. AM fungi provide benefits to plants; in return plants allocate carbon resources to fungi, preferentially allocating more resources to higher‐quality fungi. However, preferential allocations from plants to symbionts may vary with environmental context, particularly when resource availability affects the relative value of symbiotic services. We ask how differences in atmospheric CO₂‐levels influence root colonization dynamics between AMF species that differ in their quality as symbiotic partners. We find that with increasing CO₂‐conditions and over multiple plant generations, the more beneficial fungal species is able to achieve a relatively higher abundance. This suggests that increasing atmospheric carbon supply enables plants to more effectively allocate carbon to higher‐quality mutualists, and over time helps reduce lower‐quality AM abundance. Our results illustrate how environmental context may affect the extent to which organisms structure interactions with their mutualistic partners and have potential implications for mutualism stability and persistence under global change.     

Plant hormones as signals in arbuscular mycorrhizal symbiosis

Abstract

Arbuscular mycorrhizal (AM) fungi are non-specific symbionts developing mutual and beneficial symbiosis with most terrestrial plants. Because of the obligatory nature of the symbiosis, the presence of the host plant during the onset and proceeding of symbiosis is necessary. However, AM fungal spores are able to germinate in the absence of the host plant. The fungi detect the presence of the host plant through some signal communications. Among the signal molecules, which can affect mycorrhizal symbiosis are plant hormones, which may positively or adversely affect the symbiosis. In this review article, some of the most recent findings regarding the signaling effects of plant hormones, on mycorrhizal fungal symbiosis are reviewed. This may be useful for the production of plants, which are more responsive to mycorrhizal symbiosis under stress.     

AM fungal communities inhabiting the roots of submerged aquatic plant <Emphasis Type="Italic">Lobelia dortmanna</Emphasis> are diverse and include a high proportion of novel taxa

While the arbuscular mycorrhizal (AM) symbiosis is known to be widespread in terrestrial ecosystems, there is growing evidence that aquatic plants also form the symbiosis. It has been suggested that symbiosis with AM fungi may represent an important adaptation for isoëtid plants growing on nutrient-poor sediments in oligotrophic lakes. In this study, we address AM fungal root colonization intensity, richness and community composition (based on small subunit (SSU) ribosomal RNA (rRNA) gene sequencing) in five populations of the isoëtid plant species Lobelia dortmanna inhabiting oligotrophic lakes in Southern Sweden. We found that the roots of L. dortmanna hosted rich AM fungal communities and about 15 % of the detected molecular taxa were previously unrecorded. AM fungal root colonization intensity and taxon richness varied along an environmental gradient, being higher in oligotrophic and lower in mesotrophic lakes. The overall phylogenetic structure of this aquatic fungal community differed from that described in terrestrial systems: The roots of L. dortmanna hosted more Archaeosporaceae and fewer Glomeraceae taxa than would be expected based on global data from terrestrial AM fungal communities.     

Above-ground herbivory causes rapid and sustained changes in mycorrhizal colonization of grasses

Arbuscular mycorrhizal fungi (AMF) play a vital role in ecosystem functioning. In most grasslands, herbivory by both vertebrate and invertebrate herbivores is common and thus in order to assess herbivore effects on multitrophic-level interactions both should be considered. This study investigated the effects of grazing by rabbit and insect herbivores on root-colonization of grasses by AMF in two lowland grasslands in southern England, UK. A long-term exclosure site was used to provide a temporal assessment in order to elucidate whether any short-term responses to herbivore removal were sustained. Root samples from three grass species at each site were analysed in terms of total mycorrhizal colonization and proportional colonization by individual mycorrhizal structures. Colonization levels were up to 1.6 times greater under moderate levels of rabbit grazing (with summer maxima of 25% and winter minima of 11%) than in intensely grazed swards or fenced plots at both sites. The change was fast (within 8 weeks), consistent throughout the sampled field plots, and temporally sustainable over a 19-year period. There was no significant effect of insect herbivory on total colonization but proportional colonization by different AM structures was affected on some sample dates where vertebrate herbivores had been removed, indicating a slight effect on fungal structure allocation. The results suggest that the type of herbivore and perhaps more importantly the intensity of grazing are key determinants of below-ground effects upon mycorrhizal–host plant symbiosis. The data suggest that the extent of mycorrhizal colonization within grass host plants is strongly influenced by C assimilation and allocation.