Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis

A number of studies have shown that an association with mycorrhizal fungi can alter the outcome of interactions between plants and their enemies. While the directions of these effects vary, their strength suggests the need for greater attention to multispecies interactions among plant enemies, plants, and mycorrhizal fungi. We recognize that mycorrhizal fungi could effect plant enemies by improving plant nutrition, modifying plant tolerance, or modifying plant defenses. In addition, mycorrhizal fungi could directly interfere with pathogen infection, herbivory, or parasitism by occupying root space. We formalize these alternative outcomes of multispecies interactions and explore the long-term dynamics of the plant-enemy interactions based on these different scenarios using a general model of interactions between plants and plant enemies. We then review the literature in terms of the assumptions of the alternative mechanisms and the predictions of these models. Through this effort, we identify new directions in the study of tritrophic interactions between enemies, plants, and soil mutualists.     

Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit

A basic tenet of ecology is that negative feedback on abundance plays an important part in the coexistence of species within guilds. Mutualistic interactions generate positive feedbacks on abundance and therefore are not thought to contribute to the maintenance of diversity. Here, I report evidence of negative feedback on plant growth through changes in the composition of their mutualistic fungal symbionts, arbuscular mycorrhizal (AM) fungi. Negative feedback results from asymmetries in the delivery of benefit between plant and AM fungal species in which the AM fungus that grows best with the plant Plantago lanceolata is a poor growth promoter for Plantago. Growth of Plantago is, instead, best promoted by the AM fungal species that accumulate with a second plant species, Panicum sphaerocarpon. The resulting community dynamic leads to a decline in mutualistic benefit received by Plantago, and can contribute to the coexistence of these two competing plant species.     

Population Interactions and the Determinants of Population Size

Abstract The flux of individuals within populations is dependent upon six controlling processes: the intrinsic rate of increase of the plant, intraspecific competition for resources, interspecific competition, natural enemies, mutualisms and refuge effects such as the immigration of seeds from other populations. Although population interactions are generally believed to play a major role in determining the flux of individuals within populations, little attempt has been made to quantify the strength of these interactions and their role in the dynamics of populations. In this paper we examine the role of competition, herbivory and mutualistic interactions in determining the dynamics of a range of annual plant species. Firstly, it is shown that the dynamics of three weed species ( Bromus sterilis, Galium aparine, Papaver rhoeas ) in an experimental community in an arable cropping system of winter wheat are determined primarily by the rapid population growth of B. sterilis . Interactions between the species play a minor part in the dynamics of the system. Secondly, it is shown that current levels of grazing by overwintering populations of brent geese have a minor impact on the abundance of Salicornia europaea , but that increased grazing has the potential to reduce abundance and increase the instability of S. europaea populations. This is a consequence of the aggregative response of the geese, which results in an increasing proportion of the seeds of S. europaea being eaten as plant density increases. Thirdly, it is shown that there is a complex interaction between root pathogenic and arbuscular mycorrhizal fungi in natural field populations of Vulpia ciliata and that the benefit of mycorrhizal fungi to the plant is in providing protection against pathogens.     

Interactions between functionally diverse fungal mutualists inconsistently affect plant performance and competition

Plants form mutualistic relationship with a variety of belowground fungal species. Such a mutualistic relationship can enhance plant growth and resistance to pathogens. Yet, we know little about how interactions between functionally diverse groups of fungal mutualists affect plant performance and competition. We experimentally determined the effects of interaction between two functional groups of belowground fungi that form mutualistic relationship with plants, arbuscular mycorrhizal (AM) fungi and Trichoderma, on interspecific competition between pairs of closely related plant species from four different genera. We hypothesized that the combination of two functionally diverse belowground fungal species would allow plants and fungi to partition their symbiotic relationships and relax plant–plant competition. Our results show that: 1) the AM fungal species consistently outcompeted the Trichoderma species independent of plant combinations; 2) the fungal species generally had limited effects on competitive interactions between plants; 3) however, the combination of fungal species relaxed interspecific competition in one of the four instances of plant–plant competition, despite the general competitive superiority of AM fungi over Trichoderma. We highlight that the competitive outcome between functionally diverse fungal species may show high consistency across a broad range of host plants and their combinations. However, despite this consistent competitive hierarchy, the consequences of their interaction for plant performance and competition can strongly vary among plant communities.     

Potential impacts of multiple partners on mycorrhizal community dynamics

The significance of arbuscular mycorrhizal (AM) fungi in terrestrial ecosystems is widely acknowledged, but the causes and consequences of diversity in these fungi are not well understood. A recent frequency-dependent model suggests that dynamics within mycorrhizal mutualisms could promote the coexistence of at least two competing plant species and two competing fungal species within a community. Models are developed here in which simultaneous association with multiple partners may result in elevated or depressed fitness relative to association with either partner alone. This increases the range of conditions under which negative feedback occurs and coexistence of all four species is possible. Differences between plants in the relative proportions of fungi at which maximum fitness occurs may facilitate coexistence, as may differences between fungi in their abilities to establish interplant connections. These models suggest additional mechanisms by which mutualistic interactions could promote local diversity of plants and AM fungi.     

Breakdown and delayed cospeciation in the arbuscular mycorrhizal mutualism

The ancient arbuscular mycorrhizal association between the vast majority of plants and the fungal phylum Glomeromycota is a dominant nutritional mutualism worldwide. In the mycorrhizal mutualism, plants exchange photosynthesized carbohydrates for mineral nutrients acquired by fungi from the soil. This widespread cooperative arrangement is broken by 'cheater' plant species that lack the ability to photosynthesize and thus become dependent upon three-partite linkages (cheater-fungus-photosynthetic plant). Using the first fine-level coevolutionary analysis of mycorrhizas, we show that extreme fidelity towards fungi has led cheater plants to lengthy evolutionary codiversification. Remarkably, the plants' evolutionary history closely mirrors that of their considerably older mycorrhizal fungi. This demonstrates that one of the most diffuse mutualistic networks is vulnerable to the emergence, persistence and speciation of highly specific cheaters.     

Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes

Most organisms engage in beneficial interactions with other species; however, little is known regarding how individuals balance the competing demands of multiple mutualisms. Here we examine three-way interactions among a widespread grass, Schedonorus phoenix , a protective fungal endophyte aboveground, Neotyphodium coenophialum , and nutritional symbionts (arbuscular mycorrhizal fungi) belowground. In a greenhouse experiment, we manipulated the presence/absence of both fungi and applied a fertilizer treatment to individual plants. Endophyte presence in host plants strongly reduced mycorrhizal colonization of roots. Additionally, for plants with the endophyte, the density of endophyte hyphae was negatively correlated with mycorrhizal colonization, suggesting a novel role for endophyte abundance in the interaction between the symbionts. Endophyte presence increased plant biomass, and there was a positive correlation between endophyte hyphal density and plant biomass. The effects of mutualists were asymmetric: mycorrhizal fungi treatments had no significant impact on the endophyte and negligible effects on plant biomass. Fertilization affected all three species – increasing plant biomass and endophyte density, but diminishing mycorrhizal colonization. Mechanisms driving negative effects of endophytes on mycorrhizae may include inhibition via endophyte alkaloids, altered nutritional requirements of the host plant, and/or temporal and spatial priority effects in the interactions among plants and multiple symbionts.     

Plant-plant interactions vary with different mycorrhizal fungus species

Because different species of mycorrhizal fungi have different effects on the growth of particular plant species, variation in mycorrhizal fungus species composition could cause changes in the strength of plant-plant interactions. Results are presented from a growth chamber experiment that compared the strength of interactions among seedlings of ponderosa pine (Pinus ponderosa) when the pines were colonized by two different groups of ectomycorrhizal fungi in the genus Rhizopogon. Plant density effects differed between the two groups of mycorrhizal fungi: plant growth was low regardless of density when plants were colonized with pine-specific Rhizopogon species, while plant growth declined with plant density when plants were colonized by Rhizopogon species having a broader host range. This result parallels results from previous studies showing that plant interactions are more antagonistic with mycorrhizal fungi than without, implying that plant responsiveness to beneficial mycorrhizal fungi declines with increasing plant density. If such effects are prevalent in plant communities, then variation in mycorrhizal fungus community composition is predicted to have a density-dependent effect on plants.     

Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack

The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid‐free plants but only when they are connected to aphid‐infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.     

Sharing of Diverse Mycorrhizal and Root-Endophytic Fungi among Plant Species in an Oak-Dominated Cool–Temperate Forest

Most terrestrial plants interact with diverse clades of mycorrhizal and root-endophytic fungi in their roots. Through belowground plant–fungal interactions, dominant plants can benefit by interacting with host-specific mutualistic fungi and proliferate in a community based on positive plant–mutualistic fungal feedback. On the other hand, subordinate plant species may persist in the community by sharing other sets (functional groups) of fungal symbionts with each other. Therefore, revealing how diverse clades of root-associated fungi are differentially hosted by dominant and subordinate plant species is essential for understanding plant community structure and dynamics. Based on 454-pyrosequencing, we determined the community composition of root-associated fungi on 36 co-occurring plant species in an oak-dominated forest in northern Japan and statistically evaluated the host preference phenotypes of diverse mycorrhizal and root-endophytic fungi. An analysis of 278 fungal taxa indicated that an ectomycorrhizal basidiomycete fungus in the genus Lactarius and a possibly endophytic ascomycete fungus in the order Helotiales significantly favored the dominant oak (Quercus) species. In contrast, arbuscular mycorrhizal fungi were generally shared among subordinate plant species. Although fungi with host preferences contributed to the compartmentalization of belowground plant–fungal associations, diverse clades of ectomycorrhizal fungi and possible root endophytes were associated not only with the dominant Quercus but also with the remaining plant species. Our findings suggest that dominant-ectomycorrhizal and subordinate plant species can host different subsets of root-associated fungi, and diverse clades of generalist fungi can counterbalance the compartmentalization of plant–fungal associations. Such insights into the overall structure of belowground plant–fungal associations will help us understand the mechanisms that facilitate the coexistence of plant species in natural communities.     

Symbiosis between grasses and asexual fungal endophytes

The symbiosis between vertically transmitted asexual endophytic fungi and grasses is common and generally considered to be mutualistic. Recent studies have accumulated evidence of negative effects of endophytes on plant fitness, prompting a debate on the true nature of the symbiosis. Genetic factors in each of the two partners show high variability and have a range of effects (from positive to negative) on plant fitness. In addition, interacting environmental factors might modify the nature of the symbiosis. Finally, competition and multitrophic interactions among grass consumers are influenced by endophytes, and the effects of plant neighbours or consumers could feedback to affect plant fitness. We propose a mutualism-parasitism continuum for the symbiosis between asexual endophytes and grasses, which is similar to the associations between plants and mycorrhizal fungi.     

菌根真菌在生态系统中的作用

 菌根是一种植物营养根与土壤真菌形成的共生体,在自然界中分布广泛。本文着重从以下几个方面介绍相关的研究进展：1) 菌根真菌作为生态系统的重要组成部分,具有不可忽视的生物量,并成为连接绿色植物和食真菌者食物链的重要一环;2) 菌根真菌通过参与凋落物的酶降解过程影响有机物的循环,通过促进生物固氮、加速土壤磷的风化、提高土壤溶液离子的有效性以及直接吸收等过程影响氮、磷、钾、钙、镁等元素的无机循环;3) 菌根真菌与土壤微生物间存在有益的或拮抗的相互作用,并可以直接或间接地影响根际生物区系的组成和数量;菌根真菌通过对宿主植物的有益作用而影响植物的种间竞争,通过菌根网络而形成的种团可以在同种或不同种植物间实现资源的重新分配和共享;由于对种间关系的作用和对食物链的影响,菌根真菌对群落的物种构成和多样性的维持具有重要的作用;菌根真菌是群落演替过程的指示者,也是这一过程的参与者和推动者,并且菌根真菌的存在也有利于提高土壤团聚体的稳定性及促进灰壤的形成;4) 菌根真菌的种类和数量可以指示生态系统中自然的或人类活动引起的变化,并可以在生态系统的保护、恢复或重建过程中发挥重要作用。文章的最后还介绍了最新的研究热点和发展趋势。     

Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant–herbivore interaction

1. While both arbuscular mycorrhizal (AM) fungi and plant and insect genotype are well known to influence plant and herbivore growth and performance, information is lacking on how these factors jointly influence the relationship between plants and their natural herbivores. 2. The aim of the present study was to investigate how a natural community of arbuscular mycorrhizal fungi affects the growth of the perennial herb Plantago lanceolata L. (Plantaginaceae), as well as its interaction with the Glanville fritillary butterfly [Melitaea cinxia L. (Nymphalidae)]. For this, a multifactorial experiment was conducted using plant lines originating from multiple plant populations in the Åland Islands, Finland, grown either with or without mycorrhizal fungi. For a subset of plant lines, the impact of mycorrhizal inoculation, plant line, and larval family on the performance of M. cinxia larvae were tested. 3. Arbuscular mycorrhizal inoculation did not have a consistently positive or negative impact on plant growth or herbivore performance. Instead, plant genetic variation mediated the impact of arbuscular mycorrhizal fungi on plant growth, and both plant genetic variation and herbivore genetic variation mediated the response of the herbivore. For both the plant and insect, the impact of the arbuscular mycorrhizal community ranged from mutualistic to antagonistic. Overall, the present findings illustrate that genetic variation in response to mycorrhizal fungi may play a key role in the ecology and evolution of plant–insect interactions.     

Effects of mycorrhizal fungi on plant populations

We discuss four potentially important interactions between mycorrhizal fungi and populations of plants. First, vesicular-arbuscular mycorrhizal colonization has been shown to increase reproduction (via both male and female functions) and offspring survival, and thus it can increase population size, at least in the short term. This is undoubtedly important to wild plant species and especially to those whose success depends on high rates of reproduction such as early successional annuals. Second, the positive response in growth and reproduction to vesicular-arbuscular mycorrhizal colonization may be inversely related to plant population density. All else being equal, this would tend to stabilize the density of natural plant populations over time. It may also explain why positive responses to mycorrhizal inoculation of dense crops are rare. Third, vesicular-arbuscular mycorrhizal fungi can increase inequality in size and reproduction among plants within a population. Mycorrhizal fungi may thus exaggerate the genetic overrepresentation in the next generation of the most robust individuals in the current generation. Fourth, established mycorrhizal plants may serve as important sources of inoculum for initially nonmycorrhizal, conspecific seedlings. This may affect regeneration, and could contribute to patchy distributions of species within the community.     

Preference,specificity and cheating in the arbuscular mycorrhizal symbiosis

Arbuscular mycorrhizal symbioses are mutualistic interactions between fungi and most plants. There is considerable interest in this symbiosis because of the strong nutritional benefits conferred to plants and its influence on plant diversity. Until recently, the symbiosis was assumed to be unspecific. However, two studies have now revealed that although it can be largely unspecific with the fungal community composition changing seasonally, in certain ecosystems it can also be highly specific and might potentially allow plants to cheat the arbuscular mycorrhizal network that connects plants below ground.     

Anatomical relations among endophytic holoparasitic angiosperms, autotrophic host plants and mycorrhizal fungi: A novel tripartite interaction

Mycorrhizae are widespread mutualistic symbioses crucial for the functioning of terrestrial ecosystems. Not all plants associate with mycorrhizae; most parasitic plants have been suggested to be nonmycorrhizal because they have developed alternative strategies to obtain nutrients. In endophytic parasitic plants, whose vegetative bodies grow completely inside their mycorrhizal host roots, the opportunity for establishing a tripartite association seems evident, but information on these systems is lacking. In studying natural associations among the endophytic holoparasite Cytinus hypocistis, their Cistaceae host species, and associated mycorrhizal fungi, we found that mycorrhizae were associated with the hosts and the parasites, reaching high frequencies of colonization. In parasitic and host root tissues, mycorrhizal fungi spread in the parenchymatic cells by intracellular growth and formed hyphal coils and vesicles, while the cambium and the vascular tissues were never colonized. This report is the first on a tripartite association of an endophytic parasitic plant, its host, and mycorrhizae in natural conditions, representing a novel trophic interaction not previously reported within the angiosperms. Additional studies on the interactions occurring among these three players are needed because they may be crucial to our understanding of how this mutualistic-antagonistic system is functioning and evolving.     

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.     

Developing X-ray Computed Tomography to non-invasively image 3-D root systems architecture in soil

Background

The positive relationship between biodiversity and ecosystem functioning (BEF) is due mainly to complementarity between species. Most BEF studies primarily focused on plant interactions; however, plants are embedded in a dense network of multitrophic interactions above and below the ground, which are likely to play a crucial role in BEF relationships.

Scope

In the present review I point out the relevance of aboveground–belowground interactions as a source of complementarity effects in grassland biodiversity experiments. A review of the current knowledge on the role of decomposers, arbuscular mycorrhizal fungi, rhizobia, plant growth promoting rhizobacteria, invertebrate ecosystem engineers, herbivores, pathogens and predators in biodiversity experiments, indicates that soil biota can drive both positive and negative complementarity between plant species via a multitude of mechanisms.

Conclusions

I pose four main processes by which aboveground–belowground interactions determine positive complementarity effects: enlarging biotope space, mediating legume effects, increasing plant community resistance, and maintaining plant diversity. By contrast, soil biota may also reinforce negative complementarity effects by competing with plants for nutrients or by exerting herbivore or pathogen pressure, thereby reducing community productivity. Thus, considering aboveground–belowground interactions as well as interactions between antagonistic and mutualistic consumers may improve the mechanistic understanding of complementarity effects in plant diversity–ecosystem functioning experiments and should inspire future research.     

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.     

Specificity of assemblage,not fungal partner species,explains mycorrhizal partnerships of mycoheterotrophic Burmannia plants

Mycoheterotrophic plants (MHPs) growing on arbuscular mycorrhizal fungi (AMF) usually maintain specialized mycorrhizal associations. The level of specificity varies between MHPs, although it remains largely unknown whether interactions with mycorrhizal fungi differ by plant lineage, species, and/or by population. Here, we investigate the mycorrhizal interactions among Burmannia species (Burmanniaceae) with different trophic modes using high-throughput DNA sequencing. We characterized the inter- and intraspecific dynamics of the fungal communities by assessing the composition and diversity of fungi among sites. We found that fully mycoheterotrophic species are more specialized in their fungal associations than chlorophyllous species, and that this specialization possibly results from the gradual loss of some fungal groups. In particular, although many fungal species were shared by different Burmannia species, fully MHP species typically host species-specific fungal assemblages, suggesting that they have a preference for the selected fungi. Although no apparent cophylogenetic relationship was detected between fungi and plants, we observe that evolutionarily closely related plants tend to have a greater proportion of shared or closely related fungal partners. Our findings suggest a host preference and specialization toward fungal assemblages in Burmannia, improving understanding of interactions between MHPs and fungi.Subject terms: Fungi, Plant sciences, Evolution