Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field

Although arbuscular mycorrhizal (AM) fungi are ubiquitous symbionts of plants, the mutualism has rarely been tested in nature. In experiments designed to explore the ecological relevance of associations between different fungal and plant species in a natural environment, plant species were infected with different species of fungi and grown in separate trials in the laboratory and a North Carolina (USA) field. The benefits to plants varied dramatically as plant species were grown with different species of AM fungi. Effects of mycorrhizal fungi in nature were generally correlated to effects in the growth chamber, suggesting that laboratory data do reflect dynamics between plants and AM fungi in the field. Initial size at transplant and experimental block were also significant predictors of plant growth in the field. Correlation statistics between laboratory and field data were weaker when analyses involved plant species less responsive to infection by any AM fungus, suggesting that the response of a species to inoculation is a good predictor of its sensitivity to specific AM fungi in the field. AM fungal identity appears to influence the growth and reproduction of plants in the field.     

丛枝菌根在植物修复重金属污染土壤中的作用

丛枝菌根（Arbuscular mycorrhizae,AM）是自然界中分布最广的一类菌根,AM真菌能与陆地上绝大多数的高等植物共生,常见于包括重金属污染土壤在内的各种生境中。在重金属污染条件下,AM真菌可以减轻重金属对植物的毒害,影响植物对重金属的吸收和转运,在重金属污染土壤的植物修复中显示出极大的应用潜力。重点介绍了AM真菌对植物重金属耐性的影响及其在植物提取和植物稳定中的应用等方面的进展,讨论了未来研究所面临的任务和挑战。     

Low congruence between the diversity of Waxcap (Hygrocybe spp.) fungi and vascular plants in semi-natural grasslands

The diversity of fungi in semi-natural grasslands is poorly known, partly due to difficulties in species identification in the field but also because there are few specialists available. Diversity assessments of grassland fungi would be facilitated if a potential surrogate group for fungal diversity could be identified. The aim of this study was to assess whether plant diversity patterns in semi-natural grasslands are congruent with diversity patterns of Waxcap (Hygrocybe spp.) fungi. Waxcaps, together with several other groups of fungi (e.g. the genera Entoloma, Dermoloma, Camarophyllopsis, and the families Clavariaceae and Geoglossaceae) have habitat requirements similar to many plants typical for semi-natural grasslands and they are all threatened by ceased management and nutrient enrichment. Diversity data from 31 semi-natural grasslands in southern Sweden were used to examine if there is congruence in species richness, nestedness, β-diversity and species composition between plants and Hygrocybe fungi. Species richness of Hygrocybe was significantly positively correlated with plant richness, although the relationship was not strong (r²=0.14). Both plant and Hygrocybe species composition was significantly nested, i.e. species-poor sites contain a subset of species from species-rich sites, which suggests that rare species mostly occur in the species-rich sites. A species similarity analysis between the grassland sites showed that there is low overlap between species composition of plants and Hygrocybe, indicating that conservation decisions based solely on plants may not fulfil the requirements of the Hygrocybe species. The conclusion is that there is low congruence between plant and Hygrocybe species diversity, making plants a poor surrogate group for Hygrocybe fungi, and probably also for other grassland fungi.     

Interactions among mutualism,competition, and predation foster species coexistence in diverse communities

In natural systems, organisms are simultaneously engaged in mutualistic, competitive, and predatory interactions. Theory predicts that species persistence and community stability are feasible when the beneficial effects of mutualisms are balanced by density-dependent negative feedbacks. Enemy-mediated negative feedbacks can foster plant species coexistence in diverse communities, but empirical evidence remains mixed. Disparity between theoretical expectations and empirical results may arise from the effects of mutualistic mycorrhizal fungi. Here, we build a multiprey species/predator model combined with a bidirectional resource exchange system, which simulates mutualistic interactions between plants and fungi. To reach population persistence, (1) the per capita rate of increase of all plant population must exceed the sum of the negative per capita effects of predation, interspecific competition, and costs of mycorrhizal association, and (2) the per capita numerical response of enemies to mycorrhizal plants must exceed the magnitude of the per capita enemy rate of mortality. These conditions reflect the balance between regulation and facilitation in the system. Interactions between plant natural enemies and mycorrhizal fungi lead to shifts in the strength and direction of net mycorrhizal effects on plants over time, with common plant species deriving greater benefits from mycorrhizal associations than rare plant species.     

Effects of the soil microbiome on the demography of two annual prairie plants

1. Both mutualistic and pathogenic soil microbes are known to play important roles in shaping the fitness of plants, likely affecting plants at different life cycle stages.
2. In order to investigate the differential effects of native soil mutualists and pathogens on plant fitness, we compared survival and reproduction of two annual tallgrass prairie plant species (Chamaecrista fasciculata and Coreopsis tinctoria) in a field study using 3 soil inocula treatments containing different compositions of microbes. The soil inocula types included fresh native whole soil taken from a remnant prairie containing both native mutualists and pathogens, soil enhanced with arbuscular mycorrhizal (AM) fungi derived from remnant prairies, and uninoculated controls.
3. For both species, plants inoculated with native prairie AM fungi performed much better than those in uninoculated soil for all parts of the life cycle. Plants in the native whole prairie soil were either generally similar to plants in the uninoculated soil or had slightly higher survival or reproduction.
4. Overall, these results suggest that native prairie AM fungi can have important positive effects on the fitness of early successional plants. As inclusion of prairie AM fungi and pathogens decreased plant fitness relative to prairie AM fungi alone, we expect that native pathogens also can have large effects on fitness of these annuals. Our findings support the use of AM fungi to enhance plant establishment in prairie restorations.

     

Sympatry and interference of divergent Microbotryum pathogen species

The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther‐smut disease, caused by fungi in the genus Microbotryum, among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co‐occurrence of distinct, host‐specific anther‐smut fungi, rather than localized cross‐species disease transmission. Flowers from sympatric populations showed that the Microbotryum spores were frequently moved between host species. Experimental inoculations to simulate cross‐species exposure to the pathogens in these plant communities showed that the anther‐smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi‐host/multi‐pathogen communities are common in this system and they involve a previously hidden mechanism of interference between Microbotryum fungi, which likely affects both pathogen and host distributions.     

Paleomedicine and the use of plant secondary compounds in the Paleolithic and Early Neolithic

Reconstructing plant use before domestication is challenging due to a lack of evidence. Yet, on the small number of sites with assemblages, the wide range of different plant species cannot be explained simply in terms of nutrition. Assemblages from the Lower Paleolithic to the Early Neolithic were examined to investigate the relative edible and medicinal properties of the plants. The assemblages contain a mixture of edible species, plants that are both edible and medicinal, and plants with only medicinal properties. The proportion of medicinal plants at all sites is well above the natural average and increases over time. Mechanisms for preventing intestinal parasitic infections are common among animals and together with chimpanzees’ preventative and curative self‐medication practices suggest an evolutionary context for this behavior. A broad‐spectrum approach to plant collection is likely to have been in place throughout the Paleolithic driven, in part, by the need for medicinal compounds.     

Adaptation of plant‐mycorrhizal interactions to moisture availability in prairie restoration

The strength and direction of plant response to inoculation with arbuscular mycorrhizal fungi (AM fungi) is dependent on both abiotic and biotic contexts, often generating patterns of AM fungal mediation of plant adaptation. However, knowledge of plant‐community level effects of these interactions in grassland restoration is limited. We conducted a field inoculation experiment by inoculating five plant species native to a drier prairie and five plant species native to a moister prairie with mycorrhizal fungal communities from each prairie type. Species were paired by genus or family to account for phylogenetic effects. The inoculated plants were transplanted to study plots seeded with a restoration seed mix. Plots were manipulated to create either moister or drier conditions similar to environments of the plant species and mycorrhizal communities. In both transplanted and seeded plant species, we found that only drier prairie‐range species benefited from moisture‐regime matched AM fungal inoculum. Other seeded prairie plant species demonstrated a negative response to inoculation, likely due to the earlier successional stage of these species. Additionally, nonseeded plants benefited from inoculation in different ways: native nonseeded plants had highest cover with drier prairie inoculum in drier conditions, while nonnative plants had highest cover with moister prairie‐origin inoculum. These results suggest that use of local AM fungi may be particularly important in restorations at drier sites, even at relatively small differences in moisture availability. Further, specific knowledge of relative responsiveness of seeded plant species and nonseeded plant species to AM fungal inoculation will be useful in planning restorations.     

Plant invasions--the role of mutualisms

Many introduced plant species rely on mutualisms in their new habitats to overcome barriers to establishment and to become naturalized and, in some cases, invasive. Mutualisms involving animal-mediated pollination and seed dispersal, and symbioses between plant roots and microbiota often facilitate invasions. The spread of many alien plants, particularly woody ones, depends on pollinator mutualisms. Most alien plants are well served by generalist pollinators (insects and birds), and pollinator limitation does not appear to be a major barrier for the spread of introduced plants (special conditions relating to Ficus and orchids are described). Seeds of many of the most notorious plant invaders are dispersed by animals, mainly birds and mammals. Our review supports the view that tightly coevolved, plant-vertebrate seed dispersal systems are extremely rare. Vertebrate-dispersed plants are generally not limited reproductively by the lack of dispersers. Most mycorrhizal plants form associations with arbuscular mycorrhizal fungi which, because of their low specificity, do not seem to play a major role in facilitating or hindering plant invasions (except possibly on remote islands such as the Galapagos which are poor in arbuscular mycorrhizal fungi). The lack of symbionts has, however, been a major barrier for many ectomycorrhizal plants, notably for Pinus spp. in parts of the southern hemisphere. The roles of nitrogen-fixing associations between legumes and rhizobia and between actinorhizal plants and Frankia spp. in promoting or hindering invasions have been virtually ignored in the invasions literature. Symbionts required to induce nitrogen fixation in many plants are extremely widespread, but intentional introductions of symbionts have altered the invasibility of many, if not most, systems. Some of the world's worst invasive alien species only invaded after the introduction of symbionts. Mutualisms in the new environment sometimes re-unite the same species that form partnerships in the native range of the plant. Very often, however, different species are involved, emphasizing the diffuse nature of many (most) mutualisms. Mutualisms in new habitats usually duplicate functions or strategies that exist in the natural range of the plant. Occasionally, mutualisms forge totally novel combinations, with profound implications for the behaviour of the introduced plant in the new environment (examples are seed dispersal mutualisms involving wind-dispersed pines and cockatoos in Australia; and mycorrhizal associations involving plant roots and fungi). Many ecosystems are becoming more susceptible to invasion by introduced plants because: (a) they contain an increasing array of potential mutualistic partners (e.g. generalist frugivores and pollinators, mycorrhizal fungi with wide host ranges, rhizobia strains with infectivity across genera); and (b) conditions conductive for the establishment of various alien/alien synergisms are becoming more abundant. Incorporating perspectives on mutualisms in screening protocols will improve (but not perfect) our ability to predict whether a given plant species could invade a particular habitat.     

Cryptic species and host specificity in the ectomycorrhizal genus Strobilomyces (Strobilomycetaceae)

Taxonomical classification of higher fungi remains an important challenge and can benefit from the application of molecular analysis. We propose that the ectomycorrhizal (EM) fungal taxa might include a number of cryptic species because there are few morphological characteristics useful for distinguishing among these fungi. Previously, host specificity in most EM fungi was thought to be low, but we suspect that confusion of cryptic species has led to an underestimate of fungal host specificity. We analyzed both nuclear and mitochondrial DNA sequences from Strobilomyces fungi and obtained evidence that what were previously described as four species can be grouped into 14 distinct lineages, suggesting that these lineages might be distinct biological species. Moreover, we identified host plants for Strobilomyces via nucleotide sequencing of both fungal and plant DNA from EM samples. Most lineages of Strobilomyces tested in this study were associated only with Fagaceae trees, even though Strobilomyces species were previously thought to be generalists with regard to hosts. Thus, we present an approach useful for identifying cryptic species and detecting the true host range of a set of EM fungi in natural conditions.     

How are plant and fungal communities linked to each other in belowground ecosystems? A massively parallel pyrosequencing analysis of the association specificity of root-associated fungi and their host plants

In natural forests, hundreds of fungal species colonize plant roots. The preference or specificity for partners in these symbiotic relationships is a key to understanding how the community structures of root‐associated fungi and their host plants influence each other. In an oak‐dominated forest in Japan, we investigated the root‐associated fungal community based on a pyrosequencing analysis of the roots of 33 plant species. Of the 387 fungal taxa observed, 153 (39.5%) were identified on at least two plant species. Although many mycorrhizal and root‐endophytic fungi are shared between the plant species, the five most common plant species in the community had specificity in their association with fungal taxa. Likewise, fungi displayed remarkable variation in their association specificity for plants even within the same phylogenetic or ecological groups. For example, some fungi in the ectomycorrhizal family Russulaceae were detected almost exclusively on specific oak (Quercus) species, whereas other Russulaceae fungi were found even on “non‐ectomycorrhizal” plants (e.g., Lyonia and Ilex). Putatively endophytic ascomycetes in the orders Helotiales and Chaetothyriales also displayed variation in their association specificity and many of them were shared among plant species as major symbionts. These results suggest that the entire structure of belowground plant–fungal associations is described neither by the random sharing of hosts/symbionts nor by complete compartmentalization by mycorrhizal type. Rather, the colonization of multiple types of mycorrhizal fungi on the same plant species and the prevalence of diverse root‐endophytic fungi may be important features of belowground linkage between plant and fungal communities.     

Iron uptake by plants from microbial siderophores : a study with 7-nitrobenz-2 oxa-1,3-diazole-desferrioxamine as fluorescent ferrioxamine B analog

The synthetically produced fluorescent siderophore NBD-desferrioxamine B (NBD-DFO), an analog of the natural siderophore ferrioxamine B, was used to study iron uptake by plants. Short-term (10-hour) ⁵⁵Fe uptake rates by cotton (Gossypium spp.) and maize (Zea mays L.) plants from the modified siderophore were similar to those of the natural one. In longer-term uptake experiments (3 weeks), both siderophore treatments resulted in similar leaf chlorophyll concentration and dry matter yield. These results suggest that the synthetic derivative acts similarly to the natural siderophore. The NBD-DFO is fluorescent only when unferrated and can thus be used as a probe to follow iron removal from the siderophore. Monitoring of the fluorescence increase in a nutrient solution containing Fe³⁺-NBD-DFO showed that iron uptake by plants occurs at the cell membrane. The rate of iron uptake was significantly lower in both plant species in the presence of antibiotic agent, thus providing evidence for iron uptake by rhizosphere microbes that otherwise could have been attributed to plant uptake. Confocal fluorescence microscopy revealed that iron was taken up from the complex by cotton plants, and to a much lesser extent by maize plants. The active cotton root sites were located at the main and lateral root tips. Significant variations in the location and the intensity of the uptake were noticed under nonaxenic conditions, which suggested that rhizosphere microorganisms play an important role in NBD-DFO-mediated iron uptake.     

First encounters--deployment of defence-related natural products by plants

Plant-derived natural products have important functions in ecological interactions. In some cases these compounds are deployed to sites of pathogen challenge by vesicle-mediated trafficking. Polar vesicle trafficking of natural products, proteins and other, as yet uncharacterized, cargo is emerging as a common theme in investigations of diverse disease resistance mechanisms in plants. Root-derived natural products can have marked effects on interactions between plants and soilborne organisms, for example by serving as signals for initiation of symbioses with rhizobia and mycorrhizal fungi. They may also contribute to competitiveness of invasive plant species by inhibiting the growth of neighbouring plants (allelopathy). Very little is known about the mechanisms of release of natural products from aerial plant parts or from roots, although there are likely to be commonalities in these processes. There is increasing evidence to indicate that pathogens and symbionts can manipulate plant endomembrane systems to suppress host defence responses and facilitate accommodation within plant cells. The relationship between secretory processes and plant interactions forms the focus of this review, which brings together different aspects of the deployment of defence-related natural products by plants.     

Vertical transmission of fungal endophytes is widespread in forbs

To date, it has been thought that endophytic fungi in forbs infect the leaves of their hosts most commonly by air‐borne spores (termed “horizontal transmission”). Here, we show that vertical transmission from mother plant to offspring, via seeds, occurs in six forb species (Centaurea cyanus, C. nigra, Papaver rhoeas, Plantago lanceolata, Rumex acetosa, and Senecio vulgaris), suggesting that this may be a widespread phenomenon. Mature seeds were collected from field‐grown plants and endophytes isolated from these, and from subsequent cotyledons and true leaves of seedlings, grown in sterile conditions. Most seeds contain one species of fungus, although the identity of the endophyte differs between plant species. Strong evidence for vertical transmission was found for two endophyte species, Alternaria alternata and Cladosporium sphaerospermum. These fungi were recovered from within seeds, cotyledons, and true leaves, although the plant species they were associated with differed. Vertical transmission appears to be an imperfect process, and germination seems to present a bottleneck for fungal growth. We also found that A. alternata and C. sphaerospermum occur on, and within pollen grains, showing that endophyte transmission can be both within and between plant generations. Fungal growth with the pollen tube is likely to be the way in which endophytes enter the developing seed. The fact that true vertical transmission seems common suggests a more mutualistic association between these fungi and their hosts than has previously been thought, and possession of endophytes by seedling plants could have far‐reaching ecological consequences. Seedlings may have different growth rates and be better protected against herbivores and pathogens, dependent on the fungi that were present in the mother plant. This would represent a novel case of trans‐generational resistance in plants.     

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.     

Conservative ecological and evolutionary patterns in liverwort–fungal symbioses

Liverworts, the most ancient group of land plants, form a range of intimate associations with fungi that may be analogous to the mycorrhizas of vascular plants. Most thalloid liverworts contain arbuscular mycorrhizal glomeromycete fungi similar to most vascular plants. In contrast, a range of leafy liverwort genera and one simple thalloid liverwort family (the Aneuraceae) have switched to basidiomycete fungi. These liverwort switches away from glomeromycete fungi may be expected to parallel switches undergone by vascular plants that target diverse lineages of basidiomycete fungi to form ectomycorrhizas. To test this hypothesis, we used a cultivation-independent approach to examine the basidiomycete fungi associated with liverworts in varied worldwide locations by generating fungal DNA sequence data from over 200 field collections of over 30 species. Here we show that eight leafy liverwort genera predominantly and consistently associate with members of the Sebacina vermifera species complex and that Aneuraceae thalloid liverworts associate nearly exclusively with Tulasnella species. Furthermore, within sites where multiple liverwort species co-occur, they almost never share the same fungi. Our analyses reveal a strikingly conservative ecological and evolutionary pattern of liverwort symbioses with basidiomycete fungi that is unlike that of vascular plant mycorrhizas.     

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.     

Effects of Alliaria petiolata (garlic mustard; Brassicaceae) on mycorrhizal colonization and community structure in three herbaceous plants in a mixed deciduous forest

Herbaceous plant species are important components of forest ecosystems, and their persistence in forests may be affected by invasive plant species that reduce mycorrhizal colonization of plant roots. I examined the effect of the invasive plant Alliaria petiolata on arbuscular mycorrhizal fungi (AMF) colonizing the roots of three forest plant species. AMF root colonization and community structure was examined from plants that were growing either in the absence or presence of Alliaria under natural forest conditions. AMF root colonization varied among the plant species but was not significantly affected by Alliaria. With molecular methods, ～12 different taxa of AMF could be distinguished among the root samples, and these taxa belonged to the genera Acaulospora and Glomus, with Glomus dominating AMF communities. There were significant differences between the community of AMF colonizing roots of Maianthemum racemosum and Trillium grandiflorum, but only AMF communities of Maianthemum roots were significantly affected by Alliaria. Indicator species analysis found that an Acaulospora species type was a significant indicator of Maianthemum plants grown in the absence of Alliaria. These results suggest invasive plants like Alliaria may selectively suppress AMF fungi, and this suppression can affect AMF communities colonizing the roots of some native plant species.     

四川都江堰亚热带针阔混交林中主要晚生型外生菌根真菌类群的空间分布

晚生型外生菌根真菌通常出现在森林演替的后期,是成熟林中的优势外生菌根真菌类群.对四川都江堰一片亚热带针阔混交林中的菌根真菌地上群落进行调查,并应用二元逻辑回归分析对晚生型外生菌根真菌的主要类群,即鹅膏菌科、牛肝菌科和红菇科,与周围(5 m×5 m样方)树种组成的关系进行研究.还应用次级变量分析方法对主要外生菌根真菌类群的空间格局进行了分析.结果表明,非外生菌根树种及某些外生菌根树种对特定类群菌根真菌子实体的出现有抑制作用,而不同类群外生菌根真菌在克隆生长上的差异并不是子实体空间分布的决定因素.我们认为,当研究自然林中外生菌根子实体的空间分布时,除了宿主植物的分布,也应考虑非宿主植物的分布以及菌根真菌相互作用的影响.     

四川都江堰亚热带针阔混交林中主要晚生型外生菌根真菌类群的空间分布

晚生型外生菌根真菌通常出现在森林演替的后期,是成熟林中的优势外生菌根真菌类群。对四川都江堰一片亚热带针阔混交林中的菌根真菌地上群落进行调查,并应用二元逻辑回归分析对晚生型外生菌根真菌的主要类群,即鹅膏菌科、牛肝菌科和红菇科,与周围(5m×5m样方)树种组成的关系进行研究。还应用次级变量分析方法对主要外生菌根真菌类群的空间格局进行了分析。结果表明,非外生菌根树种及某些外生菌根树种对特定类群菌根真菌子实体的出现有抑制作用,而不同类群外生菌根真菌在克隆生长上的差异并不是子实体空间分布的决定因素。我们认为,当研究自然林中外生菌根子实体的空间分布时,除了宿主植物的分布,也应考虑非宿主植物的分布以及菌根真菌相互作用的影响。