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.     

Patterns of plant naturalization show that facultative mycorrhizal plants are more likely to succeed outside their native Eurasian ranges

The naturalization of an introduced species is a key stage during the invasion process. Therefore, identifying the traits that favor the naturalization of non-native species can help understand why some species are more successful when introduced to new regions. The ability and the requirement of a plant species to form a mutualism with mycorrhizal fungi, together with the types of associations formed may play a central role in the naturalization success of different plant species. To test the relationship between plant naturalization success and their mycorrhizal associations we analysed a database composed of mycorrhizal status and type for 1981 species, covering 155 families and 822 genera of plants from Europe and Asia, and matched it with the most comprehensive database of naturalized alien species across the world (GloNAF). In mainland regions, we found that the number of naturalized regions was highest for facultative mycorrhizal, followed by obligate mycorrhizal and lowest for non-mycorrhizal plants, suggesting that the ability of forming mycorrhizas is an advantage for introduced plants. We considered the following mycorrhizal types: arbuscular, ectomycorrhizal, ericoid and orchid mycorrhizal plants. Further, dual mycorrhizal species were those that included observations of arbuscular mycorrhizas as well as observations of ectomycorrhizas. Naturalization success (based on the number of naturalized regions) was highest for arbuscular mycorrhizal and dual mycorrhizal plants, which may be related to the low host specificity of arbuscular mycorrhizal fungi and the consequent high availability of arbuscular mycorrhizal fungal partners. However, these patterns of naturalization success were erased in islands, suggesting that the ability to form mycorrhizas may not be an advantage for establishing self-sustaining populations in isolated regions. Taken together our results show that mycorrhizal status and type play a central role in the naturalization process of introduced plants in many regions, but that their effect is modulated by other factors.     

Effects of a belowground mutualism on an aboveground mutualism

Studies of multitrophic interactions between below‐ and aboveground communities have generally focused on soil organisms and antagonists of plant shoots and leaves (herbivores). Despite the widespread occurrence of plant mutualists below‐ and aboveground which can occur on the same host plant, the potential for interactions between them has not been considered. Here we demonstrate that aboveground plant mutualists, insect pollinators, are strongly influenced by belowground plant mutualists, arbuscular mycorrhizal fungi. The presence of arbuscular mycorrhizal fungi in the roots of Chamerion angustifolium increased pollinator visitation and per cent seed set of this plant in the field by up to two times compared with non‐mycorrhizal plants. We propose that interactions between belowground and aboveground mutualisms are widespread and may play important functional roles in populations and communities.     

The dawn of symbiosis between plants and fungi

The colonization of land by plants relied on fundamental biological innovations, among which was symbiosis with fungi to enhance nutrient uptake. Here we present evidence that several species representing the earliest groups of land plants are symbiotic with fungi of the Mucoromycotina. This finding brings up the possibility that terrestrialization was facilitated by these fungi rather than, as conventionally proposed, by members of the Glomeromycota. Since the 1970s it has been assumed, largely from the observation that vascular plant fossils of the early Devonian (400 Ma) show arbuscule-like structures, that fungi of the Glomeromycota were the earliest to form mycorrhizas, and evolutionary trees have, until now, placed Glomeromycota as the oldest known lineage of endomycorrhizal fungi. Our observation that Endogone-like fungi are widely associated with the earliest branching land plants, and give way to glomeromycotan fungi in later lineages, raises the new hypothesis that members of the Mucoromycotina rather than the Glomeromycota enabled the establishment and growth of early land colonists.     

丛枝菌根真菌（AMF）对外来植物入侵反馈机制的研究进展

丛枝菌根真菌（AMF）在植物群落竞争演替、物种多样性的形成及群落空间分布格局、植物群落对全球变化的响应中均起着重要的调节作用;同样也能影响外来植物与本地植物的互作,影响外来植物入侵过程中植物群落演替进程,甚至决定入侵的成败。因此,AMF与外来植物共生及其对外来植物入侵的反馈已成为国际上外来植物入侵机制研究的一个热点。本文基于外来植物的入侵过程,从AMF对外来植物生长、外来植物与本地植物竞争关系的影响,以及外来植物入侵对AMF的影响及AMF对入侵的反馈3个方面综述了AMF对外来植物入侵的反馈机制。外来植物可以通过多种途径改变土著AMF的群落结构和功能,而土著AMF也能直接或间接地改变甚至逆转外来植物与入侵地植物的互作关系。未来的研究不仅需要考虑AMF与外来植物共生的菌根特性和对竞争关系的影响,还需要通过大尺度条件下的野外试验及室内补充试验深入探究影响AMF在外来植物与本地植物竞争演替中的作用的生物和非生物因子,以全面解释AMF影响外来植物入侵的反馈机制。     

丛枝菌根真菌（AMF）对外来植物入侵反馈机制的研究进展

丛枝菌根真菌（AMF）在植物群落竞争演替、物种多样性的形成及群落空间分布格局、植物群落对全球变化的响应中均起着重要的调节作用;同样也能影响外来植物与本地植物的互作,影响外来植物入侵过程中植物群落演替进程,甚至决定入侵的成败。因此,AMF与外来植物共生及其对外来植物入侵的反馈已成为国际上外来植物入侵机制研究的一个热点。本文基于外来植物的入侵过程,从AMF对外来植物生长、外来植物与本地植物竞争关系的影响,以及外来植物入侵对AMF的影响及AMF对入侵的反馈3个方面综述了AMF对外来植物入侵的反馈机制。外来植物可以通过多种途径改变土著AMF的群落结构和功能,而土著AMF也能直接或间接地改变甚至逆转外来植物与入侵地植物的互作关系。未来的研究不仅需要考虑AMF与外来植物共生的菌根特性和对竞争关系的影响,还需要通过大尺度条件下的野外试验及室内补充试验深入探究影响AMF在外来植物与本地植物竞争演替中的作用的生物和非生物因子,以全面解释AMF影响外来植物入侵的反馈机制。     

Geographic structure in a widespread plant-mycorrhizal interaction: pines and false truffles

Mutualistic interactions are likely to exhibit a strong geographic mosaic in their coevolutionary dynamics, but the structure of geographic variation in these interactions is much more poorly characterized than in host-parasite interactions. We used a cross-inoculation experiment to characterize the scales and patterns at which geographic structure has evolved in an interaction between three pine species and one ectomycorrhizal fungus species along the west coast of North America. We found substantial and contrasting patterns of geographic interaction structure for the plants and fungi. The fungi exhibited a clinal pattern of local adaptation to their host plants across the geographic range of three coastal pines. In contrast, plant growth parameters were unaffected by fungal variation, but varied among plant populations and species. Both plant and fungal performance measures varied strongly with latitude. This set of results indicates that in such widespread species interactions, interacting species may evolve asymmetrically in a geographic mosaic because of differing evolutionary responses to clinally varying biotic and abiotic factors.     

The role of plant–mycorrhizal mutualisms in deterring plant invasions: Insights from an individual‐based model

Understanding the factors that determine invasion success for non‐native plants is crucial for maintaining global biodiversity and ecosystem functioning. One hypothesized mechanism by which many exotic plants can become invasive is through the disruption of key plant–mycorrhizal mutualisms, yet few studies have investigated how these disruptions can lead to invader success. We present an individual‐based model to examine how mutualism strengths between a native plant (Impatiens capensis) and mycorrhizal fungus can influence invasion success for a widespread plant invader, Alliaria petiolata (garlic mustard). Two questions were investigated as follows: (a) How does the strength of the mutualism between the native I. capensis and a mycorrhizal fungus affect resistance (i.e., native plant maintaining >60% of final equilibrium plant density) to garlic mustard invasion? (b) Is there a non‐linear relationship between initial garlic mustard density and invasiveness (i.e., garlic mustard representing >60% of final equilibrium plant density)? Our findings indicate that either low (i.e., facultative) or high (i.e., obligate) mutualism strengths between the native plant and mycorrhizal fungus were more likely to lead to garlic mustard invasiveness than intermediate levels, which resulted in higher resistance to garlic mustard invasion. Intermediate mutualism strengths allowed I. capensis to take advantage of increased fitness when the fungus was present but remained competitive enough to sustain high numbers without the fungus. Though strong mutualisms had the highest fitness without the invader, they proved most susceptible to invasion because the loss of the mycorrhizal fungus resulted in a reproductive output too low to compete with garlic mustard. Weak mutualisms were more competitive than strong mutualisms but still led to garlic mustard invasion. Furthermore, we found that under intermediate mutualism strengths, the initial density of garlic mustard (as a proxy for different levels of plant invasion) did not influence its invasion success, as high initial densities of garlic mustard did not lead to it becoming dominant. Our results indicate that plants that form weak or strong mutualisms with mycorrhizal fungi are most vulnerable to invasion, whereas intermediate mutualisms provide the highest resistance to an allelopathic invader.     

A nurse plant benefits from facilitative interactions through mycorrhizae

• Plant facilitation promotes coexistence by maintaining differences in the regeneration niche because some nurse species recruit under arid conditions, whereas facilitated species recruit under more mesic conditions. In one Mexican community, 95% of species recruit through facilitation; Mimosa luisana being a keystone nurse for many of them. M. luisana individuals manifest greater fitness when growing in association with their facilitated plants than when growing in isolation. This observation suggests that nurses also benefit from their facilitated plants, a benefit thought to be mediated by mycorrhizal fungi.
• Under field conditions, we experimentally tested whether mycorrhizal fungi mediate the increased fitness that M. luisana experiences when growing in association with its facilitated plants. We applied fungicide to the soil for nurse plants growing alone and growing in association with their facilitated plants in order to reduce the mycorrhizal colonisation of roots. We then assessed the quantity and quality of seed production of M. luisana in four treatments (isolated‐control, isolated‐fungicide, associated‐control and associated‐fungicide).
• Fungicide application reduced the percentage root length colonised by mycorrhizae and reduced fitness of M. luisana when growing in association with their facilitated plants but not when growing in isolation. This reduction was reflected in the total number of seeds, number of seeds per pod, seed mass and seed viability.
• These results suggest that nurses benefit from the presence of their facilitated plants through links established by mycorrhizae, indicating that both plants and belowground mutualistic communities are all part of one system, coexisting by means of intrinsically linked interactions.

     

Should I stay or should I go? Mycorrhizal plants are more likely to invest in long‐distance seed dispersal than non‐mycorrhizal plants

Seed dispersal and mycorrhizal associations are key mutualisms for the functioning and regeneration of plant communities; however, these processes have seldom been explored together. We hypothesised that obligatory mycorrhizal plants will be less likely to have long‐distance dispersal (LDD) syndromes since the probability of finding suitable mycorrhizal partners is likely to decrease with distance to the mother plant. We contrasted the mycorrhizal status and LDD syndromes for 1960 European plant species, using phylogenetically corrected log‐linear models. Contrary to our expectation, having specialised structures for LDD is more frequent in obligate mycorrhizal plants than in non‐mycorrhizal plants, revealing that lack of compatible mutualists does not constrain investment in LDD structures in the European Flora. Ectomycorrhizal plants associated with wind‐dispersing fungi are also more likely to have specialised structures for wind dispersal. Habitat specificity and narrower niche of non‐mycorrhizal plants might explain the smaller investment in specialised structures for seed dispersal.     

不同来源AM真菌对朱砂根生长和生理特征的影响

朱砂根(Ardisia crenata)原产于东亚和东南亚地区, 现已入侵美国南部等地区。为了探讨AM真菌对朱砂根入侵能力的影响, 我们以根段接种的方法扩繁了源自入侵地美国德克萨斯州和原产地广东东莞、四川峨眉山和湖北兴山的朱砂根根系中的AM真菌, 研究了这些不同来源的AM真菌对朱砂根生长和生理状况的影响。结果表明4个不同来源的AM真菌均能够提高朱砂根的叶面积比(LAR)和相对生长速率(RGR), 而对其饱和净光合速率(Pn)、呼吸速率(Rd)、根冠比(R/S)和各器官中氮、磷营养元素含量均没有显著影响。四个不同来源的AM真菌对朱砂根的作用略有差异, 其中入侵地德克萨斯州与原产地广东东莞AM真菌对朱砂根生长的促进作用较强, 但入侵地AM真菌对朱砂根的促进作用并不普遍高于原产地, AM真菌的作用可能并不是导致入侵种群密度远高于本土种群密度的因素。     

Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence

Numerical models have suggested that the dynamics within mutualisms are not important for the maintenance of diversity. In this study it is demonstrated that the dynamics within mutualism can contribute to the maintenance of diversity within its participants, using a general model of frequency dependence between two mutualistically interacting guilds. Specifically, it is demonstrated that while mutualisms may exhibit positive feedback in density, there may be a negative feedback within a mutualism as a result of the change in composition within the interacting guild. Such a negative feedback results from an asymmetry in the delivery of benefit between participants of the mutualism that generates a negative interguild frequency dependence. This dynamic contributes to the maintenance of diversity within the interacting guilds. Conditions are identified for the maintenance of diversity and the maximization of benefit from mutualism within the context of the model. The utility of these conditions for testing hypotheses using data from the mutualistic interaction between plants and mycorrhizal fungi is then demonstrated.     

Arbuscular mycorrhizal fungi in the tree seedlings of two Australian rain forests: occurrence, colonization, and relationships with plant performance

The roots of rain forest plants are frequently colonized by arbuscular mycorrhizal fungi (AMF) that can promote plant growth in the nutrient poor soils characteristic of these forests. However, recent studies suggest that both the occurrence of AMF on rain forest plants and the dependence of rain forest plants on AMF can be highly variable. We examined the occurrence and levels of AMF colonization of some common seedling species in a tropical and a subtropical rain forest site in Queensland, Australia. We also used a long-term database to compare the growth and mortality rates of seedling species that rarely formed AMF with those that regularly formed AMF. In both forests, more than one-third of the seedling species rarely formed AMF associations, while 40% of species consistently formed AMF in the tropical site compared to 27% in the subtropical site. Consistent patterns of AMF occurrence were observed among plant families at the two sites. Variation among seedling species in AMF occurrence or colonization was not associated with differences in seed mass among species, variation in seedling size and putative age within a species, or lack of AMF inoculum in the soil. Comparisons of four seedling species growing both in the shaded understory and in small canopy gaps revealed an increase in AMF colonization in two of the four species in gaps, suggesting that light limitation partially explains the low occurrence of AMF. Seedling survival was significantly positively associated with seed biomass but not with AMF colonization. Furthermore, seedling species that regularly formed AMF and those that did not had similar rates of growth and survival, suggesting that mycorrhizal and nonmycorrhizal strategies were equivalent in these forests. Furthermore, the high numbers of seedlings that lacked AMF and the overall low rate of seedling growth (the average seedling required 6 years to double its height) suggest that most seedlings did not receive significant indirect benefits from AMF through connection to canopy trees via a common mycorrhizal network.