Fine-root traits in the global spectrum of plant form and function.

Plant traits determine how individual plants cope with heterogeneous environments. Despite large variability in individual traits, trait coordination and trade-offs1,2 result in some trait combinations being much more widespread than others, as revealed in the global spectrum of plant form and function (GSPFF3) and the root economics space (RES4) for aboveground and fine-root traits, respectively. Here we combine the traits that define both functional spaces. Our analysis confirms the major trends of the GSPFF and shows that the RES captures additional information. The four dimensions needed to explain the non-redundant information in the dataset can be summarized in an aboveground and a fine-root plane, corresponding to the GSPFF and the RES, respectively. Both planes display high levels of species aggregation, but the differentiation among growth forms, families and biomes is lower on the fine-root plane, which does not include any size-related trait, than on the aboveground plane. As a result, many species with similar fine-root syndromes display contrasting aboveground traits. This highlights the importance of including belowground organs to the GSPFF when exploring the interplay between different natural selection pressures and whole-plant trait integration.

Niche types and community assembly.

Studies of niche differentiation and biodiversity often focus on a few niche dimensions due to the methodological challenge of describing hyperdimensional niche space. However, this may limit our understanding of community assembly processes. We used the full spectrum of realized niche types to study arbuscular mycorrhizal fungal communities: distinguishing abiotic and biotic, and condition and resource, axes. Estimates of differentiation in relation to different niche types were only moderately correlated. However, coexisting taxon niches were consistently less differentiated than expected, based on a regional null model, indicating the importance of habitat filtering at that scale. Nonetheless, resource niches were relatively more differentiated than condition niches, which is consistent with the effect of a resource niche-based coexistence mechanism. Considering niche types, and in particular distinguishing resource and condition niches, provides a more complete understanding of community assembly, compared with studying individual niche axes or the full niche.

Symbiont plasticity as a driver of plant success.

We discuss which plant species are likely to become winners, that is achieve the highest global abundance, in changing landscapes, and whether plant-associated microbes play a determining role. Reduction and fragmentation of natural habitats in historic landscapes have led to the emergence of patchy, hybrid landscapes, and novel landscapes where anthropogenic ecosystems prevail. In patchy landscapes, species with broad niches are favoured. Plasticity in the degree of association with symbiotic microbes may contribute to broader plant niches and optimization of symbiosis costs and benefits, by downregulating symbiosis when it is unnecessary and upregulating it when it is beneficial. Plasticity can also be expressed as the switch from one type of mutualism to another, for example from nutritive to defensive mutualism with increasing soil fertility and the associated increase in parasite load. Upon dispersal, wide mutualistic partner receptivity is another facet of symbiont plasticity that becomes beneficial, because plants are not limited by the availability of specialist partners when arriving at new locations. Thus, under conditions of global change, symbiont plasticity allows plants to optimize the activity of mutualistic relationships, potentially allowing them to become winners by maximizing geographic occupancy and local abundance.

Mycorrhizal symbioses in the Andean paramo.

The Andean paramo, hereafter "paramo", is a Neotropical high-mountain region between the treeline and permanent snowline (3500-4800 m) and is considered the world's coolest biodiversity hotspot. Because of paramo's high humidity, solar radiation and temperature variation, mycorrhizal symbiosis is expected to be essential for plants. Existing theory suggests that replacement of arbuscular mycorrhizal (AM) by ectomycorrhizal (ECM) and then ericoid mycorrhizal plants (ERM) can be expected with increasing elevation. Previous findings also suggest that non-(NM) and facultatively mycorrhizal (FM) species predominate over obligatory mycorrhizal (OM) species at high elevations. However, these expectations have never been tested outside of the northern temperate zone. We addressed the distribution and environmental drivers of plant mycorrhizal types (AM, ECM and ERM) and statuses (NM, FM and OM) along the paramo's elevational gradient. We used vegetation plots from the VegParamo database, climatic and edaphic data from online repositories, and up-to-date observation information about plant mycorrhizal traits at species and genus level, the latter being proposed as hypotheses. AM plants were dominant along the entire gradient, and ERM plants were most abundant at the lowest elevations (2500-3000 m). The share of FM plants increased and that of OM plants decreased with elevation, while NM plants increased above 4000 m. Temperature and soil pH were positively related to the abundance of AM plants and negatively to ERM plants. Our results reveal patterns that contrast with those observed in temperate northern-hemisphere ecosystems.

Environmental modulation of plant mycorrhizal traits in the global flora.

Mycorrhizal symbioses are known to strongly influence plant performance, structure plant communities and shape ecosystem dynamics. Plant mycorrhizal traits, such as those characterising mycorrhizal type (arbuscular (AM), ecto-, ericoid or orchid mycorrhiza) and status (obligately (OM), facultatively (FM) or non-mycorrhizal) offer valuable insight into plant belowground functionality. Here, we compile available plant mycorrhizal trait information and global occurrence data ( ∼ 100 million records) for 11,770 vascular plant species. Using a plant phylogenetic mega-tree and high-resolution climatic and edaphic data layers, we assess phylogenetic and environmental correlates of plant mycorrhizal traits. We find that plant mycorrhizal type is more phylogenetically conserved than plant mycorrhizal status, while environmental variables (both climatic and edaphic; notably soil texture) explain more variation in mycorrhizal status, especially FM. The previously underestimated role of environmental conditions has far-reaching implications for our understanding of ecosystem functioning under changing climatic and soil conditions.

GlobalAMFungi: a global database of arbuscular mycorrhizal fungal occurrences from high-throughput sequencing metabarcoding studies.

Arbuscular mycorrhizal (AM) fungi are crucial mutualistic symbionts of the majority of plant species, with essential roles in plant nutrient uptake and stress mitigation. The importance of AM fungi in ecosystems contrasts with our limited understanding of the patterns of AM fungal biogeography and the environmental factors that drive those patterns. This article presents a release of a newly developed global AM fungal dataset (GlobalAMFungi database, https://globalamfungi.com) that aims to reduce this knowledge gap. It contains almost 50 million observations of Glomeromycotinian AM fungal amplicon DNA sequences across almost 8500 samples with geographical locations and additional metadata obtained from 100 original studies. The GlobalAMFungi database is built on sequencing data originating from AM fungal taxon barcoding regions in: i) the small subunit rRNA (SSU) gene; ii) the internal transcribed spacer 2 (ITS2) region; and iii) the large subunit rRNA (LSU) gene. The GlobalAMFungi database is an open source and open access initiative that compiles the most comprehensive atlas of AM fungal distribution. It is designed as a permanent effort that will be continuously updated by its creators and through the collaboration of the scientific community. This study also documented applicability of the dataset to better understand ecology of AM fungal taxa.

Deciphering the role of specialist and generalist plant-microbial interactions as drivers of plant-soil feedback.

Feedback between plants and soil microbial communities can be a powerful driver of vegetation dynamics. Plants elicit changes in the soil microbiome that either promote or suppress conspecifics at the same location, thereby regulating population density-dependence and species co-existence. Such effects are often attributed to the accumulation of host-specific antagonistic or beneficial microbiota in the rhizosphere. However, the identity and host-specificity of the microbial taxa involved are rarely empirically assessed. Here we review the evidence for host-specificity in plant-associated microbes and propose that specific plant-soil feedbacks can also be driven by generalists. We outline the potential mechanisms by which generalist microbial pathogens, mutualists and decomposers can generate differential effects on plant hosts and synthesize existing evidence to predict these effects as a function of plant investments into defence, microbial mutualists and dispersal. Importantly, the capacity of generalist microbiota to drive plant-soil feedbacks depends not only on the traits of individual plants but also on the phylogenetic and functional diversity of plant communities. Identifying factors that promote specialization or generalism in plant-microbial interactions and thereby modulate the impact of microbiota on plant performance will advance our understanding of the mechanisms underlying plant-soil feedback and the ways it contributes to plant co-existence.

Global patterns in endemicity and vulnerability of soil fungi.

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms.

Hedgerows increase the diversity and modify the composition of arbuscular mycorrhizal fungi in Mediterranean agricultural landscapes.

Sustainable agriculture is essential to address global challenges such as climate change and biodiversity loss. Hedgerows enhance aboveground biodiversity and provide ecosystem services, but little is known about their impact on soil biota. Arbuscular mycorrhizal (AM) fungi are one of the key components of belowground biodiversity. We compared the diversity and composition of AM fungal communities at four farmland sites located in Central Spain, where 132 soil samples in total were collected to assess soil physical and chemical properties and the AM fungal communities. We compared the richness (number of AM fungal taxa), taxonomic, functional, and phylogenetic diversity, and structure of the AM fungal communities across three farmland habitat types, namely hedgerows, woody crops (olive groves and vineyard), and herbaceous crops (barley, sunflower, and wheat). Our results showed positive effects of hedgerows on most diversity metrics. Almost 60% of the AM fungal taxa were shared among the three farmland habitat types. Hedgerows increased AM fungal taxonomic richness (31%) and alpha diversity (25%), and especially so compared to herbaceous crops (45% and 28%, respectively). Hedgerows harbored elevated proportions of AM fungi with non-ruderal life-history strategies. AM fungal communities were more similar between hedgerows and woody crops than between hedgerows and adjacent herbaceous crops, possibly because of differences in tillage and fertilization. Unexpectedly, hedgerows reduced phylogenetic diversity, which might be related to more selective associations of AM fungi with woody plants than with herbaceous crops. Overall, the results suggest that planting hedgerows contributes to maintain belowground diversity. Thus, European farmers should plant more hedgerows to attain the goals of the EU Biodiversity Strategy for 2030.

Global taxonomic and phylogenetic assembly of AM fungi.

Arbuscular mycorrhizal (AM) fungi are a ubiquitous group of plant symbionts, yet processes underlying their global assembly - in particular the roles of dispersal limitation and historical drivers - remain poorly understood. Because earlier studies have reported niche conservatism in AM fungi, we hypothesized that variation in taxonomic community composition (i.e., unweighted by taxon relatedness) should resemble variation in phylogenetic community composition (i.e., weighted by taxon relatedness) which reflects ancestral adaptations to historical habitat gradients. Because of the presumed strong dispersal ability of AM fungi, we also anticipated that the large-scale structure of AM fungal communities would track environmental conditions without regional discontinuity. We used recently published AM fungal sequence data (small-subunit ribosomal RNA gene) from soil samples collected worldwide to reconstruct global patterns in taxonomic and phylogenetic community variation. The taxonomic structure of AM fungal communities was primarily driven by habitat conditions, with limited regional differentiation, and there were two well-supported clusters of communities - occurring in cold and warm conditions. Phylogenetic structure was driven by the same factors, though all relationships were markedly weaker. This suggests that niche conservatism with respect to habitat associations is weakly expressed in AM fungal communities. We conclude that the composition of AM fungal communities tracks major climatic and edaphic gradients, with the effects of dispersal limitation and historic factors considerably less apparent than those of climate and soil.

Light availability and light demand of plants shape the arbuscular mycorrhizal fungal communities in their roots.

Plants involved in the arbuscular mycorrhizal (AM) symbiosis trade photosynthetically derived carbon for fungal-provided soil nutrients. However, little is known about how plant light demand and ambient light conditions influence root-associating AM fungal communities. We conducted a manipulative field experiment to test whether plants' shade-tolerance influences their root AM fungal communities in open and shaded grassland sites. We found similar light-dependent shifts in AM fungal community structure for experimental bait plant roots and the surrounding soil. Yet, deviation from the surrounding soil towards lower AM fungal beta-diversity in the roots of shade-intolerant plants in shade suggested preferential carbon allocation to specific AM fungi in conditions where plant-assimilated carbon available to fungi was limited. We conclude that favourable environmental conditions widen the plant biotic niche, as demonstrated here with optimal light availability reducing plants' selectivity for specific AM fungi, and promote compatibility with a larger number of AM fungal taxa.

Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi.

The arbuscular mycorrhizal (AM) fungi are a globally distributed group of soil organisms that play critical roles in ecosystem function. However, the ecological niches of individual AM fungal taxa are poorly understood. We collected > 300 soil samples from natural ecosystems worldwide and modelled the realised niches of AM fungal virtual taxa (VT; approximately species-level phylogroups). We found that environmental and spatial variables jointly explained VT distribution worldwide, with temperature and pH being the most important abiotic drivers, and spatial effects generally occurring at local to regional scales. While dispersal limitation could explain some variation in VT distribution, VT relative abundance was almost exclusively driven by environmental variables. Several environmental and spatial effects on VT distribution and relative abundance were correlated with phylogeny, indicating that closely related VT exhibit similar niche optima and widths. Major clades within the Glomeraceae exhibited distinct niche optima, Acaulosporaceae generally had niche optima in low pH and low temperature conditions, and Gigasporaceae generally had niche optima in high precipitation conditions. Identification of the realised niche space occupied by individual and phylogenetic groups of soil microbial taxa provides a basis for building detailed hypotheses about how soil communities respond to gradients and manipulation in ecosystems worldwide.

Arbuscular mycorrhizal fungi promote small-scale vegetation recovery in the forest understorey.

Root-associating arbuscular mycorrhizal (AM) fungi foster vegetation recovery in degraded habitats. AM fungi increase nutrient availability for host plants; therefore, their importance is expected to be higher when nutrient availability is low. However, little is known about how small-scale variation in nutrient availability influences plant and AM fungal communities in a stable ecosystem. We conducted a 2-year field study in the understorey of a boreonemoral forest where we examined plant and AM fungal communities at microsites (15 cm diameter) with intact vegetation cover and at disturbed microsites where vegetation was cleared away and soil was sterilized to remove soil biota. We manipulated soil nutrient content (increased with fertilizer, unchanged, or decreased with sucrose addition) and fungal activity (natural or suppressed by fungicide addition) at these microsites. After two vegetation seasons, manipulations with nutrient content resulted in significant, although moderate, differences in the content of soil nutrients (e.g. in soil phosphorus). Suppression of fungal activity resulted in lower richness, abundance and phylogenetic diversity of AM fungal community, independently of microsite type and soil fertility level. Plant species richness and diversity decreased when fungal activity was suppressed at disturbed but not in intact microsites. The correlation between plant and AM fungal communities was not influenced by microsite type or soil fertility. We conclude that small-scale variation in soil fertility and habitat integrity does not influence the interactions between plants and AM fungi. The richness, but not composition, of AM fungal communities recovered fast after small-scale disturbance and supported the recovery of species-rich vegetation.

Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities.

The benefits of the arbuscular mycorrhizal (AM) symbiosis between plants and fungi are modulated by the functional characteristics of both partners. However, it is unknown to what extent functionally distinct groups of plants naturally associate with different AM fungi. We reanalysed 14 high-throughput sequencing data sets describing AM fungal communities associating with plant individuals (2427) belonging to 297 species. We examined how root-associating AM fungal communities varied between plants with different growth forms, photosynthetic pathways, CSR (competitor, stress-tolerator, ruderal) strategies, mycorrhizal statuses and N-fixing statuses. AM fungal community composition differed in relation to all studied plant functional groups. Grasses, C4 and nonruderal plants were characterised by high AM fungal alpha diversity, while C4 , ruderal and obligately mycorrhizal plants were characterised by high beta diversity. The phylogenetic diversity of AM fungi, a potential surrogate for functional diversity, was higher among forbs than other plant growth forms. Putatively ruderal (previously cultured) AM fungi were disproportionately associated with forbs and ruderal plants. There was phylogenetic correlation among AM fungi in the degree of association with different plant growth forms and photosynthetic pathways. Associated AM fungal communities constitute an important component of plant ecological strategies. Functionally different plants associate with distinct AM fungal communities, linking mycorrhizal associations with functional diversity in ecosystems.

Fifty thousand years of Arctic vegetation and megafaunal diet.

Although it is generally agreed that the Arctic flora is among the youngest and least diverse on Earth, the processes that shaped it are poorly understood. Here we present 50 thousand years (kyr) of Arctic vegetation history, derived from the first large-scale ancient DNA metabarcoding study of circumpolar plant diversity. For this interval we also explore nematode diversity as a proxy for modelling vegetation cover and soil quality, and diets of herbivorous megafaunal mammals, many of which became extinct around 10 kyr bp (before present). For much of the period investigated, Arctic vegetation consisted of dry steppe-tundra dominated by forbs (non-graminoid herbaceous vascular plants). During the Last Glacial Maximum (25-15 kyr bp), diversity declined markedly, although forbs remained dominant. Much changed after 10 kyr bp, with the appearance of moist tundra dominated by woody plants and graminoids. Our analyses indicate that both graminoids and forbs would have featured in megafaunal diets. As such, our findings question the predominance of a Late Quaternary graminoid-dominated Arctic mammoth steppe.

Non-random association patterns in a plant-mycorrhizal fungal network reveal host-symbiont specificity.

Arbuscular mycorrhizal (AM) fungi are obligate plant symbionts that have important functions in most terrestrial ecosystems, but there remains an incomplete understanding of host-fungus specificity and the relationships between species and functional groups of plants and AM fungi. Here, we aimed to provide a comprehensive description of plant-AM fungal interactions in a biodiverse semi-natural grassland. We sampled all plant species in a 1,000-m2 homogeneous plot of dry calcareous grassland in two seasons (summer and autumn) and identified root-colonizing AM fungi by SSU rDNA sequencing. In the network of 33 plant and 100 AM fungal species, we found a significant effect of both host plant species and host plant functional group on AM fungal richness and community composition. Comparison with network null models revealed a larger-than-random degree of partner selectivity among plants. Grasses harboured a larger number of AM fungal partners and were more generalist in partner selection, compared with forbs. More generalist partner association and lower specialization were apparent among obligately, compared with facultatively, mycorrhizal plant species and among locally more abundant plant species. This study provides the most complete data set of co-occurring plant and AM fungal taxa to date, showing that at this particular site, the interaction network is assembled non-randomly, with moderate selectivity in associations between plant species and functional groups and their fungal symbionts.

Conceptual differences lead to divergent trait estimates in empirical and taxonomic approaches to plant mycorrhizal trait assignment.

Empirical and taxonomic approaches are the two main methods used to assign plant mycorrhizal traits to species lists. While the empirical approach uses only available empirical information, the taxonomic approach extrapolates certain core information about plant mycorrhizal types and statuses to related species. Despite recent claims that the taxonomic approach is now almost definitive, with little benefit to be gained from further empirical data collection, it has not been thoroughly compared with the empirical approach. Using the most complete available plant mycorrhizal trait information for Europe and both assignment approaches, we calculate the proportion of species for each trait, and model environmental drivers of trait distribution across the continent. We found large degrees of mismatch between approaches, with consequences for biogeographical interpretation, among facultatively mycorrhizal (FM; 91% of species mismatched), non-mycorrhizal (NM; 45%), and to a lesser extent arbuscular mycorrhizal (AM; 16%) plant species. This can partly be attributed to the taxonomic precision of the taxonomic approach and the use of different AM, NM, and FM concepts. Our results showed that the extrapolations of the taxonomic approach do not consistently match with empirical information and indicate that more empirical data are needed, in particular for FM, NM, and AM plant species. Clarifying certain concepts underlying mycorrhizal traits and empirically describing NM, AM, and FM species within plant families can greatly improve our understanding of the biogeography of mycorrhizal symbiosis.

The role of plant mycorrhizal type and status in modulating the relationship between plant and arbuscular mycorrhizal fungal communities.

Interactions between communities of plants and arbuscular mycorrhizal (AM) fungi shape fundamental ecosystem properties. Experimental evidence suggests that compositional changes in plant and AM fungal communities should be correlated, but empirical data from natural ecosystems are scarce. We investigated the dynamics of covariation between plant and AM fungal communities during three stages of grassland succession, and the biotic and abiotic factors shaping these dynamics. Plant communities were characterised using vegetation surveys. AM fungal communities were characterised by 454-sequencing of the small subunit rRNA gene and identification against the AM fungal reference database MaarjAM. AM fungal abundance was estimated using neutral-lipid fatty acids (NLFAs). Multivariate correlation analysis (Procrustes) revealed a significant relationship between plant and AM fungal community composition. The strength of plant-AM fungal correlation weakened during succession following cessation of grassland management, reflecting changes in the proportion of plants exhibiting different AM status. Plant-AM fungal correlation was strong when the abundance of obligate AM plants was high, and declined as the proportion of facultative AM plants increased. We conclude that the extent to which plants rely on AM symbiosis can determine how tightly communities of plants and AM fungi are interlinked, regulating community assembly of both symbiotic partners.

Host preference and network properties in biotrophic plant-fungal associations.

Analytical methods can offer insights into the structure of biological networks, but mechanisms that determine the structure of these networks remain unclear. We conducted a synthesis based on 111 previously published datasets to assess a range of ecological and evolutionary mechanisms that may influence the plant-associated fungal interaction networks. We calculated the relative host effect on fungal community composition and compared nestedness and modularity among different mycorrhizal types and endophytic fungal guilds. We also assessed how plant-fungal network structure was related to host phylogeny, environmental and sampling properties. Orchid mycorrhizal fungal communities responded most strongly to host identity, but the effect of host was similar among all other fungal guilds. Community nestedness, which did not differ among fungal guilds, declined significantly with increasing mean annual precipitation on a global scale. Orchid and ericoid mycorrhizal fungal communities were more modular than ectomycorrhizal and root endophytic communities, with arbuscular mycorrhizal fungi in an intermediate position. Network properties among a broad suite of plant-associated fungi were largely comparable and generally unrelated to phylogenetic distance among hosts. Instead, network metrics were predominantly affected by sampling and matrix properties, indicating the importance of study design in properly inferring ecological patterns.