Mycorrhizal fungi are critical members of the plant microbiome, forming a symbiosis with the roots of most plants on Earth. Most plant species partner with either arbuscular or ectomycorrhizal fungi, and these symbioses are thought to represent plant adaptations to fast and slow soil nutrient cycling rates. This generates a second hypothesis, that arbuscular and ectomycorrhizal plant species traits complement and reinforce these fungal strategies, resulting in nutrient acquisitive vs. conservative plant trait profiles. Here we analyzed 17,764 species level trait observations from 2,940 woody plant species to show that mycorrhizal plants differ systematically in nitrogen and phosphorus economic traits. Differences were clearest in temperate latitudes, where ectomycorrhizal plant species are more nitrogen use- and phosphorus use-conservative than arbuscular mycorrhizal species. This difference is reflected in both aboveground and belowground plant traits and is robust to controlling for evolutionary history, nitrogen fixation ability, deciduousness, latitude, and species climate niche. Furthermore, mycorrhizal effects are large and frequently similar to or greater in magnitude than the influence of plant nitrogen fixation ability or deciduous vs. evergreen leaf habit. Ectomycorrhizal plants are also more nitrogen conservative than arbuscular plants in boreal and tropical ecosystems, although differences in phosphorus use are less apparent outside temperate latitudes. Our findings bolster current theories of ecosystems rooted in mycorrhizal ecology and support the hypothesis that plant mycorrhizal association is linked to the evolution of plant nutrient economic strategies.
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Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism
Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.
more » « less- NSF-PAR ID:
- 10153910
- Author(s) / Creator(s):
- ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Communications Biology
- Volume:
- 1
- Issue:
- 1
- ISSN:
- 2399-3642
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Rising atmospheric carbon dioxide concentrations (CO2) and atmospheric nitrogen (N) deposition have contrasting effects on ectomycorrhizal (EM) and arbuscular mycorrhizal (AM) symbioses, potentially mediating forest responses to environmental change.
In this study, we evaluated the cumulative effects of historical environmental change on N concentrations and δ15N values in AM plants, EM plants, EM fungi, and saprotrophic fungi using herbarium specimens collected in Minnesota, USA from 1871 to 2016. To better understand mycorrhizal mediation of foliar δ15N, we also analyzed a subset of previously published foliar δ15N values from across the United States to parse the effects of N deposition and CO2rise.
Over the last century in Minnesota, N concentrations declined among all groups except saprotrophic fungi. δ15N also declined among all groups of plants and fungi; however, foliar δ15N declined less in EM plants than in AM plants. In the analysis of previously published foliar δ15N values, this slope difference between EM and AM plants was better explained by nitrogen deposition than by CO2rise.
Mycorrhizal type did not explain trajectories of plant N concentrations. Instead, plants and EM fungi exhibited similar declines in N concentrations, consistent with declining forest N status despite moderate levels of N deposition.
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Summary Arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) produce contrasting plant–soil feedbacks, but how these feedbacks are constrained by lithology is poorly understood.
We investigated the hypothesis that lithological drivers of soil fertility filter plant resource economic strategies in ways that influence the relative fitness of trees with AMF or EMF symbioses in a Bornean rain forest containing species with both mycorrhizal strategies.
Using forest inventory data on 1245 tree species, we found that although AMF‐hosting trees had greater relative dominance on all soil types, with declining lithological soil fertility EMF‐hosting trees became more dominant. Data on 13 leaf traits and wood density for a total of 150 species showed that variation was almost always associated with soil type, whereas for six leaf traits (structural properties; carbon, nitrogen, phosphorus ratios, nitrogen isotopes), variation was also associated with mycorrhizal strategy. EMF‐hosting species had slower leaf economics than AMF‐hosts, demonstrating the central role of mycorrhizal symbiosis in plant resource economies.
At the global scale, climate has been shown to shape forest mycorrhizal composition, but here we show that in communities it depends on soil lithology, suggesting scale‐dependent abiotic factors influence feedbacks underlying the relative fitness of different mycorrhizal strategies.
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Abstract To understand how diverse mutualisms coevolve and how species adapt to complex environments, a description of the underlying genetic basis of the traits involved must be provided. For example, in diverse coevolving mutualisms, such as the interaction of host plants with a suite of symbiotic mycorrhizal fungi, a key question is whether host plants can coevolve independently with multiple species of symbionts, which depends on whether those interactions are governed independently by separate genes or pleiotropically by shared genes. To provide insight into this question, we employed an association mapping approach in a clonally replicated field experiment of loblolly pine (
Pinus taeda L.) to identify genetic components of host traits governing ectomycorrhizal (EM) symbioses (mycorrhizal traits). The relative abundances of different EM fungi as well as the total number of root tips per cm root colonized by EM fungi were analyzed as separate mycorrhizal traits of loblolly pine. Single‐nucleotide polymorphisms (SNPs) within candidate genes of loblolly pine were associated with loblolly pine mycorrhizal traits, mapped to the loblolly pine genome, and their putative protein function obtained when available. The results support the hypothesis that ectomycorrhiza formation is governed by host genes of large effect that apparently have independent influences on host interactions with different symbiont species. -
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Mycorrhizal restoration benefits are widely acknowledged, yet factors underpinning this success remain unclear. To illuminate when natural regeneration might be sufficient, we investigated the degree mycorrhizal fungi would colonize
Populus fremontii (Fremont cottonwood) 2 years after the restoration of a riparian corridor, in the presence of an adjacent source. We compared colonization levels across plant populations and ecotypes, and from trees in the planted area to those in natural source populations. Four findings contribute to the theory and application of host–symbiont interactions. (1) Median ectomycorrhizal colonization of trees in the planted area was less than one‐tenth of that within natural source populations (p < 0.05), suggesting that even with adjacent intact habitat, sluggish regeneration would make proactive mycorrhizal restoration beneficial. (2) Within the planted area, median ectomycorrhizal and arbuscule colonization of trees sourced from greater distances were less than one‐third of that for trees sourced locally (p < 0.05), suggesting translocation poses barriers to symbioses. (3) Changes in colonization did not align with plant ecotypes, suggesting that geographic scales of selection for plants and fungi differ. (4) Slight increases in median mycorrhizal colonization (from 0% to 5%) were strongly correlated with increased survival for the plant provenance with lowest survival (r 2 = 46% andr s = 48%,p < 0.05), suggesting mycorrhizae are particularly beneficial when plants are under stress (including translocation‐induced stress). This study is novel in demonstrating that mycorrhizal regeneration is slow even in the presence of adjacent intact habitat, and that when colonization could seem negligible, it may still have biological significance.
