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Plant-associated soil communities: Patterns, drivers and aboveground consequences
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.ORCID iD: 0000-0003-0607-4230
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Soil contains a wealth of diversity – bacteria, fungi, nematodes, arthropods and earthworms are just some of the many organisms found belowground. These organisms play an important role in shaping the soil environment and they strongly influence plant fitness, diversity and community composition. Their impact even cascades up to affect aboveground species interactions. Ultimately, belowground organisms are a vital part of ecosystem functioning. Nevertheless, most of the diversity and ecology of belowground organisms are to this day unknown, and increasing our insights into the role and ecology of soil organisms is of importance for natural and agricultural systems.

The main goal of this thesis was to investigate spatial patterns of plant-associated soil communities (I, II), to identify the drivers of such spatial patterns (I, II, III), and to study some of the consequences of belowground spatial patterns for aboveground species interactions (IV). To answer these questions, I used both observational studies and multifactorial experiments in combination with microscopy and metabarcoding. I focused on the plant Plantago lanceolata (ribwort plantain) and its root-associated soil microbes, with a strong emphasis on arbuscular mycorrhizal fungi, an important group of root symbionts.

I found that in natural environments arbuscular mycorrhizal fungal communities frequently show high small-scale variation (I). In the following work I showed that the pattern of high small-scale heterogeneity may be due to dispersal limitation (II), abiotic conditions such as pH, soil nutrients and climate (I, III), and biotic conditions, such as interspecific community composition and genetic variation (I, II). The high variation at small spatial scales (I) in combination with genetic variation of plants and insects (IV) may help maintain high local heterogeneity in aboveground plant-associated communities, thereby influencing aboveground diversity and dynamics.

The insight gained here has increased our general knowledge on the distribution of soil microbes and the interactions taking place above and belowground. It has furthermore laid a foundation for future work on the world of soil microbes and their implications aboveground.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2018. , p. 43
Keywords [en]
aboveground-belowground interactions, arbuscular mycorrhiza, climate, dispersal, environmental drivers, fungi, genetic variation, nematodes, plant-herbivore interactions, soil communities, spatial patterns
National Category
Ecology Microbiology
Research subject
Ecology and Evolution
Identifiers
URN: urn:nbn:se:su:diva-160903ISBN: 978-91-7797-494-9 (print)ISBN: 978-91-7797-495-6 (electronic)OAI: oai:DiVA.org:su-160903DiVA, id: diva2:1255854
Public defence
2018-11-30, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: Manuscript. Paper 3: Manuscript.

Available from: 2018-11-07 Created: 2018-10-15 Last updated: 2022-02-26Bibliographically approved
List of papers
1. Multiscale patterns and drivers of arbuscular mycorrhizal fungal communities in the roots and root‐associated soil of a wild perennial herb
Open this publication in new window or tab >>Multiscale patterns and drivers of arbuscular mycorrhizal fungal communities in the roots and root‐associated soil of a wild perennial herb
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2018 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 220, no 4, p. 1248-1261Article in journal (Refereed) Published
Abstract [en]

Arbuscular mycorrhizal (AM) fungi form diverse communities and are known to influence above‐ground community dynamics and biodiversity. However, the multiscale patterns and drivers of AM fungal composition and diversity are still poorly understood.

We sequenced DNA markers from roots and root‐associated soil from Plantago lanceolata plants collected across multiple spatial scales to allow comparison of AM fungal communities among neighbouring plants, plant subpopulations, nearby plant populations, and regions. We also measured soil nutrients, temperature, humidity, and community composition of neighbouring plants and nonAM root‐associated fungi.

AM fungal communities were already highly dissimilar among neighbouring plants (c. 30 cm apart), albeit with a high variation in the degree of similarity at this small spatial scale. AM fungal communities were increasingly, and more consistently, dissimilar at larger spatial scales. Spatial structure and environmental drivers explained a similar percentage of the variation, from 7% to 25%. A large fraction of the variation remained unexplained, which may be a result of unmeasured environmental variables, species interactions and stochastic processes.

We conclude that AM fungal communities are highly variable among nearby plants. AM fungi may therefore play a major role in maintaining small‐scale variation in community dynamics and biodiversity.

National Category
Ecology
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-161033 (URN)10.1111/nph.15088 (DOI)000449521400034 ()
Available from: 2018-10-15 Created: 2018-10-15 Last updated: 2022-02-26Bibliographically approved
2. The impact of dispersal, plant genotype and nematodes on arbuscular mycorrhizal fungal colonization
Open this publication in new window or tab >>The impact of dispersal, plant genotype and nematodes on arbuscular mycorrhizal fungal colonization
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2019 (English)In: Soil Biology and Biochemistry, ISSN 0038-0717, E-ISSN 1879-3428, Vol. 132, p. 28-35Article in journal (Refereed) Published
Abstract [en]

While the majority of parasitic and mutualistic microbes have the potential for long-range dispersal, the high turnover in community composition among nearby hosts has often been interpreted to reflect dispersal constraints. To resolve this apparent contradiction, we need further insights into the relative importance of dispersal limitation, host genotype and the biotic environment on the colonization process. We focused on the important root symbionts, the arbuscular mycorrhizal (AM) fungi. We studied AM fungal colonization ability in a controlled mesocosm setting, where we placed Plantago lanceolata plants belonging to four different genotypes in sterile soil at 10, 30 and 70 cm from a central AM fungal inoculated P. lanceolata plant. In part of the mesocosms, we also inoculated the source plants with nematodes. AM fungi colonized receiver plants <1 m away over the course of ten weeks, with a strong effect of distance from source plant on AM fungal colonization. Plant genotype influenced AM fungal colonization during the early stages of colonization, while nematode inoculation had no effect on AM fungal colonization. Overall, the effect of both dispersal limitation and plant genetic variation may underlie the small-scale heterogeneity found in natural AM fungal communities.

Keywords
Arbuscular mycorrhizal fungi, Colonization ability, Dispersal, Genotype, Nematodes, Plantago lanceolata
National Category
Ecology
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-161035 (URN)10.1016/j.soilbio.2019.01.018 (DOI)000465057200004 ()
Available from: 2018-10-15 Created: 2018-10-15 Last updated: 2022-02-26Bibliographically approved
3. The impact of elevated temperature and drought on the ecology and evolution of plant-soil microbe interactions
Open this publication in new window or tab >>The impact of elevated temperature and drought on the ecology and evolution of plant-soil microbe interactions
2020 (English)In: Journal of Ecology, ISSN 0022-0477, E-ISSN 1365-2745, Vol. 108, no 1, p. 337-352Article in journal (Refereed) Published
Abstract [en]
  1. Climate change is shifting the distribution of species, and may have a profound impact on the ecology and evolution of species interactions. However, we know little about the impact of increasing temperature and changing rainfall patterns on the interactions between plants and their beneficial and antagonistic root symbionts.
  2. Here, we used a reciprocal multifactorial growth chamber experiment with seeds and soil microbial communities from three origins to investigate the impact of temperature and soil moisture on the growth, arbuscular mycorrhizal (AM) fungal colonization and root‐associated fungal community of a perennial herb. Moreover, we tested whether plants and AM fungi performed better or worse when plants were grown with their local soil biota, for example, due to plant adaptation or changes in the genetic or species composition of the soil microbial community.
  3. Temperature and soil moisture generally increased plant growth, whereas temperature but not soil moisture increased AM fungal colonization. The strength and direction of the plants' response to temperature were dependent on soil moisture and differed among plant populations, and AM fungal colonization was further affected by the origin of the soil microbial community. The root‐associated fungal community structure was impacted by temperature, soil moisture and the soil microbial origin, with interactive effects between the microbial origin and the abiotic environment. Plant biomass was lower when plants were grown with their local soil microbes, potentially due to intraspecific negative plant–soil feedbacks.
  4. Synthesis. Our findings indicate that, beyond a relatively uniform increase of plant growth and arbuscular mycorrhizal (AM) fungal colonization with increasing temperature, plants and root‐associated fungi of different origins will vary in their response to climate change (i.e. elevated temperature and shifts in rainfall). This may create pronounced, but difficult to predict, spatial and temporal variation in the ecology and evolution of plant–microbe interactions with a changing climate.
Keywords
abiotic and biotic factors, arbuscular mycorrhizal fungi, local adaptation, Plantago lanceolata, plant–soil (below‐ground) interactions, plant–soil feedback, root‐associated fungi, soil moisture
National Category
Ecology
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-161036 (URN)10.1111/1365-2745.13292 (DOI)000535186200027 ()
Available from: 2018-10-15 Created: 2018-10-15 Last updated: 2022-02-26Bibliographically approved
4. Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant-herbivore interaction
Open this publication in new window or tab >>Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant-herbivore interaction
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2017 (English)In: Ecological Entomology, ISSN 0307-6946, E-ISSN 1365-2311, Vol. 42, no 6, p. 793-802Article in journal (Refereed) Published
Abstract [en]

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 angstrom land 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.

Keywords
Arbuscular mycorrhizal fungi, genetic variation, Glomeromycota, Melitaea cinxia, multitrophic interaction, Plantago lanceolata, plant-herbivore interaction
National Category
Biological Sciences
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-149949 (URN)10.1111/een.12453 (DOI)000414613300013 ()
Available from: 2018-01-03 Created: 2018-01-03 Last updated: 2022-03-23Bibliographically approved

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