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Belowground microorganisms drive aboveground plant–pathogen–insect interactions
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.ORCID iD: 0000-0003-1015-8496
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Plants interact with a large diversity of microorganisms and insects, both below and above ground. While studies have shown that belowground microorganisms affect the performance of plants and aboveground attackers, we lack insights into how belowground microbial communities may shape interactions between aboveground pathogens and insects. In this study, we investigated the effects of soil biota and aboveground attackers on plant performance, and examined whether soil biota influence interactions between plants and attackers. We conducted a growth-chamber experiment with oak seedlings (Quercus robur) growing with three distinct natural soil microbial communities. Plants were subjected to single or dual attack by powdery mildew (Erysiphe alphitoides) and aphids (Tuberculatus annulatus), either in the presence or absence of prior attack by a free-feeding caterpillar (Phalera bucephala). Plant height was influenced by soil biota, and seedlings with multiple attackers had more but smaller leaves than healthy seedlings. The soil community affected mildew performance, and mediated the impact of co-occurring attackers on aphid performance. Our study highlights that plant performance is affected both by soil biota and aboveground attackers, and that plant–pathogen–insect interactions are shaped by belowground biota. These findings are important for our understanding of species interactions in nature as well as for practical applications such as integrated pest management.   

Keywords [en]
Belowground–aboveground interactions, Biotrophic pathogen, Compensatory growth, Herbivorous insects, Pedunculate oak
National Category
Ecology
Research subject
Ecology and Evolution
Identifiers
URN: urn:nbn:se:su:diva-195165OAI: oai:DiVA.org:su-195165DiVA, id: diva2:1583712
Funder
Swedish Research Council, 2015-03993Available from: 2021-08-09 Created: 2021-08-09 Last updated: 2022-02-28Bibliographically approved
In thesis
1. Interactions between plants, microbes and insects
Open this publication in new window or tab >>Interactions between plants, microbes and insects
2021 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Plants interact with an astonishing diversity of insects and microorganisms. Both above- and belowground, plants are attacked by herbivores and pathogens, and interact with mutualists such as pollinating insects and beneficial microorganisms. Insects and microorganisms interacting with plants may also affect one another when sharing the same host, leading to direct and indirect interactions between plants, microorganisms and insects. These interactions may have important ecological and evolutionary consequences for all involved species, and interaction outcomes might be dependent on the timing of the interaction as well as the abiotic and biotic context. Thus, in order to predict the outcome of plant–microbe–insect interactions, we need insights into how interactions vary over time and space and how these are influenced by biotic context, from the perspective of all involved species.

In this thesis, my overarching aim was to investigate when and where species interact, and to examine the influence of relative timing and biotic context on the outcomes of plant–microbe–insect interactions from a multi-species perspective. I focussed on two study systems, the pedunculate oak Quercus robur and the wood anemone Anemone nemorosa, and the insects and microorganisms associated with these plants. First, I looked into the drivers behind the spatiotemporal distribution of several fungal pathogens on plants. Specifically, I investigated whether life history traits of pathogens were linked to their metapopulation dynamics. Second, I examined the relative importance of direct and insect-mediated effects of these pathogens on plant performance. Third, I conducted multifactorial growth chamber experiments to investigate performance impacts of interactions from the perspectives of all involved species (plant, insect and pathogen). Lastly, I investigated the influence of time of attacker arrival, early arriving attackers and soil microbial communities on interaction outcomes.

I found that life history traits of pathogens were related to some aspects of metapopulation dynamics. These pathogens had direct, negative impacts on plant growth and fitness, while I did not find evidence for insect-mediated effects. For the multifactorial experiments, I observed some impacts of multiple attackers (pathogens and insects) on plant growth, though plants were mostly tolerant to attack. Attackers that shared a host could affect each other’s performances, with effects mostly being asymmetric, though the interaction outcomes were dependent on the time of arrival, early arriving attackers and soil microbial communities.

In conclusion, my findings show that i) life history traits may influence where pathogen species occur in space and time, that ii) direct effects of pathogens on plant fitness can dominate insect-mediated effects, and that iii) the outcome of species interactions is often asymmetric and dependent on relative timing as well as biotic context. By identifying some of the drivers behind, and consequences of, plant–microbe–insect interactions, this thesis contributes to the development of a predictive framework for species interactions.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2021. p. 45
Keywords
aboveground–belowground interactions, Anemone nemorosa, fungal pathogens, insect herbivores, plant–pathogen–insect interactions, pollination, soil microorganisms, spatiotemporal disease dynamics, Quercus robur
National Category
Ecology
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-195375 (URN)978-91-7911-546-3 (ISBN)978-91-7911-547-0 (ISBN)
Public defence
2021-10-01, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20 and online via Zoom, public link is available at the department website, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2021-09-08 Created: 2021-08-16 Last updated: 2022-02-25Bibliographically approved

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van Dijk, Laura J. A.Abdelfattah, AhmedEhrlén, JohanTack, Ayco J. M.

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