Endogenous rhythmic growth, a trait suitable for the study of interplays between multitrophic interactions and tree development

Herrmann, Sylvie; Grams, Thorsten E. E.; Tarkka, Mika; Angay, Oguzhan; Bacht, Michael; Bönn, Markus; Feldhahn, Lasse; Graf, Marcel; Kurth, Florence; Maboreke, Hazel; Mailänder, Sarah; Recht, Sabine; Fleischmann, F.; Rueß, Liliane; Schädler, Martin; Scheu, Stefan; Schrey, Silvia D.; Buscot, François

doi:10.1016/j.ppees.2016.02.003

Cited by 20 publications

(35 citation statements)

References 60 publications

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“…We used pedunculate oak microcuttings propagated from the clone DF159 ( Quercus robur ) and rooted as described by [ 84 ]. Microcuttings were grown in soil-based microcosms, 12 × 12 cm petri dishes filled with γ-sterilized soil collected from an oak forest stand as described in detail by Herrmann et al [ 27 ]. Half of the microcuttings were inoculated with the ectomycorrhizal fungus Piloderma croceum (J. Erikss and Hjortst).…”

Section: Methodsmentioning

confidence: 99%

“…However, localized and systemic responses of plants to nematode infection have been in the focus of investigations on agricultural crops [ 24 – 26 ], whereas knowledge in forest trees remains scarce. To support these kinds of studies, Tarkka et al [ 9 ] generated a reference library for differential gene expression of pedunculate oak during series of beneficial and detrimental below and above ground biotic interactions (OakContigDF159.1) in the frame of the research consortium TrophinOak [ 27 ]. The OakContigDF159.1 assembly was based on a set of 18 cDNA libraries from oak roots and leaves interacting with different organisms including the nematode Pratylenchus penetrans .…”

Section: Introductionmentioning

confidence: 99%

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Transcriptome analysis in oak uncovers a strong impact of endogenous rhythmic growth on the interaction with plant-parasitic nematodes

et al. 2016

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BackgroundPedunculate oak (Quercus robur L.), an important forest tree in temperate ecosystems, displays an endogenous rhythmic growth pattern, characterized by alternating shoot and root growth flushes paralleled by oscillations in carbon allocation to below- and aboveground tissues. However, these common plant traits so far have largely been neglected as a determining factor for the outcome of plant biotic interactions. This study investigates the response of oak to migratory root-parasitic nematodes in relation to rhythmic growth, and how this plant-nematode interaction is modulated by an ectomycorrhizal symbiont. Oaks roots were inoculated with the nematode Pratylenchus penetrans solely and in combination with the fungus Piloderma croceum, and the systemic impact on oak plants was assessed by RNA transcriptomic profiles in leaves.ResultsThe response of oaks to the plant-parasitic nematode was strongest during shoot flush, with a 16-fold increase in the number of differentially expressed genes as compared to root flush. Multi-layered defence mechanisms were induced at shoot flush, comprising upregulation of reactive oxygen species formation, hormone signalling (e.g. jasmonic acid synthesis), and proteins involved in the shikimate pathway. In contrast during root flush production of glycerolipids involved in signalling cascades was repressed, suggesting that P. penetrans actively suppressed host defence. With the presence of the mycorrhizal symbiont, the gene expression pattern was vice versa with a distinctly stronger effect of P. penetrans at root flush, including attenuated defence, cell and carbon metabolism, likely a response to the enhanced carbon sink strength in roots induced by the presence of both, nematode and fungus. Meanwhile at shoot flush, when nutrients are retained in aboveground tissue, oak defence reactions, such as altered photosynthesis and sugar pathways, diminished.ConclusionsThe results highlight that gene response patterns of plants to biotic interactions, both negative (i.e. plant-parasitic nematodes) and beneficial (i.e. mycorrhiza), are largely modulated by endogenous rhythmic growth, and that such plant traits should be considered as an important driver of these relationships in future studies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2992-8) contains supplementary material, which is available to authorized users.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Transcriptome analysis in oak uncovers a strong impact of endogenous rhythmic growth on the interaction with plant-parasitic nematodes

et al. 2016

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“…In the future, MyDiv can gain from the integration of other projects, such as the oak phytometer project (PhytOakmeter; Herrmann et al. ) and the global network on tree diversity experiments TreeDivNet (Verheyen et al. ) outlined below, that allow to address more specific or even broader questions.…”

Section: Investigating Links Between Biodiversity and Ecosystem Functmentioning

confidence: 99%

Mycorrhiza in tree diversity–ecosystem function relationships: conceptual framework and experimental implementation

et al. 2018

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The widely observed positive relationship between plant diversity and ecosystem functioning is thought to be substantially driven by complementary resource use of plant species. Recent work suggests that biotic interactions among plants and between plants and soil organisms drive key aspects of resource use complementarity. Here, we provide a conceptual framework for integrating positive biotic interactions across guilds of organisms, more specifically between plants and mycorrhizal types, to explain resource use complementarity in plants and its consequences for plant competition. Our overarching hypothesis is that ecosystem functioning increases when more plant species associate with functionally dissimilar mycorrhizal fungi because differing mycorrhizal types will increase coverage of habitat space for and reduce competition among plants. We introduce a recently established field experiment (MyDiv) that uses different pools of tree species that associate with either arbuscular or ectomycorrhizal fungi to create orthogonal experimental gradients in tree species richness and mycorrhizal associations and present initial results. Finally, we discuss options for future mechanistic studies on resource use complementarity within MyDiv. We show how mycorrhizal types and biotic interactions in MyDiv can be used in the future to test novel questions regarding the mechanisms underlying biodiversity–ecosystem function relationships.

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“…The DF159 oak tree saplings were produced via micropropagation which warrants their common genetic identity (Herrmann et al, 2016), and in November 2014, 2-year PhytOakmeter trees were outplanted in grassland sites. The distance between trees ranges from 6 to 10 m according to individual field plots.…”

Section: Field Sites and Phytoakmetermentioning

confidence: 99%

“…More than 20 years ago, numerous investigations have been made on how oak trees harmonize their own development, biotic interaction and adaptation to the environment. These studies were through microcosm experiments using micro-cuttings of the oak clone DF159 (Quercus robur L.) with different analytic approaches including transcriptomics (Herrmann et al, 1998(Herrmann et al, , 2015(Herrmann et al, , 2016Tarkka et al, 2013). More recently, clonal saplings regenerated from DF159 were planted in TERENO 1 field sites as "phytometers" (Herrmann et al, 2016;Ferlian et al, 2018), i.e., standardized plants transplanted into different environments to serve as 1 www.tereno.net environmental measuring "instruments" (Dietrich, 2013).…”

Section: Introductionmentioning

confidence: 99%

Tree Root Zone Microbiome: Exploring the Magnitude of Environmental Conditions and Host Tree Impact

et al. 2020

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Tree roots attract their associated microbial partners from the local soil community. Accordingly, tree root-associated microbial communities are shaped by both the host tree and local environmental variables. To rationally compare the magnitude of environmental conditions and host tree impact, the "PhytOakmeter" project planted clonal oak saplings (Quercus robur L., clone DF159) as phytometers into different field sites that are within a close geographic space across the Central German lowland region. The PhytOakmeters were produced via micro-propagation to maintain their genetic identity. The current study analyzed the microbial communities in the PhytOakmeter root zone vs. the tree root-free zone of soil two years after out-planting the trees. Soil DNA was extracted, 16S and ITS2 genes were respectively amplified for bacteria and fungi, and sequenced using Illumina MiSeq technology. The obtained microbial communities were analyzed in relation to soil chemistry and weather data as environmental conditions, and the host tree growth. Although microbial diversity in soils of the tree root zone was similar among the field sites, the community structure was site-specific. Likewise, within respective sites, the microbial diversity between PhytOakmeter root and root-free zones was comparable. The number of microbial species exclusive to either zone, however, was higher in the host tree root zone than in the tree root-free zone. PhytOakmeter "core" and "site-specific" microbiomes were identified and attributed to the host tree selection effect and/or to the ambient conditions of the sites, respectively. The identified PhytOakmeter root zone-associated microbiome predominantly included ectomycorrhizal fungi, yeasts and saprotrophs. Soil pH, soil organic matter, and soil temperature were significantly correlated with the microbial diversity and/or community structure. Although the host tree contributed to shape the soil microbial communities, its effect was surpassed by the impact of environmental factors. The current study helps to understand site-specific microbe recruitment processes by young host trees.

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Endogenous rhythmic growth, a trait suitable for the study of interplays between multitrophic interactions and tree development

Cited by 20 publications

References 60 publications

Transcriptome analysis in oak uncovers a strong impact of endogenous rhythmic growth on the interaction with plant-parasitic nematodes

Transcriptome analysis in oak uncovers a strong impact of endogenous rhythmic growth on the interaction with plant-parasitic nematodes

Mycorrhiza in tree diversity–ecosystem function relationships: conceptual framework and experimental implementation

Tree Root Zone Microbiome: Exploring the Magnitude of Environmental Conditions and Host Tree Impact

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