title: Transcriptome analysis in oak uncovers a strong impact of endogenous rhythmic growth on the interaction with plant-parasitic nematodes.
abstract: Pedunculate 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.
  
  
  
  The 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.
  
  
  
  The 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.
authors: Institute of Biology, Ecology Group, Humboldt-Universität zu Berlin, Philippstr. 13, 10115, Berlin, Germany. maborekh@hu-berlin.de.
authors: Hazel R
authors: HR
authors: Maboreke
authors: Department of Soil Ecology, UFZ - Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany.
authors: Lasse
authors: L
authors: Feldhahn
authors: Department of Soil Ecology, UFZ - Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany.
authors: Markus
authors: M
authors: Bönn
authors: Department of Soil Ecology, UFZ - Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany.|German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany.
authors: Mika T
authors: MT
authors: Tarkka
authors: Department of Soil Ecology, UFZ - Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany.|German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany.
authors: Francois
authors: F
authors: Buscot
authors: Department of Soil Ecology, UFZ - Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany.|Department of Community Ecology, UFZ - Helmholtz Centre for Environmental Research, Theodor-Lieser-Str. 4, 06120, Halle/Saale, Germany.|German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany.
authors: Sylvie
authors: S
authors: Herrmann
authors: Institute of Biology, Ecology Group, Humboldt-Universität zu Berlin, Philippstr. 13, 10115, Berlin, Germany.
authors: Ralph
authors: R
authors: Menzel
authors: Institute of Biology, Ecology Group, Humboldt-Universität zu Berlin, Philippstr. 13, 10115, Berlin, Germany.
authors: Liliane
authors: L
authors: Ruess
mesh_terms: D000818:Animals; D015536:Down-Regulation; D020869:Gene Expression Profiling; D006790:Host-Parasite Interactions / Q000235:genetics*; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D018520:Plant Shoots / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D029963:Quercus / Q000235:genetics* / Q000254:growth & development / Q000469:parasitology*; D018749:RNA, Plant / Q000302:isolation & purification / Q000378:metabolism; D017382:Reactive Oxygen Species / Q000378:metabolism; D059467:Transcriptome; D014431:Tylenchoidea / Q000502:physiology*; D015854:Up-Regulation
chemical_list: D018749:RNA, Plant; D017382:Reactive Oxygen Species
keywords: Defence; Ectomycorrhiza; Oak rhythmic growth; Plant-parasitic nematode; Systemic response; Transcriptomic profile