SummaryOaks (Quercus spp.), which are major forest trees in the northern hemisphere, host many biotic interactions, but molecular investigation of these interactions is limited by fragmentary genome data. To date, only 75 oak expressed sequence tags (ESTs) have been characterized in ectomycorrhizal (EM) symbioses.We synthesized seven beneficial and detrimental biotic interactions between microorganisms and animals and a clone (DF159) of Quercus robur. Sixteen 454 and eight Illumina cDNA libraries from leaves and roots were prepared and merged to establish a reference for RNASeq transcriptomic analysis of oak EMs with Piloderma croceum.Using the Mimicking Intelligent Read Assembly (MIRA) and Trinity assembler, the OakContigDF159.1 hybrid assembly, containing 65 712 contigs with a mean length of 1003 bp, was constructed, giving broad coverage of metabolic pathways. This allowed us to identify 3018 oak contigs that were differentially expressed in EMs, with genes encoding proline-rich cell wall proteins and ethylene signalling-related transcription factors showing up-regulation while auxin and defence-related genes were down-regulated.In addition to the first report of remorin expression in EMs, the extensive coverage provided by the study permitted detection of differential regulation within large gene families (nitrogen, phosphorus and sugar transporters, aquaporins). This might indicate specific mechanisms of genome regulation in oak EMs compared with other trees.

HighlightIncreased resource availability has no impact on endogenous rhythmic growth and related allocation shifts in oak trees; an internal clock regulates core genes during shoot and root growth cessation phases.

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SummaryThe root-rot pathogen Phytophthora quercina is a key determinant of oak decline in Europe. The susceptibility of pedunculate oak (Quercus robur) to this pathogen has been hypothesized to depend on the carbon availability in roots as an essential resource for defense.Microcuttings of Q. robur undergo an alternating rhythm of root and shoot growth. Inoculation of mycorrhizal (Piloderma croceum) and nonmycorrhizal oak roots with P. quercina was performed during both growth phases, that is, root flush (RF) and shoot flush (SF). Photosynthetic and morphological responses as well as concentrations of nonstructural carbohydrates (NSC) were analyzed. Infection success was quantified by the presence of pathogen DNA in roots.Concentrations of NSC in roots depended on the alternating root/shoot growth rhythm, being high and low during RF and SF, respectively. Infection success was high during RF and low during SF, resulting in a significantly positive correlation between pathogen DNA and NSC concentration in roots, contrary to the hypothesis.The alternating growth of roots and shoots plays a crucial role for the susceptibility of lateral roots to the pathogen. NSC availability in oak roots has to be considered as a benchmark for susceptibility rather than resistance against P. quercina.

Endogenous rhythmic growth (ERG) is displayed by many tropical and some major temperate tree species and characterized by alternating root and shoot flushes (RF and SF). These flushes occur parallel to changes in biomass partitioning and in allocation of recently assimilated carbon and nitrogen. To address how biotic interactions interplay with ERG, we cross-compared the RF/SF shifts in oak microcuttings in the presence of pathogens, consumers and a mycorrhiza helper bacterium, without and with an ectomycorrhizal fungus (EMF), and present a synthesis of the observations. The typical increase in carbon allocation to sink leaves during SF did not occur in the presence of root or leaf pathogens, and the increase in nitrogen allocation to lateral roots during RF did not occur with the pathogens. The RF/SF shifts in resource allocation were mostly restored upon additional interaction with the EMF. Its presence led to increased resource allocation to principal roots during RF, also when the oaks were inoculated additionally with other interactors. The interactors affected the alternating, rhythmic growth and resource allocation shifts between shoots and roots. The restoring role of the EMF on RF/SF changes in parallel to the corresponding enhanced carbon and nitrogen allocation to sink tissues suggests that the EMF is supporting plants in maintaining the ERG.