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

BACKGROUND: 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. RESULTS: 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. CONCLUSIONS: 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.

Ectomycorrhizal fungus supports endogenous rhythmic growth and corresponding resource allocation in oak during various below- and aboveground biotic interactions.

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.