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

Abstract

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.

Local Responses and Systemic Induced Resistance Mediated by Ectomycorrhizal Fungi

“…These studies suggest that the resistance induced by EMF is context-dependent. This idea is also supported by recent transcriptome analyses showing that host defense gene expression of leaves can be diminished when the tree roots are colonized by EMF and depends on the specific host-EMF combination (Maboreke et al, 2016;Bacht et al, 2019;Bouffaud et al, 2020).…”

Transcriptomic profiling of Solanum peruvianum LA3858 revealed a Mi-3-mediated hypersensitive response to Meloidogyne incognita

“…Most of the DEGs were enriched (P ≤ 0.05) in the cellular component category and were involved in the "cell", "cell part", "membrane", and "organelle" terms. The significantly enriched terms (P ≤ 0.05) in the molecular function category were "binding", "catalytic activity" and "transporter activity", and the enriched terms The expression level of each gene (the entire gene set) for each pair of samples was used to calculate the Pearson correlation coefficients, and the correlation coefficients between the two samples were visually displayed as a heat map (P ≤ 0.05) in the biological process category included "biological regulation", "cellular process", "metabolic process", and "response to stimulus and signaling", which were related to disease resistance [13] ( Figure S1). Notably, in the HS3 vs. HR3 comparison, many key KEGG pathways related to biotic stress were significantly enriched (P ≤ 0.05), including "plant-pathogen interaction" (16 DEGs), "plant hormone signal transduction" (16 DEGs), and "brassinosteroid biosynthesis" (3) (Fig.…”

Micro-Food Web Structure Shapes Rhizosphere Microbial Communities and Growth in Oak

“…For perennial woody plants, P. penetrans was reported to stimulate microbial growth in the rhizosphere of oak [25], predominantly due to a promotion of plant carbon flow belowground [26]. On the other hand, transcriptome analyses revealed P. penetrans to act as a strong root carbon sink leading to resource competition with the oak's ectomycorrhizal symbiont P. croceum [54]. Taking into account the worldwide occurrence of this taxon, and its broad host range, underpins its importance in regulating microbial communities, and moreover plant symbiotic relationships, not only in the rhizosphere of crop plants but also in forest trees [35].…”