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

Abstract

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.

Keywords: Defence; Ectomycorrhiza; Oak rhythmic growth; Plant-parasitic nematode; Systemic response; Transcriptomic profile.

Fig. 1

Venn diagram illustrating the numbers of significant differentially expressed contigs (DECs). Overlapping areas represent DECs common to different inoculation treatments. The figure compares the following pairs of oak microcuttings during root flush and shoot flush: Control versus Pratylenchus penetrans (Co-Pp), Control versus Piloderma croceum (Co-Pc) and Control versus sequential-inoculation of P. penetrans and P. croceum (Co-PpPc). FDR cut-off = 0.01

Fig. 2

Visualization of summarized enriched GO terms expressed in systemic tissue of oak microcuttings in response to inoculation with Pratylenchus penetrans at root flush (RF); a GO terms with a biological process role enriched for 24 upregulated contigs; b GO terms with a molecular function role enriched for 16 upregulated contigs; c GO terms with a biological process role enriched for 25 downregulated contigs; d GO terms with a molecular function role enriched for 24 downregulated contigs

Fig. 3

Visualization of summarized enriched GO terms expressed in systemic tissue of oak microcuttings in response to inoculation with Pratylenchus penetrans at shoot flush (SF); a GO terms with a biological process role enriched for 68 upregulated contigs; b GO terms with a molecular function role enriched for 60 upregulated contigs; c GO terms with a biological process role enriched for 178 downregulated contigs; d GO terms with a molecular function role enriched for 102 downregulated contigs

Fig. 4

Visualization of summarized enriched GO terms expressed in systemic tissue of oak microcuttings in response to the co-inoculation of Pratylenchus penetrans and Piloderma croceum at root flush (RF); a GO terms with a biological process role enriched for 99 upregulated contigs; b GO terms with a molecular function role enriched for 61 upregulated contigs; c GO terms with a biological process role enriched for 68 downregulated contigs; d GO terms with a molecular function role enriched for 71 downregulated contigs

Fig. 5

Visualization of summarized enriched Go terms expressed in systemic tissue of oak microcuttings in response to the co-inoculation of Pratylenchus penetrans and Piloderma croceum at shoot flush (SF); a GO terms with a biological process role enriched for 36 upregulated contigs; b GO terms with a molecular function role enriched for 22 upregulated contigs; c GO terms with a biological process role enriched for 41 downregulated contigs; d GO terms with a molecular function role enriched for 29 downregulated contigs