Nitrogen deprivation promotes Populus root growth through global transcriptome reprogramming and activation of hierarchical genetic networks.

We show a distinct and previously poorly characterized response of poplar (Populus tremula × Populus alba) roots to low nitrogen (LN), which involves activation of root growth and significant transcriptome reprogramming. Analysis of the temporal patterns of enriched ontologies among the differentially expressed genes revealed an ordered assembly of functionally cohesive biological events that aligned well with growth and morphological responses. A core set of 28 biological processes was significantly enriched across the whole studied period and 21 of these were also enriched in the roots of Arabidopsis thaliana during the LN response. More than half (15) of the 28 processes belong to gene ontology (GO) terms associated with signaling and signal transduction pathways, suggesting the presence of conserved signaling mechanisms triggered by LN. A reconstruction of genetic regulatory network analysis revealed a sub-network centered on a PtaNAC1 (P. tremula × alba NAM, ATAF, CUC 1) transcription factor. PtaNAC1 root-specific up-regulation increased root biomass and significantly changed the expression of the connected hub genes specifically under LN. Our results provide evidence that the root response to LN involves hierarchically structured genetic networks centered on key regulatory factors. Targeting these factors via genetic engineering or breeding approaches can allow dynamic adjustment of root architecture in response to variable nitrogen availabilities in the soil.