LBD-type transcription factors suppress local and systemic nitrogen responses through distinct regulatory pathways

<jats:p> Nitrogen (N) is a major determinant of plant growth and productivity. Because soil N availability and internal N demand fluctuate, plants have evolved sophisticated mechanisms to coordinate N acquisition and utilization at the whole-plant level. However, how this coordination is achieved remains poorly understood. Here, we show that N-inducible LATERAL ORGAN BOUNDARIES DOMAIN transcription factors LBD37, LBD38, and LBD39 (LBDs) function as repressors of local N uptake and assimilation and systemic N-demand signaling in Arabidopsis. Triple mutants lacking these three LBDs displayed enhanced nitrate influx and increased accumulation of nitrate, amino acids, and total N. Transcriptome analysis identified an array of N-starvation- and nitrate-inducible genes derepressed in shoots and roots, including <jats:italic>C-TERMINALLY ENCODED PEPTIDE</jats:italic> ( <jats:italic>CEP</jats:italic> ) and <jats:italic>CEP DOWNSTREAM</jats:italic> ( <jats:italic>CEPD</jats:italic> ) genes, as well as genes involved in N uptake and assimilation. Grafting and genetic analyses revealed that LBDs gate the systemic N-demand signaling relay by repressing <jats:italic>CEP</jats:italic> and <jats:italic>CEPD</jats:italic> expression organ-autonomously. We also found that LBDs locally repress genes involved in N uptake and assimilation through a distinct regulatory mechanism. We propose that LBDs are key transcriptional repressors in a regulatory framework for optimizing N acquisition and utilization under fluctuating N conditions at the whole-plant level. </jats:p>