Shoot nitrate status regulates Arabidopsis shoot growth and systemic transcriptional responses via shoot adenylate isopentenyltransferase 3

Plants systemically regulate growth and gene expression according to their internal nitrate status. Our previous study reported that shoot nitrate accumulation increases shoot expression of ADENYLATE ISOPENTENYLTRANSFERASE 3 ( IPT3 ) and shoot levels of N ⁶ -(Δ ² -isopentenyl) adenine (iP)-type cytokinin (CK). IPT3 expression is localized in the phloem, and iP-type CKs, which are synthesized by IPT3, are phloem-mobile. Hence, systemic responses to shoot nitrate status may be regulated by the shoot-expressed IPT3. To examine this, we developed a novel system to manipulate nitrate levels and IPT3 expression in a shoot-specific manner and performed growth analysis, CK determination, and RNA-sequencing. Our results demonstrated that shoot nitrate accumulation increased shoot growth and shoot concentrations of iP-type CKs via shoot IPT3. Transcriptomic responses to shoot nitrate satiety were largely tuned by shoot IPT3, with opposite effects in shoots and roots. Shoot IPT3 amplified shoot responses of nitrate-inducible genes and immune response genes to shoot nitrate accumulation, while dampened root responses of nitrate transport/assimilation genes. This transcriptomic modulation via shoot IPT3 was accompanied by coherent transcriptional changes in genes encoding mobile peptides and transcriptional repressors. Here we present a novel scheme integrating shoot nitrate satiety responses with CK signaling.