Perturbations in plant energy homeostasis prime lateral root initiation via SnRK1-bZIP63-ARF19 signaling

Plant architecture is highly plastic and known to respond sensitively to nutritional changes. Although of great agronomic importance, the underlying molecular mechanisms that sense and transduce these cues into plant development and growth are poorly understood. Applying diverse genetic, biochemical, and microscopic approaches, we disclosed that signaling via the central, evolutionarily conserved fuel-sensor kinase Snf1-RELATED KINASE1 (SnRK1) initiates lateral root (LR) primordia formation in response to transient metabolic perturbations. This is accomplished by SnRK1-mediated activation of a signaling cascade involving the pivotal LR regulator AUXIN RESPONSE FACTOR19 (ARF19). We propose that this developmental priming strategy represents a cost-efficient approach to ensure rapid growth recovery after stress release, providing in competitive ecosystems a clear advantage in terms of Darwinian fitness.Plants adjust their energy metabolism to continuous environmental fluctuations, resulting in a tremendous plasticity in their architecture. The regulatory circuits involved, however, remain largely unresolved. In Arabidopsis, moderate perturbations in photosynthetic activity, administered by short-term low light exposure or unexpected darkness, lead to increased lateral root (LR) initiation. Consistent with expression of low-energy markers, these treatments alter energy homeostasis and reduce sugar availability in roots. Here, we demonstrate that the LR response requires the metabolic stress sensor kinase Snf1-RELATED-KINASE1 (SnRK1), which phosphorylates the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) that directly binds and activates the promoter of AUXIN RESPONSE FACTOR19 (ARF19), a key regulator of LR initiation. Consistently, starvation-induced ARF19 transcription is impaired in bzip63 mutants. This study highlights a positive developmental function of SnRK1. During energy limitation, LRs are initiated and primed for outgrowth upon recovery. Hence, this study provides mechanistic insights into how energy shapes the agronomically important root system.All study data are included in the article and/or supporting information.