Pluripotent Pericycle Cells Trigger Different Growth Outputs by Integrating Developmental Cues into Distinct Regulatory Modules

Abstract

During post-embryonic development, the pericycle specifies the stem cells that give rise to both lateral roots (LRs) and periderm, the suberized barrier that protects the plant against biotic and abiotic stresses. Comparable auxin-mediated signaling hubs regulate meristem establishment in many developmental contexts, however it is unknown how specific outputs are achieved. Using the Arabidopsis root as a model, we show that while LR formation is the preset auxin-induced program, plants with age become competent to form a periderm in response to auxin. The establishment of the vascular cambium acts as the developmental switch required to trigger auxin-mediated periderm initiation. Moreover, distinct auxin signaling components and targets control LR versus periderm formation. Among the periderm specific promoting transcription factors, WUSCHEL-RELATED HOMEOBOX 4 (WOX4) and KNAT1/ BREVIPEDICELLUS (BP) stand out as their specific overexpression in the periderm results in an increased number of periderm layers, a trait of agronomical importance in breeding programs targeting stress tolerance. Altogether these findings reveal that specificity in pericycle stem cell fate is achieved by the integration of developmental cues into distinct regulatory modules.