The GUN1-NAC103 axis-mediated plastid signaling sustains root growth under plastid translation stress

Plastid signaling orchestrates nuclear gene expression to synchronize cellular responses with diverse developmental and functional states of plastids. While the mechanism has been well studied in photosynthetic tissues, the physiological role and regulatory mechanism of plastid signaling in nonphotosynthetic tissues remain poorly understood. GENOME UNCOUPLED 1 (GUN1) is a key mediator of plastid signaling in photosynthetic tissues. Here, we demonstrate that GUN1 is also involved in plastid signaling in roots when plastid translation is influenced by impaired translation elongation factor Tu activity or ribosome inhibition in Arabidopsis. Upon plastid translation stress, GUN1-dependent signaling promotes the protein stabilization of the NAC transcription factor NAC103 specifically in the root transition zone. NAC103 conducts metabolism-related regulation, ensuring de novo fatty acid biosynthesis by directly activating the gene encoding ACETYL-CoA CARBOXYLASE 2 (ACC2) but repressing genes involved in tryptophan-related metabolism. This coordinated gene reprogramming, particularly the activation of ACC2, is indispensable for sustaining cell viability in the transition zone. We further characterized that the GUN1-NAC103-ACC2 signaling is involved in root growth adaptation under iron-deficient stress. Overall, we identified a GUN1-NAC103 signaling axis required for sustaining root growth under plastid translation stress, distinct from signaling responses characterized in photosynthetic tissues.