Salt stress disrupts local auxin and COP1 gradients in Arabidopsis apical hooks

Abstract

Seedling establishment is highly sensitive to environmental cues, with light serving as a principal regulator. In darkness, seedlings enter skotomorphogenesis, marked by hypocotyl elongation and apical hook formation, which helps seedlings emerge from the soil to reach the light. Here, we show that salinity impairs soil emergence of Arabidopsis thaliana seedlings by inducing a partially photomorphogenic like phenotype in darkness, characterized by reduced apical hook curvature. Within the hook, salt stress diminished differential epidermal cell elongation required to drive hook bending, and reduced both the auxin signalling maximum and PIN3 abundance on the concave side of the hook. Transcriptome analysis revealed that salt and osmotic stresses directly alter organ-specific transcriptional profiles, including the NaCl-mediated repression of B-BOX DOMAIN PROTEIN 28 (BBX28) in hooks and cotyledons. Under control conditions, BBX28 protein accumulated asymmetrically across the hook, but this pattern was lost under salinity. Notably, the ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) exhibited an opposite gradient to BBX28, which was similarly disrupted by salt stress or by the inhibition of polar auxin transport, presenting auxin as an upstream regulator of COP1 spatial distribution. Together, these findings establish COP1 asymmetry as a novel feature of the apical hook, indicating that spatial regulation--not just absolute levels--shapes COP1 function, and reveal how salinity disrupts hormonal, transcriptional and protein networks to compromise seedling establishment under stress. Significance StatementSeedling establishment is a critical developmental transition that contributes to survival in the local environment. While light is the primary cue driving de-etiolation, how abiotic stress shapes early development in darkness remains unclear. We show that salinity induces a photomorphogenic-like response in dark-grown Arabidopsis thaliana seedlings, disrupting apical hook formation and soil emergence. This response involves disrupted asymmetrical epidermal cell elongation and auxin signalling, repression of B-BOX DOMAIN PROTEIN 28 (BBX28), and loss of a previously unrecognized spatial gradient of the key light regulator COP1 across the apical hook. Our discovery that COP1 is spatially regulated and disrupted by stress, reveals a new dimension of light signalling and developmental control, highlighting how environmental stress constrains seedling establishment.