SIZ1-Mediated SUMOylation of LBD29 Recruits ARF7 to Fine-Tune Auxin Signaling in Lateral Root Development

Auxin signaling orchestrates plant development through TRANSPORT INHIBITOR RESPONSE 1 (TIR1)/AUXIN-SIGNALING F-BOXs (AFBs)-dependent nuclear auxin signaling pathway and emerging posttranslational modification (PTM) mechanisms. Here, we identify Small Ubiquitin-like Modifier (SUMO) E3 ligase SAP AND MIZ1 DOMAIN-CONTAINING LIGASE 1 (SIZ1)-mediated SUMOylation as a critical regulator of auxin signaling. Auxin strongly induces SIZ1-mediated SUMOylation, which reshapes the SIZ1 interactome and modulates large-scale protein interactions. Transcriptome analysis shows that nearly 40% of Col-0-specific auxin-responsive genes depend on SIZ1, and integrated RNA sequencing and immunoprecipitation-mass spectrometry reveal 103 genes that are co-regulated at the transcriptional and protein levels. Among SUMOylation targets, the transcription factor LATERAL ORGAN BOUNDARIES DOMAIN 29 (LBD29) plays a key role in auxin-mediated lateral root formation. SUMOylation promotes LBD29 - AUXIN RESPONSE FACTOR 7 (ARF7) interaction, stabilizing a transcriptional activation complex that enhances downstream gene expression. Consistently, both siz1-2 and siz1-3 mutants show reduced auxin responsiveness and impaired lateral root development. Furthermore, SIZ1 transcription is induced by auxin in an ARF7-dependent manner, establishing a feedback loop. These findings establish a mechanistic framework in which SIZ1-mediated SUMOylation links LBD29 function with ARF7-dependent transcription, integrating PTM regulation into the auxin signaling network during lateral root development. This study highlights how dynamic protein modifications fine-tune auxin signaling to coordinate developmental plasticity.