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

ABSTRACT 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.