A dose-dependent bimodal switch by homologous Aux/IAA transcriptional repressors

• Published in: Molecular plant 2024-09, Vol.17 (9), p.1407-1422
• Main Authors: Cho, Hyung-Taeg, Lee, Minsu, Choi, Hee-Seung, Maeng, Kwang-Ho, Lee, Kyeonghoon, Lee, Ha-Yeon, Ganguly, Anindya, Park, Hoonyoung, Ho, Chang-Hoi
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Aux/IAA; auxin; dose-dependent regulation; Gene Expression Regulation, Plant; Indoleacetic Acids - metabolism; Plant Roots - growth & development; Plant Roots - metabolism; Repressor Proteins - genetics; Repressor Proteins - metabolism; root hair; TOPLESS (TPL); transcription; Transcription, Genetic
• ISSN: 1674-2052; 1752-9867; 1752-9867
• DOI: 10.1016/j.molp.2024.07.014

Combinatorial interactions between different regulators diversify and enrich the chance of transcriptional regulation in eukaryotic cells. However, a dose-dependent functional switch of homologous transcriptional repressors has rarely been reported. Here, we show that SHY2, an auxin/indole-3-acetic acid (Aux/IAA) repressor, exhibits a dose-dependent bimodal role in auxin-sensitive root-hair growth and gene transcription in Arabidopsis, whereas other Aux/IAA homologs consistently repress the auxin responses. The co-repressor (TOPLESS [TPL])-binding affinity of a bimodal Aux/IAA was lower than that of a consistently repressing Aux/IAA. The switch of a single amino acid residue in the TPL-binding motif between the bimodal form and the consistently repressing form switched their TPL-binding affinity and transcriptional and biological roles in auxin responses. Based on these data, we propose a model whereby competition between homologous repressors with different co-repressor-binding affinities could generate a bimodal output at the transcriptional and developmental levels. Aux/IAA proteins, repressors in the auxin signaling pathway, exhibit varying affinities for the co-repressor TPL based on the EAR-motif syntax. Aux/IAAs with weaker TPL affinities function as dose-dependent bimodal switches, modulating their transcriptional and biological activities accordingly.