AT-Hook Transcription Factors Restrict Petiole Growth by Antagonizing PIFs

• Published in: Current biology 2020-04, Vol.30 (8), p.1454-1466.e6
• Main Authors: Favero, David S., Kawamura, Ayako, Shibata, Michitaro, Takebayashi, Arika, Jung, Jae-Hoon, Suzuki, Takamasa, Jaeger, Katja E., Ishida, Takashi, Iwase, Akira, Wigge, Philip A., Neff, Michael M., Sugimoto, Keiko
• Format: Article
• Language: English
• Subjects: ACS; AHL; ATHB2; auxin; brassinosteroids; ESC; ethylene; phytochrome interacting factor; plant growth; SOB3
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.02.017

Upon detecting abiotic or biotic stress, plants generally reduce their growth, enabling resources to be conserved and diverted to stress response mechanisms. In Arabidopsis thaliana, the AT-hook motif nuclear-localized (AHL) transcription factor family has been implicated in restricting rosette growth in response to stress. However, the mechanism by which AHLs repress growth in rosettes is unknown. In this study, we establish that SUPPRESSOR OF PHYTOCHROME B4-#3 (SOB3) and other AHLs restrict petiole elongation by antagonizing the growth-promoting PHYTOCHROME-INTERACTING FACTORs (PIFs). Our data show that high levels of SOB3 expression lead to a short-petiole phenotype similar to that conferred by removal of PIF4. Conversely, the dominant-negative sob3-6 mutant has long petioles, a phenotype which is PIF-dependent. We further show that AHLs repress the expression of many PIF-activated genes, several of which are involved in hormone-mediated promotion of growth. Additionally, a subset of PIF-activated, AHL-repressed genes are directly bound by both SOB3 and PIFs. Finally, SOB3 reduces binding of PIF4 to shared target loci. Collectively, our results demonstrate that AHLs repress petiole growth by antagonizing PIF-mediated transcriptional activation of genes associated with growth and hormone pathways. By elucidating a mechanism via which the stress-responsive AHL transcription factor family influences growth in petioles, this study identifies a key step in the gene regulatory network controlling leaf growth in response to the environment. [Display omitted] •AHL transcription factors repress petiole elongation in juvenile rosettes•The effect of AHLs on petiole growth is dependent on PIFs•AHLs bind to and repress the expression of genes directly activated by PIFs•PIF binding to target genes is reduced by ectopic AHL expression Favero et al. demonstrate that the AHL transcription factors repress leaf petiole elongation by antagonizing key regulators of plant growth, the PIFs. AHLs bind to PIF-targeted loci and reduce PIF binding to these regions, thus inhibiting transcriptional activation of growth-promoting genes.