Brassinosteroids promote etiolated apical structures in darkness by amplifying the ethylene response via the EBF-EIN3/PIF3 circuit

Abstract

Germinated plants grow in darkness until they emerge above the soil. To help the seedling penetrate the soil, most dicot seedlings develop an etiolated apical structure consisting of an apical hook and folded, unexpanded cotyledons atop a rapidly elongating hypocotyl. Brassinosteroids (BRs) are necessary for etiolated apical development, but their precise role and mechanisms remain unclear. Arabidopsis thaliana SMALL AUXIN UP RNA17 (SAUR17) is an apical-organ-specific regulator that promotes production of an apical hook and closed cotyledons. In darkness, ethylene and BRs stimulate SAUR17 expression by transcription factor complexes containing PHYTOCHROME-INTERACTING FACTORs (PIFs), ETHYLENE INSENSITIVE 3 (EIN3) and its homolog EIN3-LIKE 1 (EIL1), and BRASSINAZOLE RESISTANT1 (BZR1). BZR1 requires EIN3 and PIFs for enhanced DNA-binding and transcriptional activation of the SAUR17 promoter; while EIN3, PIF3 and PIF4 stability depends on BR signaling. BZR1 transcriptionally downregulates EIN3-BINDING F-BOX 1 and 2 (EBF1 and EBF2, which encode ubiquitin ligases mediating EIN3 and PIF3 protein degradation. By modulating the EBF-EIN3/PIF protein-stability circuit, BRs induce EIN3 and PIF3 accumulation, which underlies BR-responsive expression of SAUR17 and HOOKLESS1 and ultimately apical hook development. We suggest that in the etiolated development of apical structures, BRs primarily modulate plant sensitivity to darkness and ethylene.

To curve for survival: Apical hook development

“…In addition to ethylene, brassinosteroid (BR) and GA are another two hook‐promoting phytohormones (Chory et al, 1991; Kauschmann et al, 1996; Vriezen et al, 2004; De Grauwe et al, 2007; Gallego‐Bartolome et al, 2011; An et al, 2012; Smet et al, 2014; Zhao et al, 2021). The key transcriptional factor of BR signaling, BRASSINAZOLE‐RESISTANT 1 (BZR1), physically interacts with EIN3 and PIFs to co‐activate the expression of HLS1 and SAUR17 by directly binding to their promoters (Zhao et al, 2021; Wang et al, 2022). BZR1 also promotes the protein accumulation of EIN3 and PIFs through repressing the transcription of EBF1/2 (Wang et al, 2022).…”

Jasmonates regulate apical hook development by repressing brassinosteroid biosynthesis and signaling

“…In addition, it was reported that BRs are able to collaborate with ethylene and light signaling to regulate apical hook development ( Gendron et al 2008 ; Smet et al 2014 ). BZR1 directly interacts with ETHYLENE-INSENSITIVE 3 (EIN3) to promote the expression of HLS1 and SMALL AUXIN UPREGULATED RNA 17 ( SAUR17 ; Zhao et al 2021 ; Wang, Sun, et al 2023 ). BZR1 can also interact with PHYTOCHROME INTERACTING FACTOR 3 (PIF3) to increase the expression of SAUR17 ( Wang, Sun, et al 2023 ).…”

“…BZR1 directly interacts with ETHYLENE-INSENSITIVE 3 (EIN3) to promote the expression of HLS1 and SMALL AUXIN UPREGULATED RNA 17 ( SAUR17 ; Zhao et al 2021 ; Wang, Sun, et al 2023 ). BZR1 can also interact with PHYTOCHROME INTERACTING FACTOR 3 (PIF3) to increase the expression of SAUR17 ( Wang, Sun, et al 2023 ). Previous studies also indicated that BZR1 can repress the expression of EIN3-BINDING F BOX PROTEIN 1 ( EBF1 ), affecting the accumulation of BZR1, EIN3, and PIF3 ( Zhao et al 2022 ; Wang, Sun, et al 2023 ).…”

“…BZR1 can also interact with PHYTOCHROME INTERACTING FACTOR 3 (PIF3) to increase the expression of SAUR17 ( Wang, Sun, et al 2023 ). Previous studies also indicated that BZR1 can repress the expression of EIN3-BINDING F BOX PROTEIN 1 ( EBF1 ), affecting the accumulation of BZR1, EIN3, and PIF3 ( Zhao et al 2022 ; Wang, Sun, et al 2023 ). JAs, on the other hand, play an opposite role in regulating apical hook development.…”

UPL3 Promotes BZR1 Degradation, Growth Arrest, and Seedling Survival under Starvation Stress inArabidopsis

“…For example, BZR1 plays an essential role in skotomorphogenesis and cell elongation responses to auxin, gibberellin, and darkness, through interactions with AUXIN RESPONSE FACTOR 6 (ARF6), the gibberellin-signaling component DELLA, and PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) (Bai et al, 2012; Oh et al, 2012; Oh et al, 2014). BZR1 regulates apical hook development and cotyledon greening by interacting with SMALL AUXIN UP RNA17 (SAUR17), PIFs, ETHYLENE INSENSITIVE 3 (EIN3), and EIN3-LIKE 1 (EIL1) and GROWTH REGULATING FACTOR 7 (GRF7) (Li and He, 2016; Wang et al, 2020; Zhao et al, 2021; Wang et al, 2023). BZR1 and BZR2/BES1 mediate hypocotyl elongation responses to UV and blue light by interacting with the photoreceptors UV RESISTANCE 8 (UVR8) and CRYPTOCHROME 1 (CRY1) (Liang et al, 2018; He et al, 2019).…”