Photoexcited CRYPTOCHROME1 Interacts with Dephosphorylated BES1 to Regulate Brassinosteroid Signaling and Photomorphogenesis in Arabidopsis

Abstract

Cryptochromes (CRYs) are blue light photoreceptors that mediate a variety of light responses in plants and animals, including photomorphogenesis, flowering, and circadian rhythms. The signaling mechanism by which Arabidopsis thaliana cryptochromes CRY1 and CRY2 promote photomorphogenesis involves direct interactions with COP1, a RING motifcontaining E3 ubiquitin ligase, and its enhancer SPA1. Brassinosteroid (BR) is a key phytohormone involved in the repression of photomorphogenesis, and here, we show that the signaling mechanism of Arabidopsis CRY1 involves the inhibition of BR signaling. CRY1 and CRY2 physically interact with BES1-INTERACTING MYC-LIKE1 (BIM1), a basic helix-loop-helix protein. BIM1, in turn, interacts with and enhances the activity of BRI1-EMS SUPPRESSOR1 (BES1), a master transcription factor in the BR signaling pathway. In addition, CRY1 and CRY2 interact specifically with dephosphorylated BES1, the physiologically active form of BES1 that is activated by BR in a blue light-dependent manner. The CRY1-BES1 interaction leads to both the inhibition of BES1 DNA binding activity and the repression of its target gene expression. Our study suggests that the blue light-dependent, BR-induced interaction of CRY1 with BES1 is a tightly regulated mechanism by which plants optimize photomorphogenesis according to the availability of external light and internal BR signals.

UV‐B photoreceptor UVR8 interacts with MYB73/MYB77 to regulate auxin responses and lateral root development

“…As UVR8 can interact directly with several transcription factors (e.g., BES1, BIM1, WRKY36, MYB73, and MYB77) and thus mediate UV-B-regulated gene expression, UVR8 could also regulate the expression of the transcription factor gene HY5 to mediate UV-B-regulated gene expression. Liang et al (2018) and Wang et al (2018) established the molecular basis of cross-talk between UV-B light or blue light and brassinosteroid (BR) signaling. Nucleus-localized UVR8 interacts with BR-activated dephosphorylated BES1 and BIM1 in a UV-B-independent manner, while CRYs interact with dephosphorylated BES1 and BIM1 in a blue-light-dependent manner, repressing their DNAbinding activity and also the expression of elongation genes (Liang et al, 2018;Wang et al, 2018).…”

Molecular Mechanisms of Brassinosteroid-Mediated Responses to Changing Environments in Arabidopsis

“…A group of SINAT E3 ligases, on the contrary, are involved in degrading nonphosphorylated BES1 protein in the light [86]. In addition to light-controlled protein abundance of BES1 and BZR1, recent studies demonstrated that light negatively regulates the transcriptional activity of BES1 and BZR1 [88][89][90]92]. When illuminated by red and blue light, respectively, phytochrome B (phyB) and cryptochrome 1 (CRY1) interact specifically with nonphosphorylated BES1 and BZR1.…”

“…When illuminated by red and blue light, respectively, phytochrome B (phyB) and cryptochrome 1 (CRY1) interact specifically with nonphosphorylated BES1 and BZR1. This light-dependent interaction leads to the inhibition of BES1 and BZR1 DNA-binding activity and ultimately the expression of their target genes [88][89][90]92]. Moreover, blue light-activated CRY1 also interacts with BIN2 and thus enhances the interaction between BIN2 and BZR1.…”

“…At the transcription level, it has been reported that PP2A phosphatases can promote BR signaling by dephosphorylating BES1 and BZR1, whereas 14-3-3 and BRZ-SENSITIVE-SHORT HYPOCOTYL1 (BSS1) negatively regulate BR signaling by inhibiting the translocation of BES1 and BZR1 from the cytosol to the nucleus [81][82][83]. Besides, protein degradation of BES1 and/or BZR1 has been reported to be regulated by many factors, including an F-box protein MORE AXILLARY GROWTH LOCUS2 (MAX2), ubiquitin E3 ligases such as PLANT U-BOX40 (PUB40), CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1) and SINA of Arabidopsis thaliana (SINATs), photoreceptors such as UV RESISTANCE LOCUS 8 (UVR8), CRYPTOCHROME1 (CRY1) and PHYTOCHROME B (PHYB), and an autophagy receptor DOMINANT SUPPRESSOR OF KAR2 (DSK2) [84][85][86][87][88][89][90][91][92][93]. Moreover, BES1 and BZR1 were reported to be oxidized by ROS (e.g., H 2 O 2 ) and reduced by a thioredoxin TRXh5 [94].…”

In Arabidopsis, low blue light enhances phototropism by releasing cryptochrome 1-mediated inhibition ofPIF4expression

“…Phenotypical experiments of seedlings defective for another class of blue light photoreceptors, called cryptochromes (cry), revealed that they modulate phototropism with a positive role in etiolated seedlings (Whippo and Hangarter, 2003; Ohgishi et al, 2004; Tsuchida-Mayama et al, 2010), and a potentially negative role in de-etiolated seedlings (Goyal et al, 2016). The Arabidopsis genome encodes two crys, cry1 and cry2, which coordinate blue light-mediated gene expression by the inactivation of the COP1/SPA E3 ligase complex (Holtkotte et al, 2017; Lau et al, 2019; Ponnu et al, 2019) or through the interaction with several transcription factors (Liu et al, 2008; Ma et al, 2016; Pedmale et al, 2016; Wang et al, 2018; Xu et al, 2018; He et al, 2019; Mao et al, 2020). Light-induced activation of cry1 and cry2 is controlled by BIC1 (Blue light Inhibitor of Cryptochrome 1) and BIC2 (Wang et al, 2016).…”