Arabidopsis cryptochrome 1 undergoes COP1 and LRBs‐dependent degradation in response to high blue light

Abstract

Arabidopsis cryptochrome 1 (CRY1) is an important blue light photoreceptor that promotes photomorphogenesis under blue light. The blue light photoreceptors CRY2 and phototropin 1, and the red/far-red light photoreceptors phytochromes B and A undergo degradation in response to blue and red light, respectively. This study investigated whether and how CRY1 might undergo degradation in response to high-intensity blue light (HBL).We demonstrated that CRY1 is ubiquitinated and degraded through the 26S proteasome pathway in response to HBL. We found that the E3 ubiquitin ligase constitutive photomorphogenic 1 (COP1) is involved in mediating HBL-induced ubiquitination and degradation of CRY1. We also found that the E3 ubiquitin ligases LRBs physically interact with CRY1 and are also involved in mediating CRY1 ubiquitination and degradation in response to HBL.We further demonstrated that blue-light inhibitor of cryptochromes 1 interacts with CRY1 in a blue-light-dependent manner to inhibit CRY1 dimerization/oligomerization, leading to the repression of HBL-induced degradation of CRY1.Our findings indicate that the regulation of CRY1 stability in HBL is coordinated by COP1 and LRBs, which provides a mechanism by which CRY1 attenuates its own signaling and optimizes photomorphogenesis under HBL.

Signaling Mechanisms by Arabidopsis Cryptochromes

“…This functional distinction correlates with a difference in photoreceptor stability: CRY2 is very photo-labile; it is degraded within a few hours of exposure to blue light. In contrast, CRY1 is mostly light-stable, though it was recently shown to be partially destabilized at very high fluence rates of blue light ( Lin et al, 1998 ; Miao et al, 2021 ). Another major functional distinction is the regulation of flowering time: CRY2 is a key inducer of flowering under the long-day conditions that promote flowering in Arabidopsis, while the role of CRY1 is only of minor importance and dependent on the respective environmental conditions used ( Guo et al, 1998 ; Mockler et al, 2003 ; Exner et al, 2010 ; Liu et al, 2016 ).…”

“…Moreover, BIC1 leads to an inhibition of blue light-dependent molecular activities of CRY2, such as photobody formation, phosphorylation, degradation, and binding of signaling components, suggesting that BIC1 has a primary function in inhibiting CRY2 photooligomerization ( Figure 2 ) which subsequently leads to the suppression of molecular and physiological CRY2 photoresponses ( Wang et al, 2016a ). Recently, it was shown that BIC1 also interacts with PHR1 in a blue light-dependent manner to inhibit CRY1 self-association and CRY1 degradation under high blue light fluence rates ( Miao et al, 2021 ). Gene expression of BIC1 and BIC2 is induced by blue, red, and UV-B light, thereby providing a negative feedback mechanism of CRYs and phytochromes on CRY1 and CRY2 signaling ( Wang et al, 2017 ; Tissot and Ulm, 2020 ).…”

“…This may be caused by an enhanced shuttling of COP1 out of the nucleus and/or by a generally reduced activity of proteasomes at low temperatures ( Catala et al, 2011 ; Li et al, 2021 ). Both COP1 and LRBs were also shown to control CRY1 protein stability under high blue light fluence rates ( Miao et al, 2021 ).…”

The Function and Photoregulatory Mechanisms of Cryptochromes From Moso Bamboo (Phyllostachys edulis)

“…Photoexcited Arabidopsis CRY1 and CRY2 further undergo blue light-dependent phosphorylation to both enhance their activities and facilitate their ubiquitination and degradation in the nucleus ( Shalitin et al, 2002 , 2003 ; Yu et al, 2007 ; Weidler et al, 2012 ; Liu et al, 2016 , 2022 ; Miao et al, 2021 ). Four closely related plant-specific PPKs (PPK1, PPK2, PPK3, and PPK4) have been shown to catalyze the phosphorylation of Arabidopsis CRY1 and CRY2 in blue light ( Liu et al, 2017 ; Ni et al, 2017 ).…”

“…The prototype plant CRYs are Arabidopsis CRY1 and CRY2, which mediate primarily blue light inhibition of cell elongation and photoperiodic promotion of floral initiation ( Ahmad and Cashmore, 1993 ; Mockler et al, 2003 ). It is previously reported that Arabidopsis CRY1 and CRY2 undergo these photoreactions: light-induced photo-oligomerization that is inhibited by the Blue-light Inhibitor of Cryptochromes (BICs), blue light-induced phosphorylation that is catalyzed by Photoregulatory Protein Kinases (PPKs), and polyubiquitination that is catalyzed by the E3 ubiquitin ligase Cul4 COP1/SPAs and Cul3 LRBs ( Shalitin et al, 2002 , 2003 ; Wang et al, 2016 ; Liu et al, 2017 , 2020 , 2022 ; Ma et al, 2020 , 2021 ; Shao et al, 2020 ; Chen et al, 2021 ; Miao et al, 2021 ). Biological functions of CRYs have been reported in various plant species, including tomato ( Ninu et al, 1999 ), soybean ( Zhang et al, 2008 ; Lyu et al, 2021 ), Brassica ( Chatterjee et al, 2006 ), pea ( Platten et al, 2005 ), poplar ( Mao et al, 2014 ), rice ( Matsumoto et al, 2003 ), barley ( Szucs et al, 2006 ), sorghum ( Zhou et al, 2018 ), apple ( Li et al, 2013a , b ), and wheat ( Xu et al, 2009 ).…”