Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase

Abstract

Plants have evolved specific photoreceptors that capture informational cues from sunlight. The phytochrome, cryptochrome, and UVR8 photoreceptors perceive red/far-red, blue/UV-A, and UV-B light, respectively, and control overlapping photomorphogenic responses important for plant growth and development. A major repressor of such photomorphogenic responses is the E3 ubiquitin ligase formed by CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) and SUPPRESSOR OF PHYA-105 (SPA) proteins, which acts by regulating the stability of photomorphogenesis-promoting transcription factors. The direct interaction of light-activated photoreceptors with the COP1/SPA complex represses its activity via nuclear exclusion of COP1, disruption of the COP1-SPA interaction, and/or SPA protein degradation. This process enables plants to integrate different light signals at the level of the COP1/SPA complex to enact appropriate photomorphogenic responses according to the light environment.

Plant photoreceptors and their signaling components compete for COP 1 binding via VP peptide motifs

“…Mutations in the SPA1 WD40 domain residues Lys767 and Trp812, which correspond to COP1 residues Lys422 and Trp467, cannot complement the spa1-3 mutant (Yang & Wang, 2006). These higher-order complexes are known to be part of some but not all light signaling pathways and could thus encode additional determinants for signaling specificity (Hoecker, 2017;Podolec & Ulm, 2018). In addition to the competition mechanism presented here, it has been observed that active cryptochrome and phytochrome receptors directly interact with SPA proteins and thereby separate COP1 from SPA proteins, which results in COP1 inactivation (Lian et al, 2011;Liu et al, 2011;Zuo et al, 2011;Lu et al, 2015;Sheerin et al, 2015).…”

Light‐induced stabilization of ACS contributes to hypocotyl elongation during the dark‐to‐light transition in Arabidopsis seedlings

“…Extensive molecular genetic studies have identified and characterized key molecular components in the light signaling pathway and their role in regulating various light responses in plants. Plants perceive light through various photoreceptors, including phytochromes, cryptochromes and phototropins (Mao et al, 2005;Okajima, 2016;Fujii et al, 2017;Demarsy et al, 2018;Podolec and Ulm, 2018;Wang et al, 2018), and subsequently incorporate the integrated light signals into cells by modulating the activity or stability of downstream transcription factors such as the phytochrome interacting factor (PIF) family of transcription factors and the constitutively photomorphogenic 1 (COP1)/suppressor of PHYA-105 (SPA) E3 ligase complex (Castillon et al, 2007;Pham et al, 2018). Previous studies have shown that phytochromes are involved primarily in regulating de-etiolation processes, and the phytochrome-mediated suppression of COP1/SPA activity releases the inhibition of several photomorphogenesis-promoting factors, such as elongated hypocotyl 5 (HY5), HY5 homolog, and long after far-red light 1, thereby initiating photomorphogenesis (Zhu et al, 2008;Yang et al, 2009;Li et al, 2010;Pokhilko et al, 2011;Hofmann, 2015).…”

Photoreceptor signaling: when COP1 meets VPs

“…The loss‐of‐function cop1 mutants exhibit constitutive photomorphogenic phenotypes, such as suppressed hypocotyl elongation in the absence of light, suggesting that COP1 is a negative regulator of photomorphogenesis. Studies in the following decades demonstrated that COP1 acts as the substrate receptor of the E3 ubiquitin ligase CUL4 COP1‐SPAs to facilitate ubiquitination and degradation of various transcription factors required for photomorphogenesis (Lau & Deng, ; Podolec & Ulm, ). Remarkably, three out of five classes of plant photoreceptors, phytochromes, cryptochromes, and UVR8, mediate photoresponses at least partially by inhibition of the COP1 activity (Lau & Deng, ; Podolec & Ulm, ).…”

“…Studies in the following decades demonstrated that COP1 acts as the substrate receptor of the E3 ubiquitin ligase CUL4 COP1‐SPAs to facilitate ubiquitination and degradation of various transcription factors required for photomorphogenesis (Lau & Deng, ; Podolec & Ulm, ). Remarkably, three out of five classes of plant photoreceptors, phytochromes, cryptochromes, and UVR8, mediate photoresponses at least partially by inhibition of the COP1 activity (Lau & Deng, ; Podolec & Ulm, ). However, the exact structural mechanisms underlying this photoreceptor–COP1–substrate tripartite interaction and how the evolutionarily distinct photoreceptors converge on the single hub protein COP1 remained unclear.…”

“…COP1 interacts with diverse light‐signaling transcription factors, such as the bZIP transcription factors HY5 (ELONGATED HYPOCOTYL 5) and HYH (HY5 HOMOLOG), BBX transcription factors CO/BBX1 (CONSTANS), COL3/BBX4, and STO/BBX24 (SALT TOLERANCE), and the bHLH transcription factor HFR1 (LONG HYPOCOTYL IN FAR‐RED 1), to regulate their stability in response to light (Lau & Deng, ). On the other hand, the UV‐B light receptor UVR8 and the blue light receptors CRY1 and CRY2 interact with COP1 to suppress its activity (Podolec & Ulm, ). An earlier study showed that three COP1‐interacting proteins bear a common sequence motif, referred to as VP, which contains two amino acids, valine–proline, as the invariable core, and that the VP motif may be a common COP1‐binding site (Holm et al , ).…”