The Photomorphogenic Central Repressor COP1: Conservation and Functional Diversification during Evolution

Abstract

Green plants on the earth have evolved intricate mechanisms to acclimatize to and utilize sunlight. In Arabidopsis, light signals are perceived by photoreceptors and transmitted through divergent but overlapping signaling networks to modulate plant photomorphogenic development. COP1 (CONSTITUTIVE PHOTOMORPHOGENIC 1) was first cloned as a central repressor of photomorphogenesis in higher plants and has been extensively studied for over 30 years. It acts as a RING E3 ubiquitin ligase downstream of multiple photoreceptors to target key light-signaling regulators for degradation, primarily as part of large protein complexes. The mammalian counterpart of COP1 is a pluripotent regulator of tumorigenesis and metabolism. A great deal of information on COP1 has been derived from whole-genome sequencing and functional studies in lower green plants, which enables us to illustrate its evolutionary history. Here, we review the current understanding about COP1, with a focus on the conservation and functional diversification of COP1 and its signaling partners in different taxonomic clades.

Keywords: COP1; E3 ubiquitin ligase; evolution; gravitropism; light protection; photomorphogenesis.

Figure 1

The Protein Domains and Phylogenetic Analyses of COP1 and SPAs. (A) Schematic diagrams showing functional domains of Arabidopsis SPA1 and COP1. Conserved domains are shown in the same shapes and colors. Numbers indicate the positions of amino acids. (B) The phylogenetic relationships of COP1 orthologs. Using AtCOP1 as query, all significantly similar proteins in HMMER reference proteomes containing the COP1 structural domains shown in (A) were identified as COP1 orthologs. The maximum-likelihood tree was constructed following our previous study (Han et al., 2019). COP1 exists widely in eukaryotic clades, and only in eukaryotes. (C) The phylogenetic relationships of SPA1 orthologs. Candidate SPA1 orthologs were identified as described above. SPA1 orthologs found in HMMER reference proteomes were combined with those previously identified in representative plant genomes (Han et al., 2019). SPA1 orthologs are only present in green plant lineages.

Figure 2

Three COP1/SPA-Containing Complexes Are Involved in Light Regulation of Plant Development. (A) COP1/SPA core tetramer complex. (B) CUL4–DDB1–COP1/SPA ubiquitin ligase complex. (C) UVR8–COP1/SPA complex.

Figure 3

A Model Decipicting the Conversion between Two Distinct COP1/SPA-Containing Complexes in the Presence or Absence of UV-B Light. Without UV-B irradiation, the CUL4–DDB1–COP1/SPA complex is the primary functional COP1/SPA core tetramer, and targets HY5 and other promoters of light signaling for degradation to repress photomorphogenic or photoprotective gene expression. RUP1 and RUP2 function redundantly to mediate UVR8 redimerization and halt UVR8 signaling (Heijde and Ulm, 2013). Upon UV-B irradiation, UVR8 monomerizes and associates with the COP1/SPA core tetramer complex to form a new complex. The E3 ligase responsible for HY5 degradation switches from CUL4–DDB1–COP1/SPA to CUL4–DDB1–RUP1/2. COP1, possibly in the UVR8–COP1/SPA complex, targets RUP1/2 for proteolysis and thus stabilizes HY5.

Figure 4

A Simplified Network Antagonistically Regulated by phyB and the COP1/SPA Complex during Photomorphogenesis in Arabidopsis. Photoreceptors perceive environmental light signals to promote light responses, while COP/DET/FUS proteins function as central repressors to inhibit light responses. Under red light conditions, activated phyB inhibits the activity of the photomorphogenesis-repressing transcription factors PIFs (Huq and Quail, 2002, Khanna et al., 2004, Leivar et al., 2008), and EIN3/EIL (Shi et al., 2016). On the contrary, the COP1/SPA complex stabilizes these transcription factors by targeting their E3 ligase EBF1/2 for degradation (Dong et al., 2017, Shi et al., 2016), and meanwhile destabilizes photomorphogenesis-promoting transcription factor HY5/HYH (Ang et al., 1998, Holm et al., 2002, Oyama et al., 1997, Saijo et al., 2003, Yanagawa et al., 2004) to maintain skotomorphogenesis in darkness. PIFs and EIN3/EIL1 act in parallel to activate HLS1 expression to promote the formation of the apical hook (Lyu et al., 2019, Zhang et al., 2018). These two groups of transcription factors cooperatively repress cotyledon development but promote hypocotyl elongation (Shi et al., 2018, Zhang et al., 2018, Zhong et al., 2012). In contrast, HY5/HYH promote cotyledon expansion but inhibit hypocotyl elongation by regulating the expression of light-responsive genes.

Figure 5

The Seedling Emergence Signaling Networks Regulated by Light and Mechanical Pressure. (A) Upon germination deep in the soil, the seedlings covered by soil face two stress stimuli: darkness and mechanical pressure. The active COP1/SPA complexes promote skotomorphogenesis by regulating three transcription factors (HY5, PIFs, and EIN3). In addition, mechanical impedance boosts endogenous ethylene accumulation, which induces crosstalk between ethylene and light signals. (B) During the course of hypocotyl elongation under soil, dim light penetrates into soil and reduces the activity of COP1/SPA complexes. However, ethylene responses remain highly variable depending on soil conditions. (C) After breaking out of the soil, seedlings free from mechanical pressure and under sunlight switch to photomorphogenic development. The activity of COP1/SPA complexes is completely repressed.

Figure 6

Conserved COP/DET/FUS Proteins Are Involved in Distinct Light-Regulatory Pathways in Chlamydomonas and Arabidopsis. (A) In Chlamydomonas, CrPHOT senses high light and induces photoprotection responses. In low light, both the CDD complex and COP1/SPA complex repress high light responses. In high light the activity of these E3 ubiquitin ligases is inhibited, allowing CrCO accumulation and the expression of high light-responsive genes. Under UV-B light, activated CrUVR8 monomers interact with CrCOP1 and induce the accumulation of CrHY5, and thus promote UV-B responses and acclimation. (B) In Arabidopsis, light-activated photoreceptors inactivate COP/DET/FUS protein complexes, thus allowing the accumulation of photomorphogenesis-promoting regulators such as HY5 to globally activate light-responsive genes and photomorphogenic development. Similarly to Chlamydomonas CrUVR8, Arabidopsis UVR8 senses UV-B light and forms a new complex with the COP1/SPA core apparatus, which indirectly promotes the accumulation of HY5 and photomorphogenic development.