The Plant Cell, Vol. 10, 1083–1094, July 1998, www.plantcell.org © 1998 American Society of Plant Physiologists RESEARCH ARTICLE Role of a COP1 Interactive Protein in Mediating Light-Regulated Gene Expression in Arabidopsis Yoshiharu Y. Yamamoto, a,1 Minami Matsui, a,b Lay-Hong Ang, a and Xing-Wang Deng a,2 a Department of Molecular, Cellular, and Developmental Biology, Yale University, 165 Prospect Street, New Haven, Connecticut 06520-8104 b Laboratory for Photoperception and Signal Transduction, FRP, Institute of Physical and Chemical Research (RIKEN), Saitama 351-01, Japan Arabidopsis seedlings display distinct patterns of gene expression and morphogenesis according to the ambient lightcondition. An Arabidopsis nuclear protein, CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), acts to repress photomor-phogenesis in the absence of light. The Arabidopsis CIP7 protein was identified by its capability to interact with COP1.CIP7 is a novel nuclear protein that contains transcriptional activation activity without a recognizable DNA binding mo-tif. CIP7 requires light for its high level of expression, and COP1 seems to play a role in repressing its expression indarkness. Decreasing CIP7 expression by introducing antisense CIP7 RNA resulted in defects in light-dependent antho-cyanin and chlorophyll accumulation. Antisense plants also displayed reduced expression of light-inducible genes foranthocyanin biosynthesis and photosynthesis. However, no defect was observed in light-dependent inhibition of hypo-cotyl elongation. Taken together, our data indicate that CIP7 acts as a positive regulator of light-regulated genes and isa potential direct downstream target of COP1 for mediating light control of gene expression.INTRODUCTION One of the unique features of plants is developmental plas-ticity. As sessile organisms, plants have developed strate-gies to sense the ambient environment for optimizing theirgrowth and survival. Perhaps because plant growth dependson light as the energy source, the light environment is one ofthe most important signals for regulating a seedling’s devel-opmental program (reviewed in Kendrick and Kronenberg,1994; von Arnim and Deng, 1996a). For example, dicotyle-donous seedlings germinated in the dark follow an etiolatedpattern, with elongated hypocotyls and undeveloped andclosed cotyledons. This is necessary so that plants can growthrough the soil or fallen leaves to reach the light. Light-grown seedlings have open and green cotyledons with well-developed chloroplasts for photosynthesis. At least threefamilies of photoreceptors are involved in perceiving lightand modulating the developmental program. In Arabidopsis,several of those photoreceptors have been well character-ized both genetically and physiologically. For example,phytochrome A (PHYA), phytochrome B (PHYB), and cryp-tochrome1 (CRY1/HY4) have been shown to be responsiblefor sensing distinct wavelengths of the high-irradiance lightsignal (Ahmad and Cashmore, 1993; Mohr, 1994; Quail,1994; Quail et al., 1995). It is well established that the per-ception of light by photoreceptors can lead to changes ingene expression patterns. This includes genes for photosyn-thesis and biosynthesis of protective materials against lightstress (Thompson and White, 1991; Miller et al., 1994).Genetic screens for constitutive photomorphogenic ordeetiolated development in darkness resulted in the identifi-cation of at least 10 pleiotropic Arabidopsis COP / DET / FUSCA ( FUS ) loci (Chory et al., 1989; Deng et al., 1991; Weiand Deng, 1992; Miséra et al., 1994; Wei et al., 1994b; Kwoket al., 1996). All loss-of-function mutations in those genesresult in similar pleiotropic photomorphogenic phenotypesin the dark and include activation of light-inducible genes,anthocyanin accumulation, chloroplast development, epi-dermal cell differentiation, inhibition of hypocotyl elongation,and cotyledon opening. All of these characteristics are ob-served only in wild-type plants that have been light grown.From genetic analyses, this class of genes seems to actdownstream of the multiple photoreceptors, including PHYA , PHYB , and CRY1 (Ang and Deng, 1994; Wei et al.,1994a; Kwok et al., 1996; Pepper and Chory, 1997). Among 1 Current address: Laboratory for Photoperception and Signal Trans-duction, FRP, Institute of Physical and Chemical Research (RIKEN),Saitama 351-01, Japan. 2 To whom correspondence should be addressed. E-mail [email protected]; fax 203-432-3854.1084 The Plant Cell this group of genes, four have been molecularly character-ized: COP1 , DET1 , COP9 , and FUS6 / COP11 (Deng et al.,1992; Castle and Meinke, 1994; Pepper et al., 1994; Wei etal., 1994b), and all were shown to encode nuclear proteins(Pepper et al., 1994; von Arnim and Deng, 1994; Chamovitzet al., 1996; Staub et al., 1996).Recent analysis suggests that the subcellular localizationof COP1 can be regulated by light (von Arnim and Deng,1994). When COP1 is fused with a reporter protein, b -glucu-ronidase (GUS), the GUS–COP1 fusion protein was ob-served mainly in the nucleus in the absence of light. Afterlight perception, the fusion protein was not detectable in thenucleus. The fact that the total amount of the cellular COP1protein was not changed by light suggests that light causeda specific redistribution of COP1 within the cell. Subse-quently, it was demonstrated that the nuclear localization ofthe GUS–COP1 fusion is diminished in the other nine COP / DET / FUS loci even in the dark (Chamovitz et al., 1996; vonArnim et al., 1997). The fact that COP1 alone can act auton-omously to suppress photomorphogenesis and that this abil-ity is highly dependent on its cellular abundance (McNellis etal., 1994b) suggests that COP1 is part of a key regulatorystep responsible for repression of photomorphogenesis(Torii and Deng, 1997). Furthermore, the data support theview that COP1 acts within the nucleus to suppress photo-morphogenic development in the dark and that the othernine loci are required for its proper nuclear localization orstability. The perception of light results in the inactivation ofCOP1 and reduction of its nuclear abundance.An understanding of how COP1 suppresses photomor-phogenesis in the nucleus is thus of great interest. COP1contains several characteristic motifs (Deng et al., 1992;McNellis et al., 1994a). They include a zinc binding motifcalled a RING finger (Saurin et al., 1996), a putative coiled-coil region (COIL), and WD40 repeats (Neer