A single chromoprotein with triple chromophores acts as both a phytochrome and a phototropin

Abstract

Plants sense their environmental light conditions by using three photoreceptors that absorb in the UV, blue͞near UV, and red͞far-red spectral ranges. These photoreceptors have specific chromophore components corresponding to their absorption spectra. Phytochrome, a red͞far-red light receptor, has phytochromobilin as its chromophore, whereas the blue͞near UV photoreceptors cryptochrome and phototropin have a pair of flavin derivatives. Plants use these various photoreceptors to assess the surrounding light environment. Phytochrome 3 (PHY3) is a red light receptor found in some ferns, which preferentially grow under weak light. PHY3 is composed of a phytochrome chromophore-binding domain in its N-terminal portion and an almost full-length phototropin in its C-terminal half. This unusual domain organization implies that two different light-sensing systems coexist in this single photoreceptor, although these light-sensing systems usually reside in independent photoreceptors. Here, we show that PHY3 acts as a dual-channel photoreceptor that possesses both the red lightsensing system of phytochrome and the blue light-sensing system of phototropin. Furthermore, red-and blue-light signals perceived by PHY3 are processed synergistically within this single chromoprotein. These unusual properties might confer an enhanced light sensitivity on PHY3, allowing ferns to grow under a low-light canopy.fern ͉ phototropism ͉ photoreceptor ͉ red light ͉ blue light P lants have developed sophisticated sensing systems of intensity, direction, duration, and spectral quality of light. Because light consists of components with different wavelengths, plants perceive light signals through various photoreceptors corresponding to wavelength range. These light signals induce various environmental responses of plants and even modulate developmental programs of them (1, 2). Many photomorphogenic responses have been described, for example, control of seed germination, hypocotyl elongation, cotyledon opening, chloroplast development, and gene expression. Among these responses, phototropic response and chloroplast photorelocation movement can be elicited in dicotyledonous plants only by blue͞near UV light (3) and are mediated by phototropins (4). However, in some cryptogamic plants, both phototropic response and chloroplast photorelocation movement are induced by red light (RL) as well as blue light (BL) (5).In the fern Adiantum, both BL-and RL-dependent phototropic responses and chloroplast photorelocation movements are well described (6-9). We showed that these RL-dependent responses of Adiantum are mediated by phytochrome 3 (PHY3) (10). The deduced amino acid sequence indicates that the N-terminal portion of PHY3 contains the chromophore-binding domain of phytochrome, and the C-terminal half shows a remarkable similarity to phototropin (11). The predicted domain organization of PHY3 implies that two different light-sensing systems coexist in this single chromoprotein, although it is not known whether PHY3 can function as a BL receptor or not. I...

Phototropin Receptor Kinase Activation by Blue Light

“…7,8 Moreover, this mutation has been used successfully to probe the roles of LOV1 and LOV2 in regulating phototropin activity and function. [9][10][11][12] As reported previously (ref. 13), the Cys → Ala mutation within LOV2 of Arabidopsis thaliana phot1 (C517A) results in a loss of light-induced receptor autophosphorylation when expressed in insect cells (Fig.…”

Nuclear Phytochrome A Signaling Promotes Phototropism in Arabidopsis

“…The fern Adiantum possesses a chimeric photoreceptor consisting of a phytochrome photosensory domain fused to a phototropintype photoreceptor (Kawai et al, 2003). When expressed in Arabidopsis, this photoreceptor triggers phototropism toward both red and blue light (Kanegae et al, 2006). This can be used as an evolutionary argument to propose that phytochromes and phototropins presumably act closely together in the regulation of phototropism (Marcotte et al, 1999).…”

Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns

“…Neochromes have a restricted occurrence in the plant tree of life and are hypothesized to have had two independent origins (5)-one in the green alga Mougeotia scalaris and another in ferns. The possession of neochrome may be evolutionarily advantageous, as evidenced by the greatly enhanced phototropic responses in ferns with neochrome (3,4) and by its phylogenetic distribution within the fern lineage. The early-diverging fern orders Osmundales and Schizaeales do not possess neochrome (3).…”

“…It fuses red-sensing phytochrome and blue-sensing phototropin modules into a single molecule (Fig. 1A) that mediates phototropic responses (1)(2)(3)(4). Neochromes have a restricted occurrence in the plant tree of life and are hypothesized to have had two independent origins (5)-one in the green alga Mougeotia scalaris and another in ferns.…”