A phytochrome/phototropin chimeric photoreceptor promotes growth of fern gametophytes under limited light conditions.

Many ferns thrive even in low-light niches such as under an angiosperm forest canopy. However, the shade adaptation strategy of ferns is not well understood. Phytochrome 3/neochrome (phy3/neo) is an unconventional photoreceptor, found in the fern Adiantum capillus-veneris, that controls both red and blue light-dependent phototropism and chloroplast photorelocation, which are considered to improve photosynthetic efficiency in ferns. Here we show that phy3/neo localizes not only at the plasma membrane but also in the nucleus. Since both phototropism and chloroplast photorelocation are mediated by membrane-associated phototropin photoreceptors, we speculated that nucleus-localized phy3/neo possesses a previously undescribed biological function. We reveal that phy3/neo directly interacts with Adiantum cryptochrome 3 (cry3) in the nucleus. Plant cryptochromes are blue light receptors that transcriptionally regulate photomorphogenesis; therefore, phy3/neo may function via cry3 to synchronize light-mediated development with phototropism and chloroplast photorelocation to promote fern growth under low-light conditions. Furthermore, we demonstrate that phy3/neo regulates the expression of the Cyclin-like gene AcCyc1 and promotes prothallium expansion growth. These findings provide insight into the shade adaptation strategy of ferns and suggest that phy3/neo plays a substantial role in the survival and growth of ferns during the tiny gametophytic stage under low-light conditions, such as those on the forest floor.

A phytochrome/phototropin chimeric photoreceptor of fern functions as a blue/far-red light-dependent photoreceptor for phototropism in Arabidopsis.

In the fern Adiantum capillus-veneris, the phototropic response of the protonemal cells is induced by blue light and partially inhibited by subsequent irradiation with far-red light. This observation strongly suggests the existence of a phytochrome that mediates this blue/far-red reversible response; however, the phytochrome responsible for this response has not been identified. PHY3/NEO1, one of the three phytochrome genes identified in Adiantum, encodes a chimeric photoreceptor composed of both a phytochrome and a phototropin domain. It was demonstrated that phy3 mediates the red light-dependent phototropic response of Adiantum, and that phy3 potentially functions as a phototropin. These findings suggest that phy3 is the phytochrome that mediates the blue/far-red response in Adiantum protonemata. In the present study, we expressed Adiantum phy3 in a phot1 phot2 phototropin-deficient Arabidopsis line, and investigated the ability of phy3 to induce phototropic responses under various light conditions. Blue light irradiation clearly induced a phototropic response in the phy3-expressing transgenic seedlings, and this effect was fully inhibited by simultaneous irradiation with far-red light. In addition, experiments using amino acid-substituted phy3 indicated that FMN-cysteinyl adduct formation in the light, oxygen, voltage (LOV) domain was not necessary for the induction of blue light-dependent phototropism by phy3. We thus demonstrate that phy3 is the phytochrome that mediates the blue/far-red reversible phototropic response in Adiantum. Furthermore, our results imply that phy3 can function as a phototropin, but that it acts principally as a phytochrome that mediates both the red/far-red and blue/far-red light responses.

Evolutionary aspects of plant photoreceptors.

Plant photoreceptors link environmental light cues with physiological responses, determining how individual plants complete their life cycles. Structural and functional evolution of photoreceptors has co-occurred as plants diversified and faced the challenge of new light environments, during the transition of plants to land and as substantial plant canopies evolved. Large-scale comparative sequencing projects allow us for the first time to document photoreceptor evolution in understudied clades, revealing some surprises. Here we review recent progress in evolutionary studies of three photoreceptor families: phytochromes, phototropins and neochromes.

Plant nuclear photorelocation movement.

Organelle movement and positioning are essential for proper cellular function. A nucleus moves dynamically during cell division and differentiation and in response to environmental changes in animal, fungal, and plant cells. Nuclear movement is well-studied and the mechanisms have been mostly elucidated in animal and fungal cells, but not in plant cells. In prothallial cells of the fern Adiantum capillus-veneris and leaf cells of the flowering plant Arabidopsis thaliana, light induces nuclear movement and nuclei change their position according to wavelength, intensity, and direction of light. This nuclear photorelocation movement shows some common features with the photorelocation movement of chloroplasts, which is one of the best-characterized plant organelle movements. This review summarizes nuclear movement and positioning in plant cells, especially plant-specific nuclear photorelocation movement and discusses the relationship between nuclear photorelocation movement and chloroplast photorelocation movement.

Determination of Phototropism and Polarotropism in Fern Protonemal Cells.

Fern protonemal cells grow at their apices as long, undivided filamentous cells toward red (or weak white) light and change their growth direction if the light direction is changed (i.e., phototropism). When protonemata growing between an agar surface and cover glass are irradiated with polarized red light through the glass on the protonemal side, they start growing at the point where the direction of the vibration plane of polarized light and the transition moment of the photoreceptor, which is parallel to the plasma membrane of the cell's apical part, are equal (i.e., polarotropism). Herein, the methods on how to induce and observe this protonemal phototropism and polarotropism are described.

Intramolecular co-action of two independent photosensory modules in the fern phytochrome 3.

Fern phytochrome3/neochrome1 (phy3/neo1) is a chimeric photoreceptor composed of a phytochrome-chromophore binding domain and an almost full-length phototropin. phy3 thus contains two different light-sensing modules; a red/far-red light receptor phytochrome and a blue light receptor phototropin. phy3 induces both red light- and blue light-dependent phototropism in phototropin-deficient Arabidopsis thaliana (phot1 phot2) seedlings. The red-light response is dependent on the phytochrome module of phy3, and the blue-light response is dependent on the phototropin module. We recently showed that both the phototropin-sensing module and the phytochrome-sensing module mediate the blue light-dependent phototropic response. Particularly under low-light conditions, these two light-sensing modules cooperate to induce the blue light-dependent phototropic response. This intramolecular co-action of two independent light-sensing modules in phy3 enhances light sensitivity, and perhaps allowed ferns to adapt to the low-light canopy conditions present in angiosperm forests.