Regulation of the orientation movement of chloroplasts in epidermal cells of Vallisneria: cooperation of phytochrome with photosynthetic pigment under low-fluence-rate light

Abstract

Abstract. In epidermal cells of the leaves of the aquaticangiosperm Vallisneria gigantea Graebner, the chloroplasts accumulate in the outer periclinal layer of cytoplasm (P side) under light at low fluence rates. The nature of such intracellular orientation of chloroplasts was investigated in a semiquantitative manner. Time-lapse video microscopy revealed that, while irradiation with red light (650 nm, 0.41 W" m-2) rapidly accelerated the migration of chloroplasts, not only from the anticlinal layers of cytoplasm (A sides) to the P side but also from the P side to the A sides, the increased rate of migration in both directions returned to the control rate upon subsequent irradiation with far-red light (746nm, 0.14W.m-2). These effects of red and far-red light could be observed repeatedly, both in the presence and in the absence of inhibitors of photosynthesis, suggesting the involvement of phytochrome as the photoreceptor. After saturating irradiation with red light, the increased rate of migration of chloroplasts from the P side to the A sides declined more rapidly than the increased rate of migration in the opposite direction. This imbalance in the migration of chloroplasts between the two opposing directions resulted in the accumulation of chloroplasts on the P side. The more rapid decline in the rate of migration of chloroplasts from the P side to the A sides than in the opposite direction was not observed in the presence of an inhibitor of photosynthesis. It appears, therefore, that phytochrome and photosynthetic pigment cooperatively regulate the accumulation of chloroplasts on the P side through modulation of the nature of the movement of the chloroplasts.Abbreviations: A side = cytoplasmic layer that faces the anticlinal wall; DCMU = 3-(3,4-dichlorophenyl)-l,l-dimethylurea; Pfr = farred-light-absorbing form of phytochrome; Pr = red-light-absorbing form of phytochrome; P side = cytoplasmic layer that faces the outer periclinal wall Correspondence to: S. Takagi; FAX: 81 (6) 850 5817; Tel: 81 (6) 850 5818

Actin-based photo-orientation movement of chloroplasts in plant cells

“…Within several minutes of irradiation with dim red light, the rate of migration of chloroplasts in both directions increased. After approximately 20 min, however, the rate of migration of chloroplasts from the P side to the A sides decreased compared with that in the opposite direction, leading to a gradual increase in the number of chloroplasts on the P side (Dong et al, 1995). Thus, red light appeared to initially enhance the motility of each chloroplast and to later suppress the motility of chloroplasts on the P side but not on the A sides (Fig.·5).…”

“…We frequently observed that mitochondria also gather on the P side with the accumulated chloroplasts S. Takagi Fig.·4), suggesting mutual metabolic interactions (Raghavendra et al, 1994). Using video microscopy, we analysed the mode of movement of chloroplasts during the accumulation response semi-quantitatively (Dong et al, 1995). In the dark, the chloroplasts slowly migrated between the P side and the cytoplasmic layers perpendicular to the P side (anticlinal layers; A sides) at a constant rate.…”

Photomorphogenesis of Mosses

“…The same pattern was found for Ceratodon (Kagawa et al, 1997). The situation for these two species is comparable with seed plants, where chloroplast movement is also only induced by blue light, mediated by phototropins, and not by red light (but see Dong et al, 1995). In Physcomitrella however, chloroplast movement is triggered both by blue and red light.…”

Regulation of Actin-Dependent Cytoplasmic Motility by Type II Phytochrome Occurs within Seconds in Vallisneria gigantea Epidermal Cells

“…The light source was a bank of 20-W fluorescent lamps (FL20S-PG; National, Kadoma, Japan). The procedures for the preparation of specimens were described in detail previously (Dong et al, 1995). In brief, adaxial pieces of leaf 5 to 10 mm in width and 2 to 3 mm in length were removed at the end of a light period.…”

“…Considering the importance of early downstream responses of phytochromes, we investigated the photoregulation of cytoplasmic motility in epidermal cells of Vallisneria gigantea using the microscope described above equipped with an image analyzer and a microbeam irradiator. We selected this material because previous studies with Vallisneria have demonstrated light-regulated reorientation of chloroplasts under dim and strong light (Izutani et al, 1990;Dong et al, 1995), light-induced rotational streaming of the cytoplasm (Yamaguchi and Nagai, 1981), and light-induced reorganization of the actin cytoskeleton (Dong et al, 1998). In addition, extracts prepared from green leaves of Vallisneria contain phytochrome that undergoes spectrophotometrically red/ far-red photoreversible changes in absorption .…”