Abstract
Lead ions are particularly dangerous to the photosynthetic apparatus, but little is known about the effects of trace metals, including Pb, on regulation of chloroplast redistribution. In this study a new effect of lead on chloroplast distribution patterns and movements was demonstrated in mesophyll cells of a small-sized aquatic angiosperm Lemna trisulca L. (star duckweed). An analysis of confocal microscopy images of L. trisulca fronds treated with lead (15 μM Pb2+, 24 h) in darkness or in weak white light revealed an enhanced accumulation of chloroplasts in the profile position along the anticlinal cell walls, in comparison to untreated plants. The rearrangement of chloroplasts in their response to lead ions in darkness was similar to the avoidance response of chloroplasts in plants treated with strong white light. Transmission electron microscopy X-ray microanalysis showed that intracellular chloroplast arrangement was independent of the location of Pb deposits, suggesting that lead causes redistribution of chloroplasts, which looks like a light-induced avoidance response, but is not a real avoidance response to the metal. Furthermore, a similar redistribution of chloroplasts in L. trisulca cells in darkness was observed also under the influence of exogenously applied hydrogen peroxide (H2O2). In addition, we detected an enhanced accumulation of endogenous H2O2 after treatment of plants with lead. Interestingly, H2O2-specific scavenger catalase partly abolished the Pb-induced chloroplast response. These results suggest that H2O2 can be involved in the avoidance-like movement of chloroplasts induced by lead. Analysis of photometric measurements revealed also strong inhibition (but not complete) of blue-light-induced chloroplast movements by lead. This inhibition may result from disturbances in the actin cytoskeleton, as we observed fragmentation and disappearance of actin filaments around chloroplasts. Results of this study show that the mechanisms of the toxic effect of lead on chloroplasts can include disturbances in their movement and distribution pattern.
Highlights
The movement of organelles makes it possible for cells to maintain homeostasis and adapt to the changing environmental conditions [1,2,3]
Plastids located along periclinal walls were seen in the so-called face position, while those located along anticlinal walls were observed in the so-called profile position
We have shown for the first time that the changes involved a redistribution of chloroplasts towards anticlinal walls
Summary
The movement of organelles makes it possible for cells to maintain homeostasis and adapt to the changing environmental conditions [1,2,3]. Movements of chloroplasts play a important role. An intermediate model of chloroplast distribution in darkness can be observed in palisade cells of Arabidopsis thaliana: along anticlinal walls as well as along the periclinal walls that are internally tangent, while there are no chloroplasts along the periclinal wall neighboring with the epidermis [15,16]. Such a variety of distribution of chloroplasts in darkness makes it difficult to explain the role of chloroplast location in darkness
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