Pb-induced avoidance-like chloroplast movements in fronds of Lemna trisulca L

PLoS One. 2015 Feb 3;10(2):e0116757. doi: 10.1371/journal.pone.0116757. eCollection 2015.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / drug effects
  • Actin Cytoskeleton / metabolism
  • Actin Cytoskeleton / radiation effects
  • Araceae / cytology*
  • Araceae / drug effects
  • Araceae / radiation effects
  • Catalase / metabolism
  • Chloroplasts / drug effects*
  • Chloroplasts / metabolism*
  • Chloroplasts / radiation effects
  • Darkness
  • Hydrogen Peroxide / pharmacology
  • Lead / pharmacology*
  • Movement / drug effects*
  • Movement / radiation effects
  • Plant Leaves / cytology*
  • Plant Leaves / drug effects
  • Plant Leaves / radiation effects

Substances

  • Lead
  • Hydrogen Peroxide
  • Catalase

Grants and funding

Sławomir Samardakiewicz was supported by the Polish National Science Centre Project (NCN) grant no. 8066/B/P01/2011/40. The X-ray microanalysis were performed in the Laboratory of Electron Microscopy, Nencki Institute of Experimental Biology (Warsaw, Poland) by using electron microscope JEM 1400 (JEOL Co., Japan, 2008), equipped with energy-dispersive full range X-ray microanalysis system (EDS INCA Energy TEM, Oxford Instruments, Great Britain) and high resolution digital camera CCD MORADA, SiS-Olympus, Germany). The above mentioned equipment was installed within the project sponsored by the EU Structural Funds (SPO WKP_1/1.4.3/2/2005/102/222/562/U). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.