Chloroplast aggregation during the cold-positioning response in the liverwort Marchantia polymorpha

Abstract

Under low-light conditions, chloroplasts localize along periclinal cell walls at temperatures near 20 °C, but they localize along anticlinal cell walls near 5 °C. This phenomenon is known as the cold-positioning response. We previously showed that chloroplasts move as aggregates rather than individually during the cold-positioning response in the fern Adiantum capillus-veneris. This observation suggested that chloroplasts physically interact with each other during the cold-positioning response. However, the physiological processes underlying chloroplast aggregation are unclear. In this report, we characterized chloroplast aggregation during the cold-positioning response in the liverwort Marchantia polymorpha. Confocal laser microscopy observations of transgenic liverwort plants expressing a fluorescent fusion protein that localizes to the chloroplast outer envelope membrane (OEP7-Citrine) showed that neighboring chloroplast membranes did not fuse during the cold-positioning response. Transmission electron microscopy analysis revealed that a distance of at least 10 nm was maintained between neighboring chloroplasts during aggregation. These results indicate that aggregated chloroplasts do not fuse, but maintain a distance of at least 10 nm from each other during the cold-positioning response.

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Acknowledgements

We thank Mr. Koichiro Takaoka (THERMTRON Co. Ltd., Japan) and Mr. Tadao Onuma (Onuma Factory Co. Ltd., Japan; Study Group of Ohtawara Health and Welfare) for their help in developing the temperature-controlled microscope system. We also thank Dr. Takayuki Kohchi (Kyoto University) for providing the Tak-1 and BC3-38 strains. H.T. was supported by a Postdoctoral Fellowship of the Creative Department for Innovation of Utsunomiya University. N.H. was supported by the Hayashi Rheology Memorial Foundation. This work was supported by a Fellowship for Overseas Collaboration Research of the Japanese Society of Plant Physiologists (JSPP) (for collaboration between A.H. and Y.K.), the Japan Society for the Promotion of Science (JSPS) KAKENHI (nos. 23870002 and 26840088 to Y.K.), the JST-ERATO Numata Organelle Reaction Cluster (JPMJER1602 to Y.K.), and Research and Development Grants of the Creative Department for Innovation of Utsunomiya University (Y.K.).

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Correspondence to Yutaka Kodama.

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10265_2017_958_MOESM2_ESM.avi

Movie S1: Time-lapse observation of chloroplast movement during the avoidance response induced by high-intensity white light. Images were acquired at 1-min intervals for 5 h. Bar = 5 μm. (AVI 3928 KB)

Movie S1: Time-lapse observation of chloroplast movement during the avoidance response induced by high-intensity white light. Images were acquired at 1-min intervals for 5 h. Bar = 5 μm. (AVI 3928 KB)

10265_2017_958_MOESM3_ESM.avi

Movie S2: Time-lapse observation of chloroplast movement during the cold-positioning response under low-intensity white light conditions. Images were acquired at 5-min intervals for 12 h. Bar = 5 μm. (AVI 1534 KB)

Movie S2: Time-lapse observation of chloroplast movement during the cold-positioning response under low-intensity white light conditions. Images were acquired at 5-min intervals for 12 h. Bar = 5 μm. (AVI 1534 KB)

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Tanaka, H., Sato, M., Ogasawara, Y. et al. Chloroplast aggregation during the cold-positioning response in the liverwort Marchantia polymorpha . J Plant Res 130, 1061–1070 (2017). https://doi.org/10.1007/s10265-017-0958-9

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Keywords

  • Bryophytes
  • Chloroplast aggregation
  • Chloroplast movement
  • Low temperature
  • Outer envelope membrane
  • Temperature-controlled microscopy