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Chloroplasts continuously monitor photoreceptor signals during accumulation movement

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Abstract

Under low light conditions, chloroplasts gather at a cell surface to maximize light absorption for efficient photosynthesis, which is called the accumulation response. Phototropin1 (phot1) and phototropin2 (phot2) were identified as blue light photoreceptors in the accumulation response that occurs in Arabidopsis thaliana and Adiantum capillus-veneris with neochrome1 (neo1) as a red light photoreceptor in A. capillus-veneris. However, the signal molecule that is emitted from the photoreceptors and transmitted to the chloroplasts is not known. To investigate this topic, the accumulation response was induced by partial cell irradiation with a microbeam of red, blue and far-red light in A. capillus-veneris gametophyte cells. Chloroplasts moved towards the irradiated region and were able to sense the signal as long as its signal flowed. The signal from neo1 had a longer life than the signal that came from phototropins. When two microbeams with the same wavelength and the same fluence rate were placed 20 μm apart from each other and were applied to a dark-adapted cell, chloroplasts at an equidistant position always moved towards the center (midpoint) of the two microbeams, but not towards either one. This result indicates that chloroplasts are detecting the concentration of the signal but not the direction of signal flow. Chloroplasts repeatedly move and stop at roughly 10 s intervals during the accumulation response, suggesting that they monitor the intermittent signal waves from photoreceptors.

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Acknowledgments

We thank Dr. Hironao Kataoka for his valuable comments. This work was partially supported by the Japanese Ministry of Education, Sports, Science and Technology (MEXT 13139203 and 17084006 to M.W.) and the Japan Society for the Promotion of Science (JSPS 13304061, 16107002 and 20227001 to M.W.).

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Correspondence to Masamitsu Wada.

Electronic supplementary material

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Supplementary material 1 (MOV 3405 kb)

Supplementary material 2 (MOV 4041 kb)

Supplementary material 1 (MOV 3405 kb)

Supplementary material 2 (MOV 4041 kb)

Supplementary material 3 (EPS 6608 kb)

Movie S1. A time-lapse video of the chloroplast movement that is shown in Fig. 4. Images were acquired at 15-sec intervals.

Movie S2. A time-lapse video of the chloroplast movement shown in Fig. 5. Images were acquired at 15-sec intervals.

Figure S3. Move and stop cycles during the chloroplast accumulation response induced by irradiation with a B microbeam (8 μm diameter, 10 W m−2) continuously in a dark-adapted gametophyte cell (a and b) and in a dark-adapted A. thaliana mesophyll cell (c and d) at 3-sec intervals and induced by irradiation with a R microbeam (8 μm diameter, 10 W m−2) continuously in a dark-adapted gametophyte cell (e and f) at 5-sec intervals. Other details are the same as in Fig. 6

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Tsuboi, H., Wada, M. Chloroplasts continuously monitor photoreceptor signals during accumulation movement. J Plant Res 126, 557–566 (2013) doi:10.1007/s10265-012-0542-2

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Keywords

  • Accumulation movement
  • Adiantum capillus-veneris
  • Blue light
  • Chloroplast movement
  • Microbeam
  • Red light