Chloroplasts can move in any direction to avoid strong light

Abstract

Chloroplasts migrate in response to different light intensities. Under weak light, chloroplasts gather at an illuminated area to maximize light absorption and photosynthesis rates (the accumulation response). In contrast, chloroplasts escape from strong light to avoid photodamage (the avoidance response). Photoreceptors involved in these phenomena have been identified in Arabidopsis thaliana and Adiantum capillus-veneris. Chloroplast behavior has been studied in detail during the accumulation response, but not for the avoidance response. Hence, we analyzed the chloroplast avoidance response in detail using dark-adapted Adiantum capillus-veneris gametophyte cells and partial cell irradiation with a microbeam of blue light. Chloroplasts escaped from an irradiated spot. Both duration of this response and the distance of the migrated chloroplasts were proportional to the total fluence irradiated. The speed of movement during the avoidance response was dependent on the fluence rate, but the speed of the accumulation response towards the microbeam from cell periphery was constant irrespective of fluence rate. When a chloroplast was only partially irradiated with a strong microbeam, it moved away towards the non-irradiated region within a few minutes. During this avoidance response two additional microbeam irradiations were applied to different locus of the same chloroplast. Under these conditions the chloroplast changed the moving direction after a lag time of a few minutes without rolling. Taken together, these findings indicate that chloroplasts can move in any direction and never have an intrinsic polarity. Similar phenomenon was observed in chloroplasts of Arabidopsis thaliana palisade cells.

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Acknowledgments

We thank Dr. Matthew J. Terry of University of Southampton for careful reading of the manuscript. This work was partly supported by the Japanese Ministry of Education, Sports, Science, and Technology (MEXT 13139203, 17084006 to M.W.), the Japan Society of Promotion of Science (JSPS 13304061, 16107002, 20227001 to M.W.), and a Research Fellowship for Young Scientists (to H.T.).

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Correspondence to Masamitsu Wada.

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This time-lapse movie shows chloroplast avoidance movement induced by three sequential blue microbeam irradiations from which the data of Figs. 5, 6 and 7 were taken. Note the linear movement of the chloroplast escaping from the beam. Images were acquired in 15-sec intervals

(a) Photographs showing chloroplast movement in an Arabidopsis thaliana palisade cell induced by three sequential irradiations of a blue microbeam 100 μm2 square. A dark-adapted palisade cell with a few chloroplasts still attached along the periclinal wall is shown. The chloroplast at the center of the cell (arrow) was continually observed and photographed under red light. (a1) Onset of continuous irradiation of the chloroplast (dotted line) with a blue microbeam of 30 W m−2. (a2) The position of the chloroplast and the second blue microbeam with the same fluence rate and shape as the first beam. The chloroplast moved away from the first microbeam and before the chloroplast stopped moving the second microbeam was given to a different part of the same chloroplast. The photograph was taken 6.5 min after the first beam irradiation. (a3) Chloroplast movement away from the second microbeam-irradiated area. The third microbeam irradiation was given before the chloroplast stopped escaping from the second microbeam irradiation. The photograph was taken 13 min after the first microbeam irradiation. (a4) Chloroplast movement away from the third microbeam-irradiated area. The photograph was taken 19 min after the first beam irradiation. White lines in panels a2, a3 and a4 indicate the path taken by the chloroplast. Scale bar = 10 μm. (b) The path of the center of the chloroplast during movement induced by the first (dotted line), second (broken line) and third (bold line) microbeam irradiations. Data were obtained every 15 s. (c) Time course of chloroplast avoidance movement. Arrows indicate the start of each microbeam irradiation. Data were obtained every 15 s

(a) The velocity of chloroplast avoidance movement induced by three sequential irradiations to different halves of the same chloroplast in an A. thaliana palisade cell. (b) The lag times before the start of chloroplast movement or a change in direction to escape subsequent irradiations with sequential strong microbeams. Data were obtained from photographs taken at the similar experiments to those shown in Supplemental Data S1 repeated at least 12 times

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Tsuboi, H., Wada, M. Chloroplasts can move in any direction to avoid strong light. J Plant Res 124, 201–210 (2011). https://doi.org/10.1007/s10265-010-0364-z

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Keywords

  • Adiantum capillus-veneris
  • Arabidopsis thaliana
  • Avoidance
  • Blue light
  • Chloroplast movement
  • Microbeam