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.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Ahmad M, Cashmore AR (1993) HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–166
Harada A, Sakai T, Okada K (2003) Phot1 and phot2 mediate blue light-induce transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc Natl Acad Sci USA 100:8583–8588
Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19
Huala E, Oeller PW, Liscum E, Han IS, Larse E, Briggs WR (1997) Arabidopsis NPH1: a protein kinases with a putative redox-sensing domain. Science 278:2120–2123
Iino M (2001) Phototropism in higher plants in photomovement. In: Hader D, Lebert M (eds) ESP comprehensive series in photosciences, vol 1. Elsevier Science, Amsterdam, pp 659–811
Ishikawa R, Tamaki S, Yokoi S, Inagaki N, Shinomura T, Takano M, Shimamoto K (2005) Suppression of the floral activator Hd3a is the principal cause of the night break effect in rice. Plant Cell 17:3326–3336
Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954
Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106:13106–13111
Kagawa T, Wada M (1994) Brief irradiation with red or blue light induces orientational movement of chloroplasts in dark-adapted prothallial cells of the fern Adiantum. J Plant Res 107:389–398
Kagawa T, Wada M (1999) Chloroplast-avoidance response induced by high-fluence blue light in prothallial cells of the fern Adiantum capillus-veneris as analyzed by microbeam irradiation. Plant Physiol 119:917–924
Kagawa T, Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41:84–93
Kagawa T, Wada M (2004) Velocity of chloroplast avoidance movement is fluence rate dependent. Photochem Photobiol Sci 3:592–595
Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: A phototropin homologue controlling the chloroplast high-light avoidance response. Science 291:2138–2141
Kagawa T, Kasahara M, Abe T, Yoshida S, Wada M (2004) Function analysis of phototropin2 using mutants deficient in blue light-induced chloroplast avoidance movement. Plant Cell Physiol 45:416–426
Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002a) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832
Kasahara M, Swartz TE, Olney MA, Onodera A, Mochizuki N, Fukuzawa H, Asamizu E, Tabata S, Kanegae H, Takano M, Christie JM, Nagatani A, Briggs WR (2002b) Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii. Plant Physiol 129:762–773
Mandoli DF, Briggs WR (1982) Optical properties of etiolated plant tissues. Proc Natl Acad Sci USA 79:2902–2906
Salomon M, Christie JM, Knieb E, Lempert U, Briggs WR (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39:9401–9410
Shinomura T, Nagatani A, Hanzawa H, Kubota M, Watanabe M, Furuya M (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 93:8129–8133
Suetsugu N, Wada M (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 388:927–935
Sugai M, Furuya M (1967) Photomorphogenesis in Pteris vittata I. Phytochrome-mediated spore germination and blue light interaction. Plant Cell Physiol 8:737–748
Tsuboi H, Wada M (2010a) Speed of signal transfer in the chloroplast accumulation response. J Plant Res 123:381–390
Tsuboi H, Wada M (2010b) The speed of intracellular signal transfer for chloroplast movement. Plant Signal Behav 5:433–435
Tsuboi H, Suetsugu N, Wada M (2006) Negative phototropic response of rhizoid cells in the fern Adiantum capillus-veneris. J Plant Res 119:505–512
Tsuboi H, Suetsugu N, Kawai-Toyooka H, Wada M (2007) Phototropins and neochrome1 mediate nuclear movement in the fern Adiantum capillus-veneris. Plant Cell Physiol 48:892–896
Tsuboi H, Yamashita H, Wada M (2009) Chloroplasts do not have a polarity for light-induced accumulation movement. J Plant Res 122:131–140
Wada M, Furuya M (1978) Effects of narrow-beam irradiations with blue and far-red light on the timing of cell division in Adiantum gametophytes. Planta 138:85–90
Wada M, Kadota A, Furuya M (1983) Intracellular localization and dichroic orientation of phytochrome in plasma membrane and/or ectoplasm of a centrifuged protonema of fern Adiantum capillus-veneris. Plant Cell Physiol 24:1441–1447
Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468
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.).
Electronic supplementary material
Below is the link to the electronic supplementary material.
(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
About this article
Cite this article
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
- Adiantum capillus-veneris
- Arabidopsis thaliana
- Blue light
- Chloroplast movement