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Low temperature-induced chloroplast relocation mediated by a blue light receptor, phototropin 2, in fern gametophytes

Abstract

Chloroplast movement in response to light has been known more than 100 years. Chloroplasts move towards weak light and move away from strong light. Dark-induced relocation, called dark positioning, has also been shown. However, the effects of other stimuli on chloroplast movement have not been well characterized. Here we studied low temperature-induced chloroplast relocation (termed cold positioning) in prothallial cells of the gametophytes of the fern Adiantum capillus-veneris. Under weak light chloroplasts in prothallial cells accumulated along the periclinal wall at 25°C, but they moved towards anticlinal walls when the prothalli were subsequently transferred to 4°C. A temperature shift from 25° to 10°C or lower was enough to induce cold positioning, and high-intensity light enhanced the response. Nuclei also relocated from the periclinal position (a position along periclinal walls) to the anticlinal position (a position along anticlinal walls) under cold temperature, whereas mitochondria did not. Cold positioning was not observed in mutant fern gametophytes defective of the blue light photoreceptor, phototropin 2.

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References

  1. Buchner O, Holzinger A, Lütz C (2007) Effects of temperature and light on the formation of chloroplast protrusions in leaf mesophyll cells of high alpine plants. Plant Cell Environ 30:1347–1356

  2. DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139:101–114

  3. Haberlandt G (1876) Über den Einfluß des Frostes auf die chlorophyllkörner. Österr Botan Zeitschrift 26:249–255

  4. Holzinger A, Buchner O, Lütz C, Hanson MR (2007) Temperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana. Protoplasma 230:23–30

  5. Kagawa T, Kasahara M, Abe T, Yoshida S, Wada M (2004) Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. Plant Cell Physiol 45:416–426

  6. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141

  7. Kagawa T, Wada M (1993) Light-dependent nuclear positioning in prothallial cells of Adiantum capillus-veneris. Protoplasma 177:82–85

  8. Kagawa T, Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41:84–93

  9. Kagawa T, Wada M (2002) Blue light-induced chloroplast relocation. Plant Cell Physiol 43:367–371

  10. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

  11. Kasahara M, Kagawa T, Sato Y, Kiyosue T, Wada M (2004) Phototropins mediate blue and red light-induced chloroplast movements in Physcomitrella patens. Plant Physiol 135:1388–1397

  12. Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, Kadota A, Wada M (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421:287–290

  13. Luesse DR, DeBlasio SL, Hangarter RP (2006) Plastid movement impaired 2, a new gene involved in normal blue-light-induced chloroplast movements in Arabidopsis. Plant Physiol 141:1328–1337

  14. Martin B, Öquist G (1979) Seasonal and experimentally induced changes in the ultrastructure of chloroplasts of Pinus silvestris. Physiol Plant 46:42–49

  15. Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815

  16. Sato Y, Kadota A, Wada M (1999) Mechanically induced avoidance response of chloroplasts in fern protonemal cells. Plant Physiol 121:37–44

  17. Sato Y, Kadota A, Wada M (2003a) Chloroplast movement: dissection of events downstream of photo- and mechano-perception. J Plant Res 116:1–5

  18. Sato Y, Wada M, Kadota A (2003b) Accumulation response of chloroplasts induced by mechanical stimulation in bryophyte cells. Planta 216:772–777

  19. Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci U S A 98:6969–6974

  20. Senn G (1908) Die Gestalts—und Lageveränderung der Pflanzen—Chromatophoren. Wilhelm-Engelmann, Leipzig

  21. Suetsugu N, Kagawa T, Wada M (2005) An auxilin-like J-domain protein, JAC1, regulates phototropin-mediated chloroplast movement in Arabidopsis. Plant Physiol 139:151–162

  22. Suetsugu N, Wada M (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 388:927–935

  23. Tanaka A (2007) Photosynthetic activity in winter needles of the evergreen tree Taxus cuspidata at low temperatures. Tree Physiol 27:641–648

  24. 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

  25. 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

  26. Wada M, Kagawa T, Sato Y. (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468

  27. White PR (1943) Handbook of plant tissue culture. Jaques Cartell, Lancaster, pp 1–277

  28. Yatsuhashi H, Wada M (1990) High-fluence rate response in the light-oriented chloroplast movement in Adiantum protonemata. Plant Sci 68:87–94

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Acknowledgments

The authors thank Ms. Ayumi Iwata (National Institute for Basic Biology), for maintenance of plant materials, and Dr. Inga Oberpichler (University of Karlsruhe), for providing valuable information. We also thank John Christie (University of Glasgow) for his careful reading of this manuscript and English editing. This work was partly supported by Grant-in-Aid for Scientific Research (on Priority Areas, no. 17084006) from the Ministry of Education, Sports, Science and Technology of Japan to M.W.

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Correspondence to Masamitsu Wada.

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Kodama, Y., Tsuboi, H., Kagawa, T. et al. Low temperature-induced chloroplast relocation mediated by a blue light receptor, phototropin 2, in fern gametophytes. J Plant Res 121, 441–448 (2008) doi:10.1007/s10265-008-0165-9

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Keywords

  • Adiantum capillus-veneris
  • Chloroplast relocation
  • Cold positioning
  • Fern
  • Low temperature
  • Phototropin