Journal of Plant Research

, Volume 130, Issue 4, pp 779–789 | Cite as

Temperature-dependent signal transmission in chloroplast accumulation response

  • Takeshi Higa
  • Satoshi Hasegawa
  • Yoshio Hayasaki
  • Yutaka Kodama
  • Masamitsu WadaEmail author
Regular Paper


Chloroplast photorelocation movement, well-characterized light-induced response found in various plant species from alga to higher plants, is an important phenomenon for plants to increase photosynthesis efficiency and avoid photodamage. The signal for chloroplast accumulation movement connecting the blue light receptor, phototropin, and chloroplasts remains to be identified, although the photoreceptors and the mechanism of movement via chloroplast actin filaments have now been revealed in land plants. The characteristics of the signal have been found; the speed of signal transfer is about 1 µm min−1 and that the signal for the accumulation response has a longer life and is transferred a longer distance than that of the avoidance response. Here, to collect the clues of the unknown signal substances, we studied the effect of temperature on the speed of signal transmission using the fern Adiantum capillus-veneris and found the possibility that the mechanism of signal transfer was not dependent on the simple diffusion of a substance; thus, some chemical reaction must also be involved. We also found new insights of signaling substances, such that microtubules are not involved in the signal transmission, and that the signal could even be transmitted through the narrow space between chloroplasts and the plasma membrane.


Blue light Chloroplast movement Fern Phototropin Red light Signaling 



This work was supported in part by the Japan Society of Promotion of Science [23120523, 25251033, 25120721, and 16K14758 to M.W. and 23870002, and 26840088 to Y.K.]. We would thank Dr. Akeo Kadota for his various support to this work, and Mr. Shun Kimura (Utsunomiya University) for his technical assistance.

Author contributions

Authors have made the following contributions to the manuscript: TH, YK, MW planned and designed the research. TH performed the experiments. SH, YH, YK designed and constructed a system for microbeam irradiation in a temperature-controlled microbeam irradiator.

Supplementary material

10265_2017_938_MOESM1_ESM.pdf (1.5 mb)
Supplementary material 1 (PDF 1535 KB)


  1. Anielska-Mazur A, Bernaś T, Gabryś H (2009) In vivo reorganization of the actin cytoskeleton in leaves of Nicotiana tabacum L. transformed with plastin–GFP: correlation with light-activated chloroplast responses. BMC Plant Biol 9:1–14. doi: 10.1186/1471-2229-9-64 CrossRefGoogle Scholar
  2. Babourina O, Newman I, Shabala S (2002) Blue light-induced kinetics of H+ and Ca2+ fluxes in etiolated wild-type and phototropin-mutant Arabidopsis seedlings. Proc Natl Acad Sci USA 99:2433–2438. doi: 10.1073/pnas.042294599 CrossRefPubMedGoogle Scholar
  3. Banaś AK, Aggarwal C, Łabuz J, Sztatelman O, Gabryś H (2012) Blue light signalling in chloroplast movements. J Exp Bot 63:1559–1574. doi: 10.1093/jxb/err429 CrossRefPubMedGoogle Scholar
  4. Baum G, Long JC, Jenkins GI, Trewavas AJ (1999) Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+. Proc Natl Acad Sci USA 96:13554–13559. doi: 10.1073/pnas.96.23.13554 CrossRefPubMedGoogle Scholar
  5. Buchner O, Lütz C, Holzinger A (2007) Design and construction of a new temperature-controlled chamber for light and confocal microscopy under monitored conditions: biological application for plant samples. J Microsc 225:183–191. doi: 10.1111/j.1365-2818.2007.01730.x CrossRefPubMedGoogle Scholar
  6. DeBlasio SL, Luesse DL, Hangarter RP (2005) A plant-specific protein essential for blue-light-induced chloroplast movements. Plant Physiol 139:101–114. doi: 10.1104/pp.105.061887 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Gabryś H (2012) Blue-light-activated chloroplast movements: progress in the last decade. In: Lüttge U, Beyschlag W, Büdel B, Francis D (eds) Progress in Botany 73. Springer-Verlager, Berlin, pp 189–205CrossRefGoogle Scholar
  8. Harada A, Sakai T, Okada K (2003) Phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc Natl Acad Sci USA 100:8583–8588. doi: 10.1073/pnas.1336802100 CrossRefPubMedGoogle Scholar
  9. Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155. doi: 10.1105/tpc.105.032508 CrossRefGoogle Scholar
  10. Higa T, Wada M (2015) Clues to the signals for chloroplast photo-relocation from the lifetimes of accumulation and avoidance responses. J Integr Plant Biol 57:120–126. doi: 10.1111/jipb.12310 CrossRefPubMedGoogle Scholar
  11. Jarillo JA, Gabryś H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954. doi: 10.1038/35073622 CrossRefPubMedGoogle Scholar
  12. Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoji 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. doi: 10.1073/pnas.0906250106 CrossRefPubMedGoogle Scholar
  13. 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. doi: 10.1007/BF02344062 CrossRefGoogle Scholar
  14. Kagawa T, Wada M (1996) Phytochrome- and blue light-absorbing pigment-mediated directional movement of chloroplasts in dark-adapted prothallial cells of fern Adiantum as analyzed by microbeam irradiation. Planta 198:488–493. doi: 10.1007/BF00620067 CrossRefGoogle Scholar
  15. 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 119:917–923. doi: 10.1104/pp.119.3.917 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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. doi: 10.1126/science.291.5511.2138 CrossRefPubMedGoogle Scholar
  17. 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. doi: 10.1093/pcp/pch045 CrossRefPubMedGoogle Scholar
  18. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832. doi: 10.1038/nature01213 CrossRefPubMedGoogle Scholar
  19. 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. doi: 10.1038/nature01310 CrossRefPubMedGoogle Scholar
  20. Kong SG, Wada M (2014) Recent advances in understanding the molecular mechanism of chloroplast photorelocation movement. Biochim Biophys Acta 1837:522–530. doi: 10.1016/j.bbabio.2013.12.004 CrossRefPubMedGoogle Scholar
  21. Kong SG, Suetsugu N, Kikuchi S, Nakai M, Nagatani A, Wada M (2013a) Both phototropin 1 and 2 localize on the chloroplast outer membrane with distinct localization activity. Plant Cell Physiol 54:80–92. doi: 10.1093/pcp/pcs151 CrossRefPubMedGoogle Scholar
  22. Kong SG, Arai Y, Suetsugu N, Yanagida T, Wada M (2013b) Rapid severing and motility of cp-actin filaments are required for the chloroplast avoidance response. Plant Cell 25:572–590. doi: 10.1105/tpc.113.109694 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Masuda A, Ushida K, Okamoto T. (2005) Direct observation of spatiotemporal dependence of anomalous diffusion in inhomogeneous fluid by sampling-volume-controlled fluorescence correlation spectroscopy. Physi Rev E 72, 060101(R). doi: 10.1103/PhysRevE.72.060101 CrossRefGoogle Scholar
  24. Murata T, Wada M (1989) Organization of cortical microtubules and microfibril deposition in response to blue-light-induced apical swelling in a tip-growing Adiantum protonemal cell. Planta 178:334–341. doi: 10.1007/BF00391861 CrossRefPubMedGoogle Scholar
  25. Murata T, Kadota A, Hogetsu T, Wada M (1987) Circular arrangement of cortical microtubules around the subapical part of a tip-growing fern protonema. Protoplasma 141:135–138. doi: 10.1007/BF01272895 CrossRefGoogle Scholar
  26. Murata T, Kadota A, Wada M (1997) Effects of blue light on cell elongation and microtubule orientation in dark-grown gametophytes of Ceratopteris richardii. Plant Cell Physiol 38:201–209. doi: 10.1093/oxfordjournals.pcp.a029153 CrossRefGoogle Scholar
  27. Nozue K, Kanegae T, Imaizumi T, Fukuda S, Okamoto H, Yeh KC, Lagarias JC, Wada M (1998) A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc Natl Acad Sci USA 95:15826–15830CrossRefPubMedGoogle Scholar
  28. 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. doi: 10.1105/tpc.016428 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Romagnoli S, Cai G, Cresti M (2003) In vitro assays demonstrate that pollen tube organelles use kinesin-related motor proteins to move along microtubules. Plant Cell 15:251–269. doi: 10.1105/tpc.005645 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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 USA 98:6969–6974. doi: 10.1073/pnas.101137598 CrossRefPubMedGoogle Scholar
  31. Sato Y, Kadota A, Wada M (1999) Mechanically induced avoidance response of chloroplasts in fern protonemal cells. Plant Physiol 121:37–44. doi: 10.1104/pp.121.1.37 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Sato Y, Wada M, Kadota A (2001a) Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. J Cell Sci 114:269–279PubMedGoogle Scholar
  33. Sato Y, Wada M, Kadota A (2001b) External Ca2+ is essential for chloroplast movement induced by mechanical stimulation but not by light stimulation. Plant Physiol 127:497–504. doi: 10.1104/pp.010405 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16:68–72. doi: 10.1016/ CrossRefPubMedGoogle Scholar
  35. Sidell BD, Hazel JR (1987) Temperature affects the diffusion of small molecules through cytosol of fish muscle. J Exp Biol 129:191–203PubMedGoogle Scholar
  36. Stoelzle S, Kagawa T, Wada M, Hedrich R, Dietrich P (2003) Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway. Proc Natl Acad Sci USA 100:1456–1461. doi: 10.1073/pnas.0333408100 CrossRefPubMedGoogle Scholar
  37. Suetsugu N, Wada M (2009) Chloroplast photorelocation movement. In: Sandelius AS, Aronsson H (eds) The Chloroplast-Interaction with Environment. Plant Cell Monographs. Sprinter, Berlin, pp 235–266Google Scholar
  38. Suetsugu N, Mittmann F, Wagner G, Hughes J, Wada M (2005) A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution. Proc Natl Acad Sci USA 102:13705–13709. doi: 10.1073/pnas.0504734102 CrossRefPubMedGoogle Scholar
  39. Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010) Two kinesin-like proteins mediates actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:8860–8865. doi: 10.1073/pnas.0912773107 CrossRefPubMedGoogle Scholar
  40. Tlałka M, Fricker M (1999) The role of calcium in blue-light-dependent chloroplast movement in Lemna trisulca L. Plant J 20:461–473. doi: 10.1046/j.1365-313x.1999.00621.x CrossRefPubMedGoogle Scholar
  41. Tlałka M, Gabryś H (1993) Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L. Planta 189:491–498. doi: 10.1007/BF00198211 CrossRefGoogle Scholar
  42. Trump BF, Berezesky IK, Sato T, Laiho KU, Phelps PC, DeClaris N (1984) Cell calcium, cell injury and cell death. Environ Health Perspect 57:281–287CrossRefPubMedPubMedCentralGoogle Scholar
  43. Tsuboi H, Wada M (2010) Speed of signal transfer in the chloroplast accumulation response. J Plant Res 123:381–390. doi: 10.1007/s10265-009-0284-y CrossRefPubMedGoogle Scholar
  44. Tsuboi H, Wada M (2013) Chloroplasts continuously monitor photoreceptor signals during accumulation movement. J Plant Res 126:557–566. doi: 10.1007/s10265-012-0542-2 CrossRefPubMedGoogle Scholar
  45. 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. doi: 10.1093/pcp/pcm057 CrossRefPubMedGoogle Scholar
  46. Vestergaard CL, Flyvbjerg H, Møller IM (2012) Intracellular signaling by diffusion: can waves of hydrogen peroxide transmit intracellular information in plant cells? Front Plant Sci. doi: 10.3389/fpls.2012.00295 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Wada M, Kong SG (2011) Analysis of chloroplast movement and relocation in Arabidopsis. Methods in Molecular Biology 774, “Chloroplast Research in Arabidopsis”, Methods and Protocols, vol 1. Jarvis RP. Humana Press, Totowa NJ, pp 87–102Google Scholar
  48. Wada M, O’Brien TP (1975) Observations on the structure of the protonema of Adiantum capillus-veneris L. undergoing cell division following white-light irradiation. Planta 126:213–227. doi: 10.1007/BF00388964 CrossRefPubMedGoogle Scholar
  49. 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 L. Plant Cell Physiol 24:1441–1447CrossRefGoogle Scholar
  50. Wen F, Xing D, Zhang LR (2008) Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis. J Exp Bot 59:2891–2901. doi: 10.1093/jxb/ern147 CrossRefPubMedGoogle Scholar
  51. Yatsuhashi H, Kadota A, Wada M (1985) Blue- and red-light action in photoorientation of chloroplasts in Adiantum protonemata. Planta 165:43–50. doi: 10.1007/BF00392210 CrossRefPubMedGoogle Scholar
  52. Zurzycki J (1955) Chloroplast arrangements as a factor of photosynthesis. Acta Soc Bot Pol 24:27–63. doi: 10.5586/asbp.1974.052 CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  • Takeshi Higa
    • 1
  • Satoshi Hasegawa
    • 2
  • Yoshio Hayasaki
    • 2
  • Yutaka Kodama
    • 3
  • Masamitsu Wada
    • 1
    Email author
  1. 1.Department of Biological SciencesTokyo Metropolitan UniversityTokyoJapan
  2. 2.Center for Optical Research and EducationUtsunomiya UniversityTochigiJapan
  3. 3.Center for Bioscience Research and EducationUtsunomiya UniversityTochigiJapan

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