Chloroplast Movements in Response to Environmental Signals

  • Yoshikatsu Sato
  • Akeo Kadota
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

Plants use light not only as an energy source for photosynthesis but also as an environmental signal for developmental regulation. In most plants, the photosynthetic organelle, the chloroplast, does not rest in the same position of the cell but instead relocates in response to external stimuli in order to maximize photosynthetic activity. Genetic and reverse genetic studies using Arabidopsis thaliana have allowed rapid progress in our knowledge of this field. Extensive advances in the last five years have identified and characterized new components controlling chloroplast movement, including blue-light receptors, phototropins and an actin-binding protein associated with chloroplast movements called “CHUP1” (chloroplast unusual positioning 1). This chapter gives integrated current information about the mechanisms of chloroplastmovement. In the first part of this review, we summarize most recentwork on light-induced chloroplast movement and in the following section we describe the new type of chloroplast movement induced by mechanical stimulation. In the last section, we discuss the ecological significance of chloroplast movement.


Avoidance Response Chloroplast Movement Accumulation Response Leucine Zipper Domain Microbeam Irradiation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Baum G, Long JC, Jenkins GI and Trewavas AJ (1999) Stimulation of the blue light phototropic receptor NPH1 causes a transient increase in cytosolic Ca2+ . Proc Natl Acad Sci USA 96: 13554-13559CrossRefPubMedGoogle Scholar
  2. Briggs WR, Beck CF, Cashmore AR, Christie JM, Hughes J, Jarillo JA, Kagawa T, Kanegae H, Liscum E, Nagatani A, Okada K, Salomon M, Rudiger W, Sakai T, Takano M, Wada M and Watson JC (2001) The phototropin family of photore-ceptors. Plant Cell 13: 993-997CrossRefPubMedGoogle Scholar
  3. Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA, Liscum E and Briggs WR (1998) Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for pho-totropism. Science 282: 1698-1701CrossRefPubMedGoogle Scholar
  4. Christie JM, Swartz TE, Bogomolni RA and Briggs WR (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32: 205-219CrossRefPubMedGoogle Scholar
  5. DeBlasio SL, Mullen JL, Luesse DR and Hangarter RP (2003) Phytochrome modulation of blue light-induced chloroplast movements in Arabidopsis. Plant Physiol 133: 1471-1479CrossRefPubMedGoogle Scholar
  6. Dong X-J, Nagai R and Takagi S (1998) Microfilaments anchor chloroplasts along the outer periclinal wall in Vallisneria epi-dermal cells through cooperation of PFR and photosynthesis. Plant Cell Physiol 39: 1299-1306Google Scholar
  7. Emi T, Kinoshita T and Shimazaki K (2001) Specific binding of vf14-3-3a isoform to the plasma membrane H+ -ATPase in response to blue light and fusicoccin in guard cells of broad bean. Plant Physiol 125: 1115-1125CrossRefPubMedGoogle Scholar
  8. Evans JR and Von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiol 110: 339-346PubMedGoogle Scholar
  9. Ferl RJ (1996) 14-3-3 proteins and signal transduction. Annu Rev Plant Physiol Plant Mol Biol 47: 49-73CrossRefPubMedGoogle Scholar
  10. Gallagher S, Short TW, Ray PM, Pratt LH and Briggs WR (1988) Light-mediated changes in two proteins found associated with plasma membrane fractions from pea stem sections. Proc Natl Acad Sci USA 85: 8003-8007CrossRefPubMedGoogle Scholar
  11. Hager A and Birch M (1993) Blue-light-induced phosphoryla-tion of a plasma-membrane protein from phototropically sen-sitive tips of maize coleoptiles. Planta 189: 567-576CrossRefGoogle Scholar
  12. Harada A, Sakai T and Okada K (2003) Phot1 and phot2 me-diate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves. Proc Natl Acad Sci USA 100: 8583-8588CrossRefPubMedGoogle Scholar
  13. Haupt W (1999) Chloroplast movement: from phenomenology to molecular biology. Prog Bot 60: 3-36Google Scholar
  14. Haupt W and Scheuerlein R (1990) Chloroplast movement. Plant Cell Environ 13: 595-614CrossRefGoogle Scholar
  15. Holt MR and Koffer A (2001) Cell motility: proline-rich proteins promote protrusions. Trends Cell Biol 11: 38-46CrossRefPubMedGoogle Scholar
  16. Huala E, Oeller PW, Liscum E, Han IS, Larsen E and Briggs WR (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278: 2120-2123CrossRefPubMedGoogle Scholar
  17. Inada S, Ohgishi M, Mayama T, Okada K and Sakai T (2004) RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16: 887-896CrossRefPubMedGoogle Scholar
  18. Jarillo JA, Ahmad M and Cashmore AR (1998) NPL1 (acces-sion No. AF053941): A second member of the NPH ser-ine/threonine kinase family of Arabidopsis (PGR98-100). Plant Physiol 117: 719Google Scholar
  19. Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR and Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410: 952-954CrossRefPubMedGoogle Scholar
  20. Kadota A and Wada M (1992a) Photoorientation of chloro-plasts in protonemal cells of the fern Adiantum as analyzed by use of a video-tracking system. Bot Mag Tokyo 105: 265-279CrossRefGoogle Scholar
  21. Kadota A and Wada M (1992b) Photoinduction of formation of circular structures by microfilaments on chloroplast during in-tracellular orientation in protonemal cells of the fern Adiantum capillus-veneris. Protoplasma 167: 97-107CrossRefGoogle Scholar
  22. Kadota A, Wada M and Furuya M (1985) Phytochrome-mediated polarotropism of Adiantum capillus-veneris L. protonemata as analyzed by microbeam irradiation with polarized light. Planta 195: 30-36CrossRefGoogle Scholar
  23. Kadota A, Sato Y and Wada M (2000) Intracellular chloroplast photorelocation in the moss Physcomitrella patens is mediated by phytochrome as well as by a blue-light receptor. Planta 210: 932-937CrossRefPubMedGoogle Scholar
  24. Kagawa T and Wada M (1996) Phytochrome- and blue-light-absorbing pigment-mediated directional movement of chloro-plasts in dark-adapted prothallial cells of fern Adiantum as analyzed by microbeam irradiation. Planta 198: 488-493CrossRefGoogle Scholar
  25. Kagawa T and Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41: 84-93PubMedGoogle Scholar
  26. Kagawa T and Wada M (2002) Blue light-induced chloroplast relocation. Plant Cell Physiol 43: 367-371CrossRefPubMedGoogle Scholar
  27. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K and Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138-2141CrossRefPubMedGoogle Scholar
  28. Kagawa T, Kasahara M, Abe T, Yoshida S and Wada M (2004) Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. Plant Cell Physiol 45: 416-426CrossRefPubMedGoogle Scholar
  29. Kandasamy MK and Meagher RB (1999) Actin-organelle inter-action: association with chloroplast in Arabidopsis leaf mes-ophyll cells. Cell Motil Cytoskeleton 44: 110-118CrossRefPubMedGoogle Scholar
  30. Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M and Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420: 829-832CrossRefPubMedGoogle Scholar
  31. Kasahara M, Kagawa T, Sato Y, Kiyosue T and Wada M (2004) Phototropins mediate blue and red light-induced chloroplast movements in Physcomitrella patens. Plant Physiol 135: 1388-1397CrossRefPubMedGoogle Scholar
  32. Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, Kadota A and Wada M (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421: 287-290CrossRefPubMedGoogle Scholar
  33. Kinoshita T and Shimazaki K (1999) Blue light activates the plasma membrane H+ -ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18: 5548-5558CrossRefPubMedGoogle Scholar
  34. Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M and Shi-mazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414: 656-660CrossRefPubMedGoogle Scholar
  35. Kinoshita T, Emi T, Tominaga M, Sakamoto K, Shigenaga A, Doi M and Shimazaki K (2003) Blue-light- and phosphorylation-dependent binding of a 14-3-3 protein to phototropins in stomatal guard cells of broad bean. Plant Physiol 133: 1453-1463CrossRefPubMedGoogle Scholar
  36. Knieb E, Salomon M and Rudiger W (2004) Tissue-specific and subcellular localization of phototropin determined by immuno-blotting. Planta 218: 843-851CrossRefPubMedGoogle Scholar
  37. Liscum E and Briggs WR (1995) Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. Plant Cell 7: 473-485CrossRefPubMedGoogle Scholar
  38. Malec P, Rinaldi R and Gabrys H (1996) Light-induced chloro-plast movements in Lemna trisulca. Identification of the motile system. Plant Sci 120: 127-137CrossRefGoogle Scholar
  39. Mittmann F, Brucker G, Zeidler M, Repp A, Abts T, Hartmann E and Hughes J (2004) Targeted knockout in Physcomitrella reveals direct actions of phytochrome in the cytoplasm. Proc Natl Acad Sci USA 101: 13939-13944CrossRefPubMedGoogle Scholar
  40. Motchoulski A and Liscum E (1999) Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science 286: 961-964CrossRefPubMedGoogle Scholar
  41. Nozue K, Kanegae T, Imaizumi T, Fukuda S, Okamoto H, Yeh KC, Lagarias JC and Wada M (1998) A phytochrome from the fern Adiantum with features of the putative pho-toreceptor NPH1. Proc Natl Acad Sci USA 95: 15826-15830CrossRefPubMedGoogle Scholar
  42. Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A and Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15: 2805-2815CrossRefPubMedGoogle Scholar
  43. Palmer JM, Short TW, Gallagher S and Briggs WR (1993) Blue light-induced phosphorylation of a plasma membrane-associated protein in Zea mays L. Plant Physiol 102: 1211-1218PubMedGoogle Scholar
  44. Russell AJ, Cove DJ, Trewavas AJ and Wang TL (1998) Blue light but not red light induces a calcium transient in the moss Physcomitrella patens (Hedw.) B, S & G. Planta 206: 278-283CrossRefGoogle Scholar
  45. Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M and Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98: 6969-6974PubMedGoogle Scholar
  46. Sakamoto K and Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14: 1723-1735CrossRefPubMedGoogle Scholar
  47. Salomon M, Zacherl M and Rudiger W (1996) Changes in blue-light-dependent protein phosphorylation during the early de-velopment of etiolated oat seedlings. Planta 199: 336-342CrossRefPubMedGoogle Scholar
  48. Salomon M, Christie JM, Knieb E, Lempert U and Briggs WR (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39: 9401-9410CrossRefPubMedGoogle Scholar
  49. Sato Y, Kadota A and Wada M (1999) Mechanically induced avoidance response of chloroplasts in fern protonemal cells. Plant Physiol 121: 37-44CrossRefPubMedGoogle Scholar
  50. Sato Y, Wada M and Kadota A (2001a) Choice of tracks, micro-tubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light re-ceptor. J Cell Sci 114: 269-279Google Scholar
  51. Sato Y, Wada M and Kadota A (2001b) External Ca2+ is essential for chloroplast movement induced by mechanical stimulation but not by light stimulation. Plant Physiol 127: 497-504CrossRefGoogle Scholar
  52. Sato Y, Kadota A and Wada M (2003a) Chloroplast movement: dissection of events downstream of photo- and mechano-perception. J Plant Res 116: 1-5Google Scholar
  53. Sato Y, Wada M and Kadota A (2003b) Accumulation response of chloroplasts induced by mechanical stimulation in bryophyte cells. Planta 216: 772-777Google Scholar
  54. Schonbohm E, Schonbohm E and Meyer-Wegener J (1990a) On the signal-transduction chains of two Pfr -mediated short-term processes: increase of anchorage and movement of Mougeotia chloroplasts. Photochem Photobiophys 52: 203-209CrossRefGoogle Scholar
  55. Schonbohm E, Meyer-Wegener J and Schonbohm E (1990b) No evidence for Ca2+ influx as an essential link in the signal transduction chains of either light-oriented chloroplast move-ments or Pfr -mediated chloroplast anchorage in Mougeotia. J Photochem Photobiol B: Biol 5: 331-341CrossRefGoogle Scholar
  56. Serlin BS and Roux SJ (1984) Modulation of chloroplast move-ment in the green alga Mougeotia by the Ca2+ ionophore A23187 and by calmodulin antagonists. Proc Natl Acad Sci USA 81: 6368-6372CrossRefPubMedGoogle Scholar
  57. Sharma VK, Jain PK, Maheshwari SC and Khurana JP (1997) Rapid blue-light-induced phosphorylation of plasma-membrane-associated proteins in wheat. Phytochemistry 44: 775-780CrossRefGoogle Scholar
  58. Short TW, Reymond P and Briggs WR (1993) A pea plasma-membrane protein exhibiting blue light-induced phosphory-lation retains photosensitivity following triton solubilization. Plant Physiol 101: 647-655PubMedGoogle Scholar
  59. Smith H (2000) Phytochromes and light signal perception by plants: an emerging synthesis. Nature 407: 585-591CrossRefPubMedGoogle Scholar
  60. Stoelzle S, Kagawa T, Wada M, Hedrich R and Dietrich P (2003) Blue light activates calcium-permeable channels in Arabidop-sis mesophyll cells via the phototropin signaling pathway. Proc Natl Acad Sci USA 100: 1456-1461CrossRefPubMedGoogle Scholar
  61. Suetsugu N, Mittmann F, Wagner G, Hughes J and Wada M (2005) A chimeric photoreceptor gene, NEOCHROME, has arisen twice during plant evolution. Proc Natl Acad Sci USA 102: 13705-13709CrossRefPubMedGoogle Scholar
  62. Takagi S, Kamitsubo E and Nagai R (1991) Light-induced changes in the behavior of chloroplasts under centrifuga-tion in Vallisneria epidermal cells. J Plant Physiol 138: 257-262Google Scholar
  63. Tlalka M and Gabrys H (1993) Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L. Planta 189: 491-498CrossRefGoogle Scholar
  64. Tlalka M, Runquist M and Fricker M (1999) Light perception and the role of the xanthophyll cycle in blue-light-dependent chloroplast movements in Lemna trisulca L. Plant J 20: 447-459CrossRefPubMedGoogle Scholar
  65. Trojan A and Gabrys H (1996) Chloroplast distribution in Arabidopsis thaliana (L.) depends on light conditions during growth. Plant Physiol 111: 419-425PubMedGoogle Scholar
  66. Wada M and Kagawa T (2001) Light-controlled chloroplast movement. In: H äder D-P and Lebert M (eds) Photomove-ment, pp 824-897. Elsevier, Amsterdam.Google Scholar
  67. Wada M, Grolig F and Haupt W (1993) Light-oriented chloro-plast positioning: contribution to progress in photobiology. J Photochem Photobiol B 17: 3-25CrossRefGoogle Scholar
  68. Wada M, Kagawa T and Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54: 455-468CrossRefPubMedGoogle Scholar
  69. Yatsuhashi H (1996) Photoregulation systems for light-oriented chloroplast movement. J Plant Res 109: 139-146CrossRefGoogle Scholar
  70. Yatsuhashi H, Kadota A and Wada M (1985) Blue-light and red-light action in photoorientation of chloroplasts in Adiantum protonemata. Planta 165: 43-50CrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Yoshikatsu Sato
    • 1
  • Akeo Kadota
    • 2
  1. 1.Division of Evolutionary BiologyNational Institute for Basic BiologyMyodaijiJapan
  2. 2.Department of Biological Sciences, Graduate School of ScienceTokyo Metropolitan UniversityHachiojiJapan

Personalised recommendations