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Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of Vallisneria gigantea

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Abstract

In leaf epidermal cells of the aquatic angiosperm Vallisneria gigantea Graebner, high-intensity blue light induces the actin-dependent avoidance response of chloroplasts. By semi-quantitative motion analysis and phalloidin staining, time courses of the blue-light-induced changes in the mode of movement of individual chloroplasts and in the configuration of actin filaments were examined in the presence and absence of a flavoprotein inhibitor, diphenylene iodonium. In dark-adapted cells, short, thick actin bundles seemed to surround each chloroplast, which was kept motionless in the outer periclinal cytoplasm of the cells. After 10 min of irradiation with high-intensity blue light, a rapid, unidirectional movement of chloroplasts was induced, concomitant with the appearance of aggregated, straight actin bundles stretched over the outer periclinal cytoplasm. Diphenylene iodonium inhibited the avoidance response of chloroplasts, apparently by delaying a change in the mode of chloroplast movement from random sway to unidirectional migration, by suppressing the appearance of aggregated, straight actin bundles. In partially irradiated individual cells, redistribution of chloroplasts and reorganization of actin filaments occurred only in the areas exposed to blue light. From the results, we propose that the short, thick actin bundles in the vicinity of chloroplasts function to anchor the chloroplasts in dark-adapted cells, and that the aggregated, straight actin bundles organized under blue-light irradiation provide tracks for unidirectional movement of chloroplasts.

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Fig. 1
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Abbreviations

DPI :

Diphenylene iodonium

P-side :

Cytoplasmic layer that faces the outer periclinal wall

References

  • Blatt MR, Briggs WR (1980) Blue-light-induced cortical fiber reticulation concomitant with chloroplast aggregation in the alga Vaucheria sessilis. Planta 147:355–362

    Article  Google Scholar 

  • Blatt MR, Wessells NK, Briggs WR (1980) Actin and cortical fiber reticulation in the siphonaceous alga Vaucheria sessilis. Planta 147:363–375

    Article  CAS  Google Scholar 

  • Christie JM, Salomon M, Nozue K, Wada M, Briggs WR (1999) LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc Natl Acad Sci USA 96:8779–8783

    Article  CAS  PubMed  Google Scholar 

  • Christie JM, Swartz TE, Bogomolni RA, Briggs WR (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32:205–219.

    Article  CAS  PubMed  Google Scholar 

  • Cox G, Hawes CR, van der Lubbe L, Juniper BE (1987) High-voltage electron microscopy of whole, critical-point dried plant cells 2. Cytoskeletal structures and plastid motility in Selaginella. Protoplasma 140:173–186

    Google Scholar 

  • Dong XJ, Ryu JH, Takagi S, Nagai R (1996) Dynamic changes in the organization of microfilaments associated with the photocontrolled motility of chloroplasts in epidermal cells of Vallisneria. Protoplasma 195:18–24

    CAS  Google Scholar 

  • Dong XJ, Nagai R, Takagi S (1998) Microfilaments anchor chloroplasts along the outer periclinal wall in Vallisneria epidermal cells through cooperation of Pfr and photosynthesis. Plant Cell Physiol 39:1299–1306

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Haupt W, Scheuerlein R (1990) Chloroplast movement. Plant Cell Environ 13:595–614

    Google Scholar 

  • Izutani Y, Takagi S, Nagai R (1990) Orientation movements of chloroplasts in Vallisneria epidermal cells: different effects of light at low- and high-fluence rate. Photochem Photobiol 51:105–111

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kadota A, Wada M (1992a) Photoinduction of formation of circular structures by microfilaments on chloroplasts during intracellular orientation in protonemal cells of the fern Adiantum capillus-veneris. Protoplasma 167:97–107

    Google Scholar 

  • Kadota A, Wada M (1992b) Photoorientation of chloroplasts in protonemal cells of the fern Adiantum as analyzed by use of a video-tracking system. Bot Mag Tokyo 105:265–279

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kandasamy MK, Meagher RB (1999) Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskel 44:110–118

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kinoshita T, Emi T, Doi M, Shimazaki K (2002) Phosphorylation, 14-3-3 protein and photoreceptor in blue light response of stomatal guard cells. J Photosci 9:335–337

    CAS  Google Scholar 

  • Liscum E, Briggs WR (1995) Mutations in the NPH1 locus disrupt the perception of phototropic stimuli. Plant Cell 7:473–485

    Article  CAS  PubMed  Google Scholar 

  • McCurdy DW, Kovar DR, Staiger CJ (2001) Actin and actin-binding proteins in higher plants. Protoplasma 215:89–104

    CAS  PubMed  Google Scholar 

  • Mineyuki Y, Kataoka H, Masuda Y, Nagai R (1995) Dynamic changes in the actin cytoskeleton during the high-fluence rate response of the Mougeotia chloroplast. Protoplasma 185:222–229

    CAS  Google Scholar 

  • Nagai R (1993) Regulation of intracellular movements in plant cells by environmental stimuli. Int Rev Cytol 145:251–310

    CAS  Google Scholar 

  • O’Donnell VB, Tew DG, Jones OTG, England PJ (1993) Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem J 290:41–49

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Park Y-I, Chow WS, Anderson JM (1996) Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. Plant Physiol 111:867–875

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto K, Briggs WR (2002) Cellular and subcellular localization of phototropin 1. Plant Cell 14:1723–1735

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Wada M, Kadota A (2001) 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 114:269–279

    CAS  PubMed  Google Scholar 

  • Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51:257–288

    Article  CAS  PubMed  Google Scholar 

  • Takagi S (2003) Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206:1963–1969

    Article  CAS  PubMed  Google Scholar 

  • Takagi S, Nagai R (1985) Light-controlled cytoplasmic streaming in Vallisneria mesophyll cells. Plant Cell Physiol 26:941–951

    CAS  Google Scholar 

  • Takagi S, Kong SG, Mineyuki Y, Furuya M (2003) Regulation of actin-dependent cytoplasmic motility by type II phytochrome occurs within seconds in Vallisneria epidermal cells. Plant Cell 15:331–345

    Article  CAS  PubMed  Google Scholar 

  • Tlałka M, Runquist M, Fricker M (1999) Light perception and the role of the xanthophyll cycle in blue-light-dependent chloroplast movements in Lemna trisulca L. Plant J 20:447–459

    Article  PubMed  Google Scholar 

  • Wada M, Kagawa T (2001) Light-controlled chloroplast movement. In: Häder D-P, Lebert M (eds) Photomovement. Elsevier, Amsterdam, pp 897–924

  • Wada M, Sugai M (1994) Photobiology of ferns. In: Kendrick RE, Kronenberg GHM (eds) Photomorphogenesis in plants. Kluwer, Dordrecht, pp 783–802

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

    CAS  Google Scholar 

  • Yamaguchi Y, Nagai R (1981) Motile apparatus in Vallisineria leaf cells. I. Organization of microfilaments. J Cell Sci 48:193–205

    CAS  PubMed  Google Scholar 

  • Yasuda R, Miyata H, Kinosita K Jr (1996) Direct measurement of the torsional rigidity of single actin filaments. J Mol Biol 263:227–236

    Article  CAS  PubMed  Google Scholar 

  • Yatsuhashi H (1996) Photoregulation systems for light-oriented chloroplast movement. J Plant Res 109:139–146

    CAS  Google Scholar 

  • Yatsuhashi H, Kadota A, Wada M (1985) Blue- and red-light action in photoorientation of chloroplasts in Adiantum protonemata. Planta 165:43–50

    Article  Google Scholar 

  • Zurzycki J (1955) Chloroplasts arrangement as a factor in photosynthesis. Acta Soc Bot Pol 24:27–63

    Google Scholar 

  • Zurzycki J (1957) The destructive effect of light on the photosynthetic apparatus. Acta Soc Bot Pol 26:157–175

    CAS  Google Scholar 

  • Zurzycki J (1962) The actin spectrum for the light dependent movements of chloroplasts in Lemna trisulca. Acta Soc Bot Pol 31:489–528

    Google Scholar 

  • Zurzycki J (1967) Properties and localization of the photoreceptor active displacements of chloroplasts in Funaria hygrometrica. II. Studies with polarized light. Acta Soc Bot Pol 36:143–152

    CAS  Google Scholar 

  • Zurzycki J (1972) Primary reactions in the chloroplast rearrangement. Acta Protozool 11:189–200

    CAS  Google Scholar 

  • Zurzycki J (1980) Blue light-induced intracellular movements. In: Senger H (ed) The blue light syndrome. Springer, Berlin, pp 50–68

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Acknowledgements

This work was partly supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture, Japan, to S.T. and by a Sasagawa Scientific Research Grant from the Japan Science Society to N.S.

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Author notes

  1. Kikuko Domoto

    Present address: Fujicco Co., Minatojima-Nakamachi 6-13-4, Chuo-ku, 650-8558, Kobe, Japan

Authors and Affiliations

  1. Department of Biology, Graduate School of Science, Osaka University, Machikaneyama 1-1, Toyonaka, 560-0043, Osaka, Japan

    Nami Sakurai, Kikuko Domoto & Shingo Takagi

Authors
  1. Nami Sakurai
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  2. Kikuko Domoto
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  3. Shingo Takagi
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Correspondence to Shingo Takagi.

Additional information

Preliminary results of part of the local irradiation study have already been reported in abstract form [N. Sakurai et al. (2002) J Photosci 9:326–328].

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Sakurai, N., Domoto, K. & Takagi, S. Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of Vallisneria gigantea. Planta 221, 66–74 (2005). https://doi.org/10.1007/s00425-004-1416-1

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