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Distribution pattern changes of actin filaments during chloroplast movement in Adiantum capillus-veneris

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Abstract

Chloroplasts change their positions in a cell in response to light intensities. The photoreceptors involved in chloroplast photo-relocation movements and the behavior of chloroplasts during their migration were identified in our previous studies, but the mechanism of movement has yet to be clarified. In this study, the behavior of actin filaments under various light conditions was observed in Adiantum capillus-veneris gametophytes. In chloroplasts staying in one place under a weak light condition and not moving, circular structures composed of actin filaments were observed around the chloroplast periphery. In contrast, short actin filaments were observed at the leading edge of moving chloroplasts induced by partial cell irradiation. In the dark, the circular structures found under the weak light condition disappeared and then reappeared around the moving chloroplasts. Mutant analyses revealed that the disappearance of the circular actin structure was mediated by the blue light photoreceptor, phototropin2.

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References

  • 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

    Article  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

    Article  CAS  Google Scholar 

  • Haupt W (1999) Chloroplast movement: from phenomenology to molecular biology. Progress Bot 60:3–36

    Article  CAS  Google Scholar 

  • Kadota A, Wada M (1989) Photoinduction of circular F-actin on chloroplast in a fern protonemal cell. Protoplasma 151:171–174

    Google Scholar 

  • Kadota A, Wada M (1992a) Reorganization of the cortical cytoskeleton in tip-growing fern protonemal cells during phytochrome-mediated phototropism and blue light-induced apical swelling. Protoplasma 166:35–41

    Article  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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  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 homologue controlling the chloroplast high-light avoidance response. Science 291:2138–2141

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kodama Y, Suetsugu N, Kong SG, Wada M (2010) Two interacting coiled-coil proteins, WEB1 and PMI2, maintain the chloroplast photorelocation movement velocity in Arabidopsis. Proc Natl Acad Sci USA 107:19591–19596

    Article  PubMed  CAS  Google Scholar 

  • Krzeszowiec W, Rajwa B, Dobrucki J, Gabryś H (2007) Actin cytoskeleton in Arabidopsis thaliana under blue and red light. Biol Cell 99:251–260

    Article  PubMed  CAS  Google Scholar 

  • Kumatani T, Sakurai-Ozato N, Miyawaki N, Yokota E, Shimmen T, Terashima T, Takagi S (2006) Possible association of actin filaments with chloroplasts of spinach mesophyll cells in vivo and in vitro. Protoplasma 229:45–52

    Article  PubMed  CAS  Google Scholar 

  • Nozue K, Kanegae T, Imaizumi T, Fukuda S, Okamoto H, Yeh KC, Lagarias JC, Wada M (1998) A phytochorme from the fern Adiantum with features of the putative photoreceptor NPH1. Proc Natl Acad Sci USA 95:15826–15830

    Article  PubMed  CAS  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  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoylN-hydroxysuccinimide ester. Protoplasma 148:80–86

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQ, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:8860–8865

    Google Scholar 

  • Tsuboi H, Wada M (2010) Speed of signal transfer in the chloroplast accumulation response. J Plant Res 123:381–390

    Article  PubMed  CAS  Google Scholar 

  • Tsuboi H, Wada M (2011a) Chloroplast can move in any direction to avoid strong light. J Plant Res 124:201–210

    Article  PubMed  Google Scholar 

  • Tsuboi H, Wada M (2011b) Chloroplasts move towards the nearest anticlinal walls under dark condition. J Plant Res (in press)

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tsuboi H, Yamashita H, Wada M (2009) Chloroplasts do not have a polarity for light-induced accumulation movement. J Plant Res 122:131–140

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 24:1441–1447

    CAS  Google Scholar 

  • Whippo CW, Khurana P, Davis PA, DeBlasio SL, DeSloover D, Staiger CJ, Hangarter RP (2011) THRUMIN1 is a light-regulated actin-bundling protein involved in chloroplast motility. Curr Biol 21:59–64

    Article  PubMed  CAS  Google Scholar 

  • Yamashita H, Sato Y, Kanegae T, Kagawa T, Wada M, Kadota A (2011) Chloroplast actin filaments organize meshwork on the photorelocated chloroplasts in the moss Physcomitrella patens. Planta 233:357–368

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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Acknowledgments

This work was partially supported by the Japanese Ministry of Education, Sports, Science and Technology (MEXT 17084006 to M.W.) and the Japan Society for the Promotion of Science (JSPS 16107002 and 20227001 to M.W.).

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Correspondence to Masamitsu Wada.

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Tsuboi, H., Wada, M. Distribution pattern changes of actin filaments during chloroplast movement in Adiantum capillus-veneris . J Plant Res 125, 417–428 (2012). https://doi.org/10.1007/s10265-011-0444-8

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