Abstract
Plants have evolved sophisticated mechanisms to survive in various environmental changes. Chloroplast movement is an essential response to optimize photosynthesis and to avoid photodamage under fluctuating light conditions. Chloroplasts accumulate at periclinal walls to maximize light absorption under weak light while they move to anticlinal walls to minimize light exposure under strong light. The light strength is monitored by blue light receptor phototropins in general. In Arabidopsis thaliana, both phototropin1 (phot1) and phototropin2 (phot2) are involved in accumulation response, but phot2 is specifically involved in avoidance response. Such appropriate photorelocation movements of chloroplasts are mediated by a structure made of short actin filaments specialized for chloroplast movement. The short actin filaments are dynamically reorganized on the leading edges of moving chloroplasts, so that named chloroplast actin (cp-actin) filaments. In this chapter, we summarize recent knowledge about cp-actin filaments and next challenges to elucidate the underlying mechanisms.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
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 9:64
Banaś AK, Aggarwal C, Łabuz J, Sztatelman O, Gabryś H (2012) Blue light signalling in chloroplast movements. J Exp Bot 63:1559–1574
Blanchoin L, Staiger CJ (2010) Plant formins: diverse isoforms and unique molecular mechanism. Biochim Biophys Acta 1803:201–206
Chalkia D, Nikolaidis N, Makalowski W, Klein J, Nei M (2008) Origins and evolution of the formin multigene family that is involved in the formation of actin filaments. Mol Biol Evol 25:2717–2733
DeBlasio SL, Mullen JL, Luesse DR, Hangarter RP (2003) Phytochrome modulation of blue light-induced chloroplast movements in Arabidopsis. Plant Physiol 133:1471–1479
Deeks MJ, Cvrckova F, Machesky LM, Mikitova V, Ketelaar T, Zarsky V, Davies B, Hussey PJ (2005) Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytol 168:529–540
Diao M, Ren S, Wang Q, Qian L, Shen J, Liu Y, Huang S (2018) Arabidopsis formin 2 regulates cell-to-cell trafficking by capping and stabilizing actin filaments at plasmodesmata. elife 7:e36316
Duan Z, Tominaga M (2018) Actin-myosin XI: an intracellular control network in plants. Biochem Biophys Res Commun 506:403–408
Firat-Karalar EN, Welch MD (2011) New mechanisms and functions of actin nucleation. Curr Opin Cell Biol 23:4–13
Goley ED, Welch MD (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713–726
Haupt W (1956) Chloroplastenbewegung. Z Bot 44:455–462
Higa T, Hasegawa S, Hayasaki Y, Kodama Y, Wada M (2017) Temperature-dependent signal transmission in chloroplast accumulation response. J Plant Res 130:779–789
Ichikawa S, Yamada N, Suetsugu N, Wada M, Kadota A (2011) Red light, phot1 and JAC1 modulate phot2-dependent reorganization of chloroplast actin filaments and chloroplast avoidance movement. Plant Cell Physiol 52:1422–1432
Ingouff M, Fitz Gerald JN, Guerin C, Robert H, Sorensen MB, Van Damme D, Geelen D, Blanchoin L, Berger F (2005) Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat Cell Biol 7:374–380
Jaedicke K, Lichtenthaler AL, Meyberg R, Zeidler M, Hughes J (2012) A phytochrome-phototropin light signaling complex at the plasma membrane. Proc Natl Acad Sci U S A 109:12231–12236
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
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
Kadota A, Sato Y, Wada M (2000) Intracellular chloroplast photorelocation in the moss Physcomitrella patens is mediated by phytochrome as well as by a blue-light receptor. Planta 210:932–937
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 U S A 106:13106–13111
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
Kagawa T, Wada M (2004) Velocity of chloroplast avoidance movement is fluence rate dependent. Photochem Photobiol Sci 3:592–595
Kandasamy MK, Meagher RB (1999) Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskeleton 44:110–118
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
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
Kong S-G, Arai Y, Suetsugu N, Yanagida T, Wada M (2013) Rapid severing and motility of chloroplast-actin filaments are required for the chloroplast avoidance response in Arabidopsis. Plant Cell 25:572–590
Krzeszowiec W, Gabryś H (2007) Phototropin mediated relocation of myosins in Arabidopsis thaliana. Plant Signal Behav 2:333–336
Krzeszowiec W, Rajwa B, Dobrucki J, Gabryś H (2007) Actin cytoskeleton in Arabidopsis thaliana under blue and red light. Biol Cell 99:251–260
Kumatani T, Sakurai-Ozato N, Miyawaki N, Yokota E, Shimmen T, Terashima I, Takagi S (2006) Possible association of actin filaments with chloroplasts of spinach mesophyll cells in vivo and in vitro. Protoplasma 229:45–52
Lan Y, Liu X, Fu Y, Huang S (2018) Arabidopsis class I formins control membrane-originated actin polymerization at pollen tube tips. PLoS Genet 14:e1007789
Li FW, Mathews S (2016) Evolutionary aspects of plant photoreceptors. J Plant Res 129:115–122
Li Y, Shen Y, Cai C, Zhong C, Zhu L, Yuan M, Ren H (2010) The type II Arabidopsis formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell 22:2710–2726
Li FW, Villarreal JC, Kelly S, Rothfels CJ, Melkonian M, Frangedakis E, Ruhsam M, Sigel EM, Der JP, Pittermann J, Burge DO, Pokorny L, Larsson A, Chen T, Weststrand S, Thomas P, Carpenter E, Zhang Y, Tian Z, Chen L, Yan Z, Zhu Y, Sun X, Wang J, Stevenson DW, Crandall-Stotler BJ, Shaw AJ, Deyholos MK, Soltis DE, Graham SW, Windham MD, Langdale JA, Wong GK, Mathews S, Pryer KM (2014) Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. Proc Natl Acad Sci U S A 111:6672–6677
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 U S A 95:15826–15830
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
Oikawa K, Yamasato A, Kong S-G, Kasahara M, Nakai M, Takahashi F, Ogura Y, Kagawa T, Wada M (2008) Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol 148:829–842
Paves H, Truve E (2007) Myosin inhibitors block accumulation movement of chloroplasts in Arabidopsis thaliana leaf cells. Protoplasma 230:165–169
Sakai Y, Takagi S (2005) Reorganized actin filaments anchor chloroplasts along the anticlinal walls of Vallisneria epidermal cells under high-intensity blue light. Planta 221:823–830
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
Sattarzadeh A, Krahmer J, Germain AD, Hanson MR (2009) A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana. Mol Plant 2(6):1351–1358
Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzen-Chromatophoren. Wilhelm Engelmann, Leipzig
Sparkes I (2011) Recent advances in understanding plant myosin function: life in the fast lane. Mol Plant 4:805–812
Suetsugu N, Wada M (2016) Evolution of the cp-actin-based motility system of chloroplasts in green plants. Front Plant Sci 7:561
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 U S A 102:13705–13709
Suetsugu N, Dolja VV, Wada M (2010a) Why have chloroplasts developed a unique motility system? Plant Signal Behav 5:1190–1196
Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010b) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:8860–8865
Suetsugu N, Sato Y, Tsuboi H, Kasahara M, Imaizumi T, Kagawa T, Hiwatashi Y, Hasebe M, Wada M (2012) The KAC family of kinesin-like proteins is essential for the association of chloroplasts with the plasma membrane in land plants. Plant Cell Physiol 53:1854–1865
Suetsugu N, Higa T, Gotoh E, Wada M (2016) Light-induced movements of chloroplasts and nuclei are regulated in both cp-actin-filament-dependent and -independent manners in Arabidopsis thaliana. PLoS One 11:e0157429
Takagi S (2000) Roles for actin filaments in chloroplast motility and anchoring. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer Academic, Dordrecht, The Netherlands, pp 203–212
Takagi S (2003) Actin-based photo-orientation movement of chloroplasts in plant cells. J Exp Biol 206:1963–1969
Takagi S, Takamatsu H, Sakurai-Ozato N (2009) Chloroplast anchoring: its implications for the regulation of intracellular chloroplast distribution. J Exp Bot 60:3301–3310
Takamatsu H, Takagi S (2011) Actin-dependent chloroplast anchoring is regulated by Ca2+-calmodulin in spinach mesophyll cells. Plant Cell Physiol 52:1973–1982
Tsuboi H, Wada M (2011) Chloroplasts can move in any direction to avoid strong light. J Plant Res 124:201–210
Usami H, Maeda T, Fujii Y, Oikawa K, Takahashi F, Kagawa T, Wada M, Kasahara M (2012) CHUP1 mediates actin-based light-induced chloroplast avoidance movement in the moss Physcomitrella patens. Planta 236:1889–1897
van Gisbergen PA, Bezanilla M (2013) Plant formins: membrane anchors for actin polymerization. Trends Cell Biol 23:227–233
Wada M (2013) Chloroplast movement. Plant Sci 210:177–182
Wada M (2016) Chloroplast and nuclear photorelocation movements. Proc Jpn Acad Ser B Phys Biol Sci 92:387–411
Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468
Wada M, Kong S-G (2018) Actin-mediated movement of chloroplasts. J Cell Sci 131:jcs210310
Wang J, Xue X, Ren H (2012) New insights into the role of plant formins: regulating the organization of the actin and microtubule cytoskeleton. Protoplasma 249(Suppl 2):S101–S107
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
Yamada N, Suetsugu N, Wada M, Kadota A (2011) Phototropin-dependent biased relocalization of cp-actin filaments can be induced even when chloroplast movement is inhibited. Plant Signal Behav 6:1651–1653
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
Ye J, Zheng Y, Yan A, Chen N, Wang Z, Huang S, Yang Z (2009) Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell 21:3868–3884
Zurzycki J (1955) Chloroplast arrangement as a factor in photosynthesis. Acta Soc Bot Pol 24:27–63
Acknowledgment
The work was supported by the grants from the Japan Society for the Promotion of Science (JSPS) (No. 20227001, 23120523, 25120721, 25251033, and 16K14758) and from Ohsumi Frontier Science Foundation to M.W. and by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (No. 2016R1D1A3B03935947) and the Next-Generation BioGreen 21 Program grant funded by the Korea government Rural Development Administration (RDA) (No. PJ01366901) to S.-G. K.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Wada, M., Kong, SG. (2019). Chloroplast Actin Filaments Involved in Chloroplast Photorelocation Movements. In: Sahi, V., Baluška, F. (eds) The Cytoskeleton. Plant Cell Monographs, vol 24. Springer, Cham. https://doi.org/10.1007/978-3-030-33528-1_3
Download citation
DOI: https://doi.org/10.1007/978-3-030-33528-1_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-33527-4
Online ISBN: 978-3-030-33528-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)