Abstract
This chapter presents updated information on organelle movements in plant cells, with attention focused on photosynthesizing cells. The first part summarizes current knowledge on cytoskeletal and motor proteins which integrate the intracellular communication and transport phenomena. Next, the relationship between cytoplasmic streaming and organelle motility is discussed, including recent models of hydrodynamic flow in plant cells. Subsequently, organelle movements are characterized, starting from nonphotosynthesizing organelles: Golgi network, peroxisomes, mitochondria and nuclei, followed by the light-controlled redistribution of chloroplasts. Recent evidence pertaining to the mechanisms is presented, with a special focus on the involvement of the cytoskeletal elements/motor proteins.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Anielska-Mazur A, BernaĆ T, GabryĆ 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
Arnaud D, DĂ©jardin A, LeplĂ© JC, Lesage-Descauses MC, Pilate G (2007) Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Res 14:103â116
Avisar D, Prokhnevsky AI, Makarova KS, Koonin EV, Dolja VV (2008) Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol 146:1098â1108
Boevink P, Oparka K, Santa Cruz S, Martin B, Bettridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on actin/ER network. Plant J 15:441â447
Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204â210
Britz S (1979) Chloroplast and nuclear migration. Encycl Plant Physiol 7:170â205
Burkhardt JK (1998) The role of microtubule-based motor proteins in maintaining the structure and function of the Golgi complex. Biochim Biophys Acta 1404:113â126
CĂĄrdenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol 146:1611â1621
Chen H, Bernstein BW, Bamburg JR (2000) Regulating actin-filament dynamics in vivo. Trends Biochem Sci 25:19â23
Chen MH, Huang LF, Li HM, Chen YR, Yu SM (2004) Signal peptide-dependent targeting of rice α-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol 135:1367â1377
Cheung AY, Duan QH, Costa SS, de Graaf BHJ, Di Stilio VS, Feijo J, Wu HM (2008) The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubule-binding reporter proteins. Mol Plant 1:686â702
daSilva LL, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F (2004) Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16:1753â1771
De La Cruz EM, Wells AL, Rosenfeld SS, Ostap EM, Sweeney HL (1999) The kinetic mechanism of myosin V. Proc Natl Acad Sci USA 96:13726â13731
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 195:18â24
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 39:1299â1306
DorĂ©e M, Pickard A (1980) Release of Ca2+ from intracellular pools stops cytoplasmic streaming in Tradescantia staminal hairs. Experientia 36:1291â1292
Esseling-Ozdoba A, Houtman D, Van Lammeren AAM, Eiser E, Emons AMC (2008) Hydrodynamic flow in the cytoplasm of plant cells. J Microsc 231:274â283
Forde J, Steer MW (1976) Cytoplasmic streaming in Elodea. Can J Bot 54:2688â2694
Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 12:2349â2363
Goddard RH, Wick SM, Silflow CD, Snustad DP (1994) Microtubule components of the plant cell cytoskeleton. Plant Physiol 104:1â6
Goldstein RE, Tuval I, van de Meent JW (2008) Microfluidics of cytoplasmic streaming and its implications for intracellular transport. Proc Natl Acad Sci USA 105:3663â3667
Hardham AR, Gunning BE (1978) Structure of cortical microtubule arrays in plant cells. J Cell Biol 77:14â34
Hashimoto K, Igarashi H, Mano S, Nishimura M, Shimmen T, Yokota E (2005) Peroxisomal localization of a myosin XI isoform in Arabidopsis thaliana. Plant Cell Physiol 46:782â789
Haupt W (1999) Chloroplast movement: from phenomenology to molecular biology. Prog Bot 60:3â36
Haupt W, Scheuerlein R (1990) Chloroplast movement. Plant Cell Environ 13:595â614
Hawes C, Satiat-Jeunemaitre B (2005) The plant Golgi apparatus â going with the flow. Biochim Biophys Acta 1744:93â107
Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159â187
Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10:682â696
Holmes KC, Popp D, Gebhard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44â49
Ingouff M, Fitz Gerald JN, GuĂ©rin C, Robert H, SĂžrensen 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 4:374â380
Islam MdS, Niwa Y, Takagi S (2009) Light dependent intracellular positioning of mitochondria in Arabidopsis thaliana mesophyll cells. Plant Cell Physiol 50:1032â1040
Iwabuchi K, Sakai T, Takagi S (2007) Blue light-dependent nuclear positioning in Arabidopsis thaliana leaf cells. Plant Cell Physiol 48:1291â1298
Iwabuchi K, Minamino R, Takagi S (2010) Actin reorganization underlies phototropin-dependent positioning of nuclei in Arabidopsis thaliana leaf cells. Plant Physiol 152:1309â1319
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 51:105â111
Jarillo JA, GabryĆ H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL-1 controls chloroplast relocation induced by blue light. Nature 410:952â954
Jedd G, Chua N-H (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol 43:384â392
Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin:DNase I complex. Nature 347:37â44
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 106:13106â13111
Kagawa T, Wada M (1993) Light-dependent nuclear positioning in prothallial cells of Adiantum capillus-veneris. Protoplasma 177:82â85
Kamiya N, Kuroda K (1956) Velocity distribution of the protoplasmic streaming in Nitella cells. Bot Mag Tokyo 69:544â554
Kao YL, Deavours BE, Phelps KK, Walker RA, Reddy AS (2000) Bundling of microtubules by motor and tail domains of a kinesin-like calmodulin-binding protein from Arabidopsis: regulation by Ca2+/Calmodulin. Biochem Biophys Res Commun 267:201â207
Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829â832
Kato N, Reynolds D, Brown ML, Boisdore M, Fujikawa Y, Morales A, Meisel Lee A (2008) Multidimensional fluorescence microscopy of multiple organelles in Arabidopsis seedlings. Plant Methods 4:1â14
Katsuta J, Shibaoka H (1988) The roles of the cytoskeleton and the cell wall in nuclear positioning in tobacco BY-2 cells. Plant Cell Physiol 29:403â413
Katsuta J, Hashiguchi Y, Shibaoka H (1990) The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. J Cell Sci 95:413â422
Ketelaar T, de Ruijter NC, Emons AM (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285â292
Knight AE, Kendrick-Jones J (1993) A myosin-like protein from a higher plant. J Mol Biol 231:148â154
Kohno T, Shimmen T (1988) Mechanism of Ca2+ inhibition of cytoplasmic streaming in lily pollen tubes. J Cell Sci 91:501â509
Kovar DR, Staiger CJ, Weaver EA, McCurdy DW (2000) AtFim1 is an actin filament crosslinking protein from Arabidopsis thaliana. Plant J 24:625â636
Krzeszowiec W, GabryĆ H (2007) Blue light-induced reorganization of myosins in Arabidopsis thaliana. Plant Signal Behav 2:333â336
Krzeszowiec W, Rajwa B, Dobrucki J, GabryĆ H (2007) Actin cytoskeleton in Arabidopsis thaliana under blue and red light. Biol Cell 99:251â260
Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LS, Goodson HV, Hirokawa N, Howard J, Malmberg RL, McIntosh JR, Miki H, Mitchison TJ, Okada Y, Reddy AS, Saxton WM, Schliwa M, Scholey JM, Vale RD, Walczak CE, Wordeman L (2004) A standardized kinesin nomenclature. J Cell Biol 167:19â22
Lawrence CJ, Morris NR, Meagher RB, Dawe RK (2001) Dyneins have run their course in plant lineage. Traffic 2:362â363
Lee YR, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136:3877â3883
Lenartowska M, Michalska A (2008) Actin filament organization and polarity in pollen tubes revealed by myosin II subfragment I decoration. Planta 228:891â896
Li JF, NebenfĂŒhr A (2007) Organelle targeting of myosin XI is mediated by two globular tail subdomains with separate cargo binding sites. J Biol Chem 282:20593â20602
Liu L, Lee YR, Pan R, Maloof JN, Liu B (2005) An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arbidopsis. Mol Biol Cell 16:811â823
Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK (2005) Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221:95â104
Ma YZ, Yen LF (1989) Actin and myosin in pea tendrils. Plant Physiol 89:586â589
Mathur J, Mathur J, HĂŒlskamp M (2002) Simultaneous visualization of peroxisomes and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants. Plant Physiol 128:1031â1045
Michelot A, GuĂ©rin C, Huang S, Ingouff M, Richard S, Rodiuc N, Staiger CJ, Blanchoin L (2005) The formin homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis FORMIN1. Plant Cell 17:2296â2313
NebenfĂŒhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127â1141
Nick P (2008) Plant microtubules: development and flexibility. Springer, Berlin
Nogales E, Whittaker M, Milligan RA, Downing KH (1999) High-resolution model of the microtubule. Cell 96:79â88
Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning 1 is essential for proper chloroplast positioning. Plant Cell 15:2805â2815
Palevitz BA, Hepler PK (1975) Identification of actin in situ at the ectoplasm-endoplasm interface of Nitella, Microfilament-chloroplast association. J Cell Biol 65:29â38
Park YI, Chow WS, Anderson JM (1996) Chloroplast movement in the shade plant Tradescantia albiflora helps protect photosystem II against light stress. Plant Physiol 111:867â875
Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146:1109â1116
Reddy AS, Day IS (2001) Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence. Genome Biol 7:0024
Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M (2007) Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol 48:345â361
Runions J, Brach T, KĂŒhner S, Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot 57:43â50
Ruthardt N, Gulde N, Spiegel H, Fischer R, Emans N (2005) Four-dimensional imaging of cytoplasmic strand dynamics in tobacco BY-2 cells. Protoplasma 225:205â215
Ryu JH, Takagi S, Nagai R (1995) Stationary organization of the actin cytoskeleton in Vallisneria: the role of stable microfilaments at the end walls. J Cell Sci 108:1531â1539
Ryu JH, Mizuno K, Takagi S, Nagai R (1997) Extracellular components implicated in the stationary organization of the actin cytoskeleton in mesophyll cells of Vallisneria. Plant Cell Physiol 38:420â432
Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969â6974
Sakai Y, Takagi S (2005) Reorganized actin filaments anchor chloroplasts along the anticlinal walls of Vallisneria epidermal cells under high-intensity blue light. Planta 221:823â830
Sakurai N, Domoto K, Takagi S (2005) Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of Vallisneria gigantea. Planta 221:66â74
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 114:269â279
Shimmen T (2007) The sliding theory of cytoplasmic streaming: fifty years of progress. J Plant Res 120:31â43
Sowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ (2002) Signal-mediated depolymerization of actin in pollen during the self-incompatibility response. Plant Cell 14:2613â2626
Staehelin AL, Kang BH (2008) Nanoscale architecture of endoplasmic reticulum export sites and of Golgi membranes as determined by electron tomography. Plant Physiol 147:1454â1468
Staiger CJ, Hussey PJ (2004) Actin and actin-modulating proteins. In: Hussey PJ (ed) The plant cytoskeleton in cell differentiation and development. Blackwell, London, pp 32â80
Staiger CJ, Schliwa M (1987) Actin localization and function in higher plants. Protoplasma 41:1â12
Staiger CJ, Sheahan MB, Khurana P, Wang X, McCurdy DW, Blanchoin L (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J Cell Biol 184:269â280
Su H, Wang T, Dong H, Ren H (2007) The Villin/Gelsolin/Fragmin superfamily proteins in plants. J Integr Plant Biol 49:1183â1191
Sugi H, Chaen S (2003) Force-velocity relationships in actin-myosin interactions causing cytoplasmic streaming in algal cells. J Exp Biol 206:1971â1976
Sztatelman O, Waloszek A, BanaĆ AKB, GabryĆ H (2010) Photoprotective function of chloroplast avoidance movement: In vivo chlorophyll fluorescence study. J Plant Physiol 167:709â716
Takagi S (1997) Photoregulation of cytoplasmic streaming: cell biological dissection of signal transduction pathway. J Plant Res 110:299â303
Takagi S, Nagai R (1985) Light-controlled cytoplasmic streaming in Vallisneria mesophyll cells. Plant Cell Physiol 26:941â951
Takagi S, Kong SG, Mineyuki Y, Furuya M (2003) Regulation of actin-dependent cytoplasmic motility by type II phytochrome occurs within seconds in Vallisneria gigantea epidermal cells. Plant Cell 15:331â345
Takemiya A, Inoue S, Doi M, Kinoshita T, Shimazaki K (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17:1120â1127
Thomas C, Dieterle M, Gatti S, Hoffmann C, Moreau F, Papuga J, Steinmetz A (2008) Actin bundling via LIM domains. Plant Signal Behav 3:320â321
Thomas C, Tholl S, Moes D, Dieterle M, Papuga J, Moreau F, Steinmetz A (2009) Actin bundling in plants. Cell Motil Cytoskelet 66:940â957
Tominaga M, Kojima H, Yokota E, Orii H, Nakamori R, Katayama E, Anson M, Shimmen T, Oiwa K (2003) Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. EMBO J 22:1263â1272
Trojan A, GabryĆ H (1996) Chloroplast distribution in Arabidopsis thaliana depends on light conditions during growth. Plant Physiol 111:419â425
Vahey M, Titus M, Trautwein R, Scordilis S (1982) Tomato actin and myosin: contractile proteins from a higher plant. Cell Motil 2:131â147
Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112:467â480
Vale RD, Fletterick RJ (1997) The design plan of kinesin motors. Annu Rev Cell Dev Biol 13:745â777
van de Meent JW, Tuval I, Goldstein RE (2008) Natureâs microfluidic transporter: rotational cytoplasmic streaming at high Peclet numbers. Phys Rev Lett 101:178102
Van Gestel K, Köhler RH, Verbelen J-P (2002) Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J Exp Bot 53:659â667
Verchot-Lubicz J, Goldstein RE (2009) Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma 240:99â107
Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N et al (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7:1124â1131
Voigt B, Timmers ACJ, Samaj J, Muller J, Baluska F, Menzel D (2005) GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 84:595â608
Wada M, Suetsugu N (2004) Plant organelle positioning. Curr Opin Plant Biol 7:626â631
Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455â468
Wang Z, Pesacreta TC (2004) A subclass of myosin XI is associated with mitochondria, plastids, and the molecular chaperone subunit TCP-1alpha in maize. Cell Motil Cytoskelet 57:218â232
Wang HY, Yu Y, Chen ZL, Xia GX (2005) Functional characterization of Gossypium hirsutum profilin 1 gene (GhPFN1) in tobacco suspension cells. Characterization of in vivo functions of a cotton profilin gene. Planta 222:594â603
Wang HJ, Wan AR, Jauh GY (2008) An actin-binding protein, LlLIM1, mediates calcium and hydrogen regulation of actin dynamics in pollen tubes. Plant Physiol 147:1619â1636
Wasteneys GO, Galway ME (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54:691â722
Williamson RE (1974) Actin in the alga Chara corallina. Nature 248:801â802
Williamson RE (1992) Cytoplasmic streaming in characean algae: mechanism, regulation by Ca2+, and organization. In: Melkonian M (ed) Algal cell motility. Chapman and Hall, New York, pp 73â97
Williamson RE, Ashley CC (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature 296:647â651
Woehlke G, Schliwa M (2000) Directional motility of kinesin motor proteins. Biochim Biophys Acta 1496:117â1127
Wojtaszek P, Anielska-Mazur A, GabryĆ H, BaluĆĄka F, Volkmann D (2005) Recruitment of myosin VIII towards plastid surfaces is root cap-specific and provides the evidence for actomyosin involvement in root osmosensing. Funct Plant Biol 32:721â736
Woods CM, Polito VS, Reid MS (1984) Response to chilling stress in plant cells II. Redistribution of intracellular calcium. Protoplasma 121:17â24
Yang Yd, Elamawi R, Bubeck J, Peperkok R, Ritzenthaler C, Robinson DG (2005) Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotiana tabacum BY-2 cells provides evidence for transient association of Golgi stacks with endoplasmic reticulum exit sites. Plant Cell 17:1513â1531
Zheng M, Beck M, MĂŒller J, Chen T, Wang X, Wang F, Wang Q, Wang Y, BaluĆĄka F, Logan DC, Ć amaj J, Lin J (2009) Actin turnover is required for myosin-dependent mitochondrial movements in Arabidopsis root hairs. PloS ONE 4:e5961
Zurzycki J (1955) Chloroplast arrangements as a factor in photosynthesis. Acta Soc Bot Pol 24:27â63
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Krzeszowiec, W., GabryĆ, H. (2011). Intracellular Movements: Integration at the Cellular Level as Reflected in the Organization of Organelle Movements. In: Wojtaszek, P. (eds) Mechanical Integration of Plant Cells and Plants. Signaling and Communication in Plants, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19091-9_4
Download citation
DOI: https://doi.org/10.1007/978-3-642-19091-9_4
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-19090-2
Online ISBN: 978-3-642-19091-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)