Abstract
Gravisensing cells (statocytes) from plant root caps are characterized by a polar arrangement of organelles and sedimented amyloplast-based statoliths. Immunofluorescence microscopy fails to visualize prominent actin filaments in statocytes but indicates a highly dynamic cytoskeletal network, composed at least of actin, myosin-like proteins and profilin, surrounding sedimented statoliths. Experiments under microgravity demonstrated that the positioning of statoliths depends on the external gravitational force and on endocellular cytoskeleton-based forces exerted on their surfaces. Accepting the amyloplast-based statolith hypothesis, these results strongly suggest that gravisensing occurs in a close vicinity of statolith surfaces. Experiments with grass nodes revealed transient changes of the signalling molecule IP3 within few seconds after gravistimulation. The importance of mutants for dissecting the gravity-related signal transduction chains is highlighted.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Bähler M (1996) Myosins on the move to signal transduction. Curr Opin Cell Biol 8: 18–22
Baluška F and Hasenstein KH (1997) Root cytoskeleton: Its role in perception of and response to gravity. Planta 203: S69–S78
Baluška F, Volkmann D and Barlow PW (1996) Specialized zones of development in roots: View from the cellular level. Plant Physiol 112:3–4
Baluška F, Samaj J, Napier, R and Volkmann D (1999) Maize calreticulin localizes to plasmodesmata in root apex. Plant J 19: 481–487
Baluška F, Vitha S, Barlow PW and Volkmann D (1997) Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: A major developmental switch occurs in the postmitotic transition region. Eur J Cell Biol 72: 113–121
Baluška F, Kreibaum A, Vitha S, Parker JS, Barlow PW and Sievers A (1997) Central root cap cells are depleted of endoplasmic microtubules and actin filament bundles: Implications for their role as gravity-sensing statocytes. Protoplasma 196: 212–223
Barlow PW (1995) Gravity perception in plants: A multiplicity of systems derived by evolution. Plant Cell Environ 18: 951–952
Blancaflor EB, Fasano JM and Gilroy S (1998) Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol 116: 213–222
Bögre L, Ligterink W, Heberle-Bors E and Hirt H (1996) Mechanosensors in plants. Nature 383: 489–490
Braam J, Sistrunk ML, Polisensky DH, Wei X, Purugganan M, Antosiewicz DM, Campbell P and Johnson KA (1997) Plant responses to environmental stress: Regulation and functions of’the Arabidopsis TCH genes. Planta 203: S35–S41
Braun M (1996) Immunocytolocalization of myosin in rhizoids of Chara globularis Thuill. Protoplasma 191: 1–8
Buchen B, Braun M and Sievers A (1993) Statoliths pull on microfilaments. Experiments under microgravity. Protoplasma 172: 38–42
Burack WR and Shaw AS (2000) Signal transduction: Hanging on a scaffold. Curr Opin Cell Biol 12: 211–216
Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T and Masson PH (1998) The Arabidopsis thaliana AGRAVITROPIC1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci USA 95: 15112–15117
Chicurel ME, Chen CS and Ingber DE (1998) Cellular control lies in the balance of forces. Curr Opin Cell Biol 10: 232–239
Davies E, Shimps B, Brown K and Stankovi DB (1999) Gravity, stress, calcium and gene expression. J Grav Physiol 6: P21–P22
Ding B (1998) Intercellular protein trafficking through plasmodesmata. Plant Mol Biol 38: 279–310
Evans ML and Ishikawa H (1997) Cellular specificity of the gravitropic motor response in roots. Planta 203: S115–S122
Franklin-Tong VE, Drabak B, Allan AC, Watkins PAC and Trewavas AJ (1996) Growth of pollen tubes of Papaver rhoeas is regulated by a slow-moving calcium wave propagated by inositol 1,4,5-trisphosphate. Plant Cell 8: 1305–1321
Freilich S, Oron E, Kapp Y, Nevo-Caspi Y, Orgad S, Segal D and Chamovitz DA (1999) The COP9 signalosome is essential for development of Drosophila melanogaster. Curr Biol 9: 1187–1190
Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN and Tasaka M (1998) Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14: 425–430
Glogauer M, Arora P, Chou D, Janmey PA, Downey GP and McCulloch CAG (1998) The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J Biol Chem 273: 1689–1698
Godbolé R, Takahashi H and Hertel R (1999) The Lazy mutation in rice affects a step between statoliths and gravity-induced lateral auxin transport. Plant Biol 1: 379–381
Hargrave PA and McDowell JH (1993) Rhodopsin and phototransduction. Int Rev Cytol 137: 49–97
Heberle-Bors CJC and Hirt H (1994) MAP kinases: Universal multipurpose signaling tools. Plant Mol Biol 24: 407–416
Hejnowicz Z and Sievers A (1981) Regulation of the position of statoliths in Chara rhizoids. Protoplasma 108: 117–137
Hirt H (1997) Multiple roles of MA Pkinases in plant signal transduction. Trends Plant Sci 2: 11–15
Ingber DE (1997) Tensegrity: The architectural basis of cellular mechanotransduction. Annu Rev Physiol 59: 575–559
Ishikawa H and Evans ML (1992) Induction of curvature in maize roots by calcium or by thigmostimulation. Role of the postmitotic isodiametric growth zone. Plant Physiol 100:762–768
Ishikawa H and Evans ML (1993) The role of the distal elongation zone in the response of maize roots to auxin and gravity. Plant Physiol 102: 1203–1210
Janßen M, Hunte C, Schulz M and Schnabl H (1996) Tissue specification and intracellular distribution of actin isofoms in Vicia faba L. Protoplasma 191: 158–163
Jonak C, Ligterink W and Hirt H (1999) MAP kinases in plant signal transduction. Cell Mol Life Sci 55: 204–213
Juniper BE, Groves S, Landau-Schachar B and Audus LJ (1966) Root cap and the perception of gravity. Nature 209: 93–94
Kandasamy MK and Meagher RB (1999) Actin-organelle interaction: Association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskel 44: 110–118
Kernan M and Zuker Ch (1995) Genetic approaches to mechanosensory transduction. Curr Opin Neurobiol 5: 443–448
Klahre U and Chua N-H (1999) The Arabidopsis ACTIN-RELATED PROTEIN2 (AtARP2) promoter directs expression in xylem precursor cells and pollen. Plant Mol Biol 41: 65–73
Köhler RH and Hanson MR (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113: 81–89
Köhler RH, Cao J, Zipfle WR, Webb WW and Hanson MR (1997) Exchange of protein molecules through connections between higher plant plastids. Science 276: 2039–2042
Kost B, Spielhofer P and Chua N-H (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16: 393–401
Laurinavi☐ius R, Sto☐kus A, Buchen B and Sievers A (1996) Structure of cress root statocytes in microgravity (BION-10 mission). Adv Space Res 17: 91–94
Legué V, Blancaflor E, Wymer C, Perbal G, Fantin D and Gilroy S (1997) Cytoplasmic free Ca2+ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiol 114: 789–800
Lorenzi G and Perbal G (1990) Root growth and statocyte polarity in lentil seedling roots grown in microgravity or on a slowly rotating clinostat. Physiol Plant 78: 532–537
Luschnig C, Gaxiola RA, Grisafi P and Fink GR (1998) EIRl, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12: 2175–2187
Machesky LM and Gould KL (1999) The ARP2/3 complex: A multifunctional actin organizer. Curr Opin Cell Biol 11: 117–121
Marchant A, Kargul J, May ST, Müller P, Delbarre A, Perrot-Rechenmann C and Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18: 2066–2073
Meagher RB, McKinney EC and Kandasamy MK (1999) Isovariant dynamics expand and buffer the responses of complex systems: The diverse plant actin gene family. Plant Cell 11:995–1005
Menzel D (1994) Tansley Review No. 77. Cell differentiation and the cytoskeleton in Acetabularia. New Phytol 128: 369–393
Mermall V, Post PL and Mooseker MS (1998) Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279: 527–533
Miège C and Maréchal É (1999) 1,2-sn-Diacylglycerol in plant cells: Product, substrate and regulator. Plant Physiol Biochem 37: 795–808
Montell C (1999) Visual transduction in Drosophila. Annu Rev Cell Dev Biol 15: 231–268
Monshausen G and Sievers A (1998) Weak mechanical stimulation causes hyperpolarisation in root cells of Lepidium. Bot Acta 111: 303–306
Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E and Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 23: 6903–6911
Mundt KE, Porte J, Murray JM, Brikos C, Christensen PU, Caspari T, Hagan IM, Millar JBA, Simanis V, Hofmann K and Carr AM (1999) The COP9/signalosome complex is conserved in fission yeast and has a role in S phase. Curr Biol 9: 1427–1430
Munnik T, Irvine RF and Musgrave A (1998) Phospholipid signalling in plants. Biochim Biophys Acta 1389: 222–272
Palme K and G älweiler L (1999) PIN-pointing the molecular basis of auxin transport. Curr Opin Plant Biol 2: 375–381
Perbal G and Driss-Ecole D (1989) Polarity of statocytes in lentil seedling roots grown in space (Spacelab Dl Mission). Physiol Plant 75: 518–524
Perbal G and Driss-Ecole D (1994) Sensitivity to gravistimulus of lentil seedling roots grown in space during the IML1 Mission of Spacelab. Physiol Plant 90: 313–318
Perbal G, Driss-Ecole D, Rutin J and Sallé G (1987) Graviperception of lentil seedling roots grown in space (Spacelab Dl Mission). Physiol Plant 70: 119–126
Perbal G, Driss-Ecole D, Sallé G and Raffln F (1986) Perception of gravity in the lentil root. Naturwissenschaften 73: 444–446
Perbal G, Driss-Ecole D, Tewinkel M and Volkmann D (1997) Statocyte polarity and gravisensitivity in seedling roots grown in microgravity. Planta 203: S57–S62
Perera IY, Heilmann I and Boss WF (1999) Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. Proc Natl Acad Sci USA 96: 5838–5843
Pickard BG and Ding JP (1992) Gravity sensing by higher plants. In: Comparative Aspects of Mechanoreceptor Systems, Pharis RP and Reid DM (eds), Heidelberg: Springer-Verlag, pp 193–281
Radford JE and White RG (1998) Localization of a myosin-like protein to plasmodesmata. Plant J 14: 743–750
Reichelt S, Knight AE, Hodge TP, Baluška F, Samaj J, Volkmann D and Kendrick-Jones J (1999) Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19: 555–567
Rosen E, Chen R and Masson PH (1999) Root gravitropism: A complex response to a simple stimulus? Trends Plant Sci 4: 407–412
Sachs F (1997) Mechanical transduction by ion channels: How forces reach the channel. In: Cytoskeletal Regulation of Membrane Function, Froehner SC (ed), New York: Rockefeller University Press, pp 209–218
Sack F (1997) Plastids and gravitropic sensing. Planta 203: S63–S68
Sack FD, Suyemoto M and Leopold AC (1986) Amyloplast sedimentation and organelle saltation in living columella cells. Am J Bot 73: 1692–1698
Sato Y, Kadota A and Wada M (1999) Mechanically induced avoidance response of chloroplasts in fern protonemal cells. Plant Physiol 121: 37–44
Sedbrook JC, Chen R and Masson PH (1999) ARG1 (altered response to gravity) encodes a DnaJ-like protein that potentially interacts with the cytoskeleton. Proc Natl Acad Sci USA 96:1140–1145
Sievers A and Busch MB (1992) An inhibitor of the Ca2+-ATPase in the sarcoplasmic and endoplasmic reticula inhibits transduction of the gravity stimulus in cress roots. Planta 188: 619–622
Sievers A, Buchen B and Hodick D (1996) Gravity sensing in tip-growing cells. Trends Plant Sci 1:273–279
Sievers A, Buchen B, Volkmann D and Hejnowicz Z (1991) Role of the cytoskeleton in gravity perception. In: Lloyd CW (ed) The Cytoskeletal Basis of Plant Growth and Form. London: Academic Press, pp 169–182
Sievers A, Kruse S, Kuo-Huang LL and Wendt M (1989) Statoliths and microfilaments in plant cells. Planta 179: 275–278
Smith JD, Todd P and Staehelin LA (1997) Modulation of statolith mass and grouping in white clover (Trifolium repens) grown in 1-g, microgravity and on the clinostat. Plant J 12: 1361–1373
Soldati T, Schwarz EC and Geissler H (1999) Unconventional myosins at the crossroad of signal transduction and cytoskeleton remodeling. Protoplasma 209: 28–37
Spencer RH, Chang G and Rees DC (1999) Teeling the pressure’: Structural insights into a gated mechanosensitive channel. Curr Opin Struct Biol 9: 448–454
Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Annu Rev Plant Physiol Plant Mol Biol 51: 257–288
Staiger CJ, Gibbon BC, Kovar DR and Zonia LE (1997) Profilin and actin-depolymerizing factor: Modulators of actin organization in plants. Trends Plant Sci 2: 275–281
Staves MP, Wayne R and Leopold AC (1997a) Cytochalasin D does not inhibit gravitropism in roots. Am J Bot 84: 1530–1535
Staves MP, Wayne R and Leopold AC (1997b) The effect of the external medium on the gravitropic curvature of rice (Oryza sativa, Poaceae) roots. Am J Bot 84: 1522–1529
Tasaka M, Kato T and Fukaki H (1999) The endodermis and shoot gravitropism. Trends Plant Sci 4: 103–107
Thuleau P, Schroeder JI and Ranjeva R (1998) Recent advances in the regulation of plant calcium channels: Evidence for regulation by G-proteins, the cytoskeleton and second messengers. Curr Opin Plant Biol 1: 424–427
Tsugeki R and Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci USA 96: 12941–12946
Vitha S, Baluška F, Mews M and Volkmann D (1997) Immunofluorescence detection of F- actin on low melting wax sections from plant tissue. J Histochem Cytochem 45: 89–95
Vitha S, Baluška F, Braun M, Samaj J, Volkmann D and Barlow PW (2000) Comparison of cryofixation and aldehyde fixation for plant actin immunocytochemistry: Aldehydes do not destroy F-actin. Histochem J, in press
Volkmann D and Baluška F (1999) The actin cytoskeleton in plants: From transport networks to signaling networks. Microsc Res Tech 47: 135–154
Volkmann D and Sievers A (1979) Graviperception in multicellular organs. In: Encyclopedia of Plant Physiology, NS, vol. 7, Physiology of Movements. Haupt W and Feinleib ME (eds), Berlin: Springer-Verlag, pp 573–600
Volkmann D and Tewinkel M (1996) Gravisensing of cress roots: Investigations of threshold values under specific conditions of sensor physiology in microgravity. Plant Cell Environm 19: 1195–1202
Volkmann D and Tewinkel M (1998) Gravisensitivity of cress roots. Adv Space Res 21: 1209–1217
Volkmann D, Behrens HM and Sievers A (1986) Development and gravity sensing of cress roots under microgravity. Naturwissenschaften 73: 438–441
Volkmann D, Winn-Börner U and Waberzeck K (1993) Graviresponsiveness of cress seedlings and structural status of presumptive statocytes from the hypocotyl. J Plant Physiol 142: 710–716
Volkmann D, Baluška F, Lichtscheidl IK, Driss-Ecole D and Perbal G (1999) Statoliths motions in gravity-perceiving plant cells: Does actomyosin counteract gravity? FASEB J 13: S143–S147
Volkmann D, Buchen B, Hejnowicz Z, Tewinkel M and Sievers A (1991) Oriented movement of statoliths studied in a reduced gravitational field during parabolic flights of rockets. Planta 185:153–161
Wendt M, Kuo-Huang LL and Sievers A (1987) Gravitropic bending of cress roots without contact between amyloplasts and complexes of endoplasmic reticulum. Planta 172: 321–329
White RG and Sack FD (1990) Actin microfilaments in presumptive statocytes of root caps and coleoptiles. Am J Bot 77:17–26
White RG, Badelt K, Overall RL and Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180: 169–184
Williamson RE (1993) Organelle movements. Annu Rev Plant Physiol Plant Mol Biol 44: 181–202
Wu X, Jung G and Hammer JA III (2000) Functions of unconventional myosins. Curr Opin Cell Biol 12: 42–51
Wunsch C and Volkmann D (1993) Immunocytological detection of myosin in the root tip cells of Lepidium sativum. Eur J Cell Biol Suppl 61: p 46
Yang Z (1996) Signal transduction proteins in plants: An overview. In: Signal Transduction in Plant Growth and Development. Verma DPS (ed), Wien/New York: Springer-Verlag, pp 1–37
Zieschang HE and Sievers A (1991) Graviresponse and the localization of its initiating cells in Phleum pratense L. Planta 184: 468–477
Author information
Authors and Affiliations
Editor information
Rights and permissions
Copyright information
© 2000 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Volkmann, D., Baluška, F. (2000). Actin Cytoskeleton Related to Gravisensing in Higher Plants. In: Staiger, C.J., Baluška, F., Volkmann, D., Barlow, P.W. (eds) Actin: A Dynamic Framework for Multiple Plant Cell Functions. Developments in Plant and Soil Sciences, vol 89. Springer, Dordrecht. https://doi.org/10.1007/978-94-015-9460-8_31
Download citation
DOI: https://doi.org/10.1007/978-94-015-9460-8_31
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-5504-0
Online ISBN: 978-94-015-9460-8
eBook Packages: Springer Book Archive