Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지

Plant Cells on Earth and in Space

  • Published : 2000.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Two quite different types of plant cells are analysed with regard to transduction of the gravity stimulus: (i) Unicellular rhizoids and protonemata of characean green algae; these are tube-like, tip-growing cells which respond to the direction of gravity. (ii) Columella cells located in the center of the root cap of higher plants; these cells (statocytes) perceive gravity. The two cell types contain heavy particles or organelles (sataoliths) which sediment in the field of gravity, thereby inducing the graviresponse. Both cell types were studied under microgravity conditions ($10^{-4}$/ g) in sounding rockets or spacelabs. From video microscopy of living Chara cells and different experiments with both cell types it was concluded that the position of statoliths depends on the balance of two forces, i.e. the gravitational force and the counteracting force mediated by actin microfilaments. The actomyosin system may be the missing link between the gravity-dependent movement of statoliths and the gravity receptor(s); it may also function as an amplifier.

Keywords

References

  1. Allan E and Trewavas AJ (1985) Quantitative changes in calmodulin and NAD kinase during early cell development in the root apex of Pisum sativum. Planta 165: 493-501 https://doi.org/10.1007/BF00398094
  2. Baluska F and Hasenstein KH (1997) Root cytoskeleton: its role in perception of and response to gravity. Planta 203: S69- S78
  3. Baluska 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 https://doi.org/10.1007/BF01279569
  4. Barlow PW and Sargent JA (1978) The ultrastructure of the regenerating root cap of Zea mays L. Ann Bot 42: 791-799
  5. Barlow PW, Hawes CR, and Horne JC (1984) Structure of amyloplasts and endoplasmic reticulum in the root caps of Lepidium sativum and Zea mays observed after selective membrane staining and by high-voltage electron microscopy. Planta 160: 363-371 https://doi.org/10.1007/BF00393418
  6. Bartnik E and Sievers A (1988) In-vivo observation of a spherical aggregate of endoplasmic reticulum and of Golgi vesicles in the tip of fast-growing Chara rhizoids. Planta 176: 1-9 https://doi.org/10.1007/BF00392473
  7. Bartnik E, Hejnowicz Z, and Sievers A (1990) Shuttle-like movements of Golgi vesicles in the tip of growing Chara rhizoids. Protoplasma 159: 1-8 https://doi.org/10.1007/BF01326629
  8. Bibikova TN, Zhigilei A, and Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203: 495-505 https://doi.org/10.1007/s004250050219
  9. Biro RL, Hale CC II, Wiegand OF, and Roux SJ (1982) Effects of chlorpromazine on gravitropism in Avena coleoptiles. Ann Bot 50: 735-747
  10. Bjorkman T (1988) Perception of gravity by plants. Adv Bot Res 15: 1-41
  11. Bjorkman T and Leopold AC (1987) Effect of inhibitors of auxin transport and of calmodulin on a gravisensing-dependent current in maize roots. Plant Physiol 84: 847-850
  12. Blancaflor EB and Hasenstein K-H (1997) The organization of the actin cytoskeleton in vertical and graviresponding primary roots of maize. Plant Physiol 113: 1447-1455
  13. 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 https://doi.org/10.1104/pp.116.1.213
  14. Braun M (1996a) Immunolocalization of myosin in rhizoids of Chara globularis Thuill. Protoplasma 191: 1-8 https://doi.org/10.1007/BF01280820
  15. Braun M (1996b) Anomalous gravitropic response of Chara rhizoids during enhanced accelerations. Planta 199: 443-455 https://doi.org/10.1007/BF00195738
  16. Braun M (1997) Gravitropism in tip-growing cells. Planta 203: S11-S19
  17. Braun M and Sievers A (1993) Centrifugation causes adaptation of microfilaments; studies on the transport of statoliths in gravity sensing Chara rhizoids. Protoplasma 174: 50-61 https://doi.org/10.1007/BF01404042
  18. Braun M and Sievers A (1994) Role of the microtubule cytoskeleton in gravisensing Chara rhizoids. Eur J Cell Biol 63: 289-298
  19. Braun M and Wasteneys GO (1998a) Distribution and dynamics of the cytoskeleton in graviresponding protonemata and rhizoids of characean algae: exclusion of microtubules and a convergence of actin filaments in the apex suggest an actinmediated gravitropism. Planta 205: 39-50 https://doi.org/10.1007/s004250050294
  20. Braun M and Wasteneys GO (1998b) Reorganization of the actin and microtubule cytoskeleton throughout blue-Iightinduced differentiation of characean protonemata into multicellular thalli. Protoplasma 202: 38-53 https://doi.org/10.1007/BF01280873
  21. Braun M and Richter P (1999) Relocalization of the calcium gradient and a dihydropyridine receptor is involved in upward bending by bulging of Chara protonemata, but not in downward bending by bowing of Chara rhizoids. Planta 209: 414-423 https://doi.org/10.1007/s004250050744
  22. Braun M, Baluska F, von Witsch M, and Menzel D (1999a) Redistribution of actin, profilin and phosphatidylinositol-4,5bisphosphate (PIP2) in growing and maturing root hairs. Planta 209: 435-443 https://doi.org/10.1007/s004250050746
  23. Braun M, Buchen B, and Sievers A (1999b) Electron microscopical analysis of gravisensing Chara rhizoids developed under microgravity conditions. FASEB J 13: 113- 120
  24. Buchen B, Hejnowicz Z, Braun M, and Sievers A (1991) Cytoplasmic streaming in Chara rhizoids: Studies in a reduced gravitational field during parabolic flights of rockets. Protoplasma 165: 121-126 https://doi.org/10.1007/BF01322282
  25. Buchen B, Braun M, and Sievers A (1997) Statoliths, cytoskeletal elements and cytoplasmic streaming of Chara rhizoids under reduced gravity during TEXUS flights. In: Life Sciences Experiments Performed on Sounding Rockets (1985-1994). ESA Publications Division, Nordwijk, ESA-SP 1206, pp 71-75
  26. Buckhout TJ (1983) ATP-dependent $Ca^{2+}$-transport in endoplasmic reticulum isolated from the roots of Lepidium sativum L. Planta 159: 84-90 https://doi.org/10.1007/BF00998818
  27. Buder J (1961) Der Geotropismus der Characeenrhizoide. Ber Dtsch Bot Ges 74: 14-23
  28. Busch MB and Sievers A (1990) Hormone treatment of roots causes not only a reversible loss of starch but also of structural polarity in statocytes. Planta 181: 358-364 https://doi.org/10.1007/BF00195888
  29. Busch MB, Kortje KH, Rahmann H, and Sievers A (1993) Characteristic and differential calcium signals from cell structures of the root cap detected by energy-filtering electron microscopy. Eur J Cell Biol 60: 88-100
  30. Cai G, Moscatelli A, and Cresti M (1997) Cytoskeletal organization and pollen tube growth. Trends Plant Sci 2: 86-91 https://doi.org/10.1016/S1360-1385(96)10057-1
  31. Cai W, Braun M, and Sievers A (1997) Displacement of statoliths in Chara rhizoids during horizontal rotation on clinostats. Acta Bot Exp Sinica 30: 147-155
  32. Chandra S, Chabot JF, Morrison GH, and Leopold AC (1982) Localization of $Ca^{2+}$ in amyloplasts of root cap cells using ion microscopy. Science 216: 1221-1223 https://doi.org/10.1126/science.216.4551.1221
  33. Chen R, Rosen E, and Masson PH (1999) Gravitropism in higher plants. Plant Physiol 120: 343-350 https://doi.org/10.1104/pp.120.2.343
  34. Darwin C (1880) The Power of Movement in Plants. John Murray, London.
  35. Driss-Ecole D, Jeune B, Prouteau M, Julianus P, and Perbal G (2000) Lentil root statoliths reach a stable state in microgravity. Planta 211: 396-405 https://doi.org/10.1007/s004250000298
  36. Evans ML and Hasenstein K-H (1987) Stimulus-response coupling in the action of auxin and gravity on roots. In: Cosgrove DJ, Knievel DP (eds) , Physiology of Cell Expansion during Plant Growth. Bethesda, American Society of Plant Physiologists, pp 202-214
  37. Falke LC, Edwards KL, Pickard BG, and Misler S (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett 237: 141-144 https://doi.org/10.1016/0014-5793(88)80188-1
  38. 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 https://doi.org/10.1046/j.1365-313X.1998.00137.x
  39. Green PB, Erickson RO, and Richmond PA (1970) On the physical basis of cell morphogenesis. Ann NY Acad Sci 175: 712-731 https://doi.org/10.1111/j.1749-6632.1970.tb45187.x
  40. Grolig F (1990) Actin-based organelle movements in interphase Spirogyra. Protoplasma 155: 29-42 https://doi.org/10.1007/BF01322613
  41. Grolig F and Wagner G (1988) Light dependent chloroplast reorientation in Mougeotia and Mesotaenium: biased by pigment-regulated plasmalemma anchorage sites to actin filaments. Bot Acta 101: 2-6
  42. Haberlandt G (1900) Ober die Perzeption des geotropischen Reizes. Ber Dtsch Bot Ges 18: 261-272
  43. Hejnowicz Z and Sievers (1971) Mathematical model of geotropically bending Chara rhizoids. Z Pflanzenphysiol 66: 34-48
  44. Hejnowicz Z and Sievers A (1981) Regulation of the position of statoliths in Chara rhizoids. Protoplasma 108: 117-137 https://doi.org/10.1007/BF01276887
  45. Hejnowicz Z, Sondag C, Alt W, and Sievers A (1998) Temporal course of graviperception in intermittantly stimulated cress roots. Plant Cell Environ 21: 1293-1300 https://doi.org/10.1046/j.1365-3040.1998.00375.x
  46. Hensel W (1984) A role of microtubules in the polarity of statocytes from roots of Lepidium sativum L. Planta 162: 404-414 https://doi.org/10.1007/BF00393452
  47. Hensel W (1985) Cytochalasin B affects the structural polarity of statocytes from cress roots (Lepidium sativum L.). Protoplasma 129: 178-187 https://doi.org/10.1007/BF01279915
  48. Hensel W (1987) Cytodifferentiation of polar plant cells: formation and turnover of endoplasmic reticulum in root statocytes. Exp Cell Res 172: 377-384 https://doi.org/10.1016/0014-4827(87)90395-8
  49. Hensel W (1988) Demonstration by heavy-meromyosin of actin microfilaments in extracted cress (Lepidium sativum L) root statocytes. Planta 173: 142-143 https://doi.org/10.1007/BF00394498
  50. Hensel Wand Sievers A (1980) Effects of prolonged omnilateral gravistimulation on the ultrastructure and on the graviresponse of roots. Planta 150: 338-346 https://doi.org/10.1007/BF00384664
  51. Hodick D (1993) The protonema of Chara fragilis Desv.: regenerative formation, photomorphogenesis, and gravitropism. Bot Acta 106: 388-393
  52. Hodick D (1994) Negative gravitropism in Chara protonemata and rhizoids: a model integrating the opposite gravitropic responses of protonemata and rhizoids. Planta 195: 43-49
  53. Hodick D and Sievers A (1998) Hypergravity can reduce but not enhance the gravitropic response of Chara globularis protonemata. Protoplasma 204: 145-154 https://doi.org/10.1007/BF01280321
  54. Hodick D, Buchen B, and Sievers A (1998) Statolith positioning by microfilaments in Chara rhizoids and protonemata. Adv Space Res 21: 1183-1189 https://doi.org/10.1016/S0273-1177(97)00633-9
  55. Hwang J-U, Suh S, Yi H, Kim J, and Lee Y (1997) Actin filaments modulate both stomatal opening and inward K+channel activities in guard cells of Vicia faba L. Plant Physiol 115: 335-342
  56. Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104: 613-627
  57. Iversen T-H (1969) Elimination of geotropic responsiveness in roots of cress (Lepidium sativum) by removal of statolith starch. Physiol Plant 22: 1251-1262 https://doi.org/10.1111/j.1399-3054.1969.tb09115.x
  58. Iversen T -H and Larsen P (1973) Movement of amyloplasts in the statocytes of geotropically stimulated roots: the pre-inversion effect. Physiol Plant 28: 172-181 https://doi.org/10.1111/j.1399-3054.1973.tb01171.x
  59. Jackson SL and Heath IB (1990) Visualization of actin arrays in growing hyphae of the fungus Saprolegnia ferax. Protoplasma 154: 66-70 https://doi.org/10.1007/BF01349537
  60. Juniper BE and Clowes FAL (1965) Cytoplasmic organelles and cell growth in root caps. Nature 208: 864-865 https://doi.org/10.1038/208864a0
  61. Juniper BE, Groves S, Landau-Schachar B, and Audus LJ (1966) Root cap and the perception of gravity. Nature 209: 93-94 https://doi.org/10.1038/209093a0
  62. Kadota A, Yoshizaki N, and Wada M (1999) Cytoskeletal changes during resumption of tip growth in nongrowing protonemal cells of the fern Adiantum capillus-veneris L. Protoplasma 207: 195-202 https://doi.org/10.1007/BF01283000
  63. Kiss JZ, Wright JB, and Caspar T (1996) Gavitropism in the roots of intermediate-starch mutants of Arabidopsis. Physiol Plant 97: 237-244 https://doi.org/10.1034/j.1399-3054.1996.970205.x
  64. Kiss JZ, Katembe WJ, and Edelmann RE (1997) Gravitropism and development of wild-type and starch-deficient mutans of Arabidopsis during spaceflight. Physiol Plant 102: 493-502 https://doi.org/10.1034/j.1399-3054.1998.1020403.x
  65. Kuznetsov 0 and Hasenstein KH (1996) Intracellular magnetophoresis of amyloplasts and induction of root curvature. Planta 198: 87-94 https://doi.org/10.1007/BF00197590
  66. Kuznetsov O and Hasenstein KH (1997) Magnetophoretic induction of curvature in coleoptiles and hypocotyls. J Exp Bot 48: 1951-1957 https://doi.org/10.1093/jxb/48.11.1951
  67. Lee JS and Evans ML (1985) Polar transport of auxin across gravistimulated roots of maize and its enhancement by calcium. Plant Physiol 77: 824
  68. Lee JS, Mulkey T J, and Evans ML (1984) Inhibition of polar calcium movement and gravitropism in roots treated with auxin-transport inhibitors. Planta 160: 536-543 https://doi.org/10.1007/BF00411142
  69. Legue V, Blancaflor E, Wymer C, Perbal G, Fantin 0, and Gilroy S (1997) Cytoplasmic free $Ca^{2+}$ in Arabidopsis roots changes in response to touch but not gravity. Plant Physiol 114: 789-800
  70. Leitz G, Schnepf E, and Greulich KO (1995) Micromanipulation of statoliths in gravity-sensing Chara rhizoids by optical tweezers. Planta 197: 278-288 https://doi.org/10.1007/BF00202648
  71. Levina NN, Lew RR, and Heath IB (1994) Cytoskeletal regulation of ion channel distribution in the tip-growing organism Saprolegnia ferax. J Cell Sci 107: 127-134
  72. Lorenzi G and Perbal G (1990) Actin filaments responsible for the location of the nucleus in the lentil statocyte are sensitive to gravity. Biol Cell 68: 259-263 https://doi.org/10.1016/0248-4900(90)90317-V
  73. Lu Y-T and Feldman LJ (1997) Light-regulated root gravitropism: a role for, and characterization of, a calcium/calmodulindependent protein kinase homolog. Planta 203: S91-S97
  74. Meske V, Ruppert V, and Hartmann E (1996) Structural basis of the red light induced repolarization of tip-growth in caulonema cells of Ceratodon purpureus. Protoplasma 192: 189-198 https://doi.org/10.1007/BF01273891
  75. Miller DO, Lancelle SA, and Hepler PK (1996) Actin microfilaments do not form a dense meshwork in Lilium longiflorum pollen tube tips. Protoplasma 195: 123-132 https://doi.org/10.1007/BF01279191
  76. Miller DO, de Ruijter NCA, Bisseling T, and Emons AMC (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant Cell 17: 141-154
  77. Monshausen GB, Zieschang HE, and Sievers A (1996) Differential proton secretion in the apical elongation zone caused by gravistimulation is induced by a signal from the root cap. Plant Cell Environ 19: 1408-1414 https://doi.org/10.1111/j.1365-3040.1996.tb00019.x
  78. Nemec B (1900) Ober die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18: 241-245
  79. Olsen GM and Iversen T-H (1980) Ultrastructure and movements of cell structures in normal pea and an ageotropic mutant. Physiol Plant 50: 275-284 https://doi.org/10.1111/j.1399-3054.1980.tb04463.x
  80. Parke J, Miller C, and Anderton BH (1986) Higher plant myosin heavy-chain identified using a monoclonal antibody. Eur J Cell Biol 41: 9-13
  81. Perbal G and Rievire S (1976) Relation entre reaction geotropique et evolution due statenchyme dans la racine d'asperge. Physiol Plant 38: 39-47 https://doi.org/10.1111/j.1399-3054.1976.tb04855.x
  82. Perera IY, Heilmann I, and Boss WF (1999) Transient and sustained increases in inositol-1,2,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. Proc Natl Acad Sci USA 96: 5838-5843 https://doi.org/10.1073/pnas.96.10.5838
  83. Pickard BG and Ding JP (1992) Gravity sensing by higher plants. Adv Comp Environ Physiol 10: 81-110
  84. Quatrano RS, Brian L, Aldridge J, and Schulz T (1991) Polar axis fixation in Fucus zygotes: components of the cytoskeleton and extracellular matrix. Development 1: 11-16
  85. Sanders O, Brownlee C, and Harper JF (1999) Communicating with calcium. Plant Cell 11: 691-706 https://doi.org/10.2307/3870893
  86. Sack FD (1991) Plant gravity sensing. Int Rev Cytol 127: 193-252
  87. Sack FD (1997) Plastids and gravitropic sensing. Planta 203: S63-S68
  88. Sack FD, Priestley DA, and Leopold AC (1983) Surface charge on isolated maize-coleoptile amyloplasts. Planta 157: 511-517 https://doi.org/10.1007/BF00396881
  89. Schroeder JI and Hedrich R (1989) Involvement of ion channels and active transport in osmoregulation and signaling of higher plant cells. Trends Biol Sci 14:187-192 https://doi.org/10.1016/0968-0004(89)90272-7
  90. Schroter K, Lauchli A, and Sievers A (1975) Mikroanalytische Identifikation von Bariumsulfat-Kristallen in den Statolithen von Chara fragilis Desv. Planta 122: 213-225 https://doi.org/10.1007/BF00385269
  91. Sedbrook J, Chen R, and Masson P (1999) ARG1 (Altered Response to Gravity) encodes for a novel DnaJ-like protein which potentially interacts with the cytoskeleton. Proc Natl Acad Sci USA 96: 1140-1145 https://doi.org/10.1073/pnas.96.3.1140
  92. Shaw SL and Quatrano RS (1996) Polar localization of a dihydropyridine receptor on living Fucus zygotes. J Cell Sci 109: 335-342
  93. Sievers A (1971) Gravity receptors in lower plants. In: Gordon SA, Cohen MJ (eds) , Gravity and the Organism. University of Chicago Press, Chicago, pp 51-63
  94. Sievers A (1999) Gravitational biology in Bonn. Am Soc Gravit Space Biol Newslett 15(3): 15-22
  95. Sievers A and Schroter K (1971) Versuch einer Kausalanalyse der geotropischen Reaktionskette im Chara-Rhizoid. Planta 96: 339-353 https://doi.org/10.1007/BF00386948
  96. Sievers A and Volkmann D (1972) Verursacht differentieller Druck der Amyloplasten auf ein komplexes Endomembransystem die Geoperzeption in Wurzeln? Planta 102: 160-172 https://doi.org/10.1007/BF00384870
  97. Sievers A and Volkmann D (1977) Ultrastructure of gravityperceiving cells in plant roots. Proc R Soc Land B 199: 525-536
  98. Sievers A and Schnepf E (1981) Morphogenesis and polarity of tubular cells with tip growth. In: Kiermayer (ed), Cytomorphogenesis in Plants, Cell Biology Monographs, Vol 8, Springer, New York, pp 265-299
  99. Sievers A and Schmitz M (1982) Rontgen-Mikroanalyse von Barium, Schwefel und Strontium in Statolithen-Kompartimenten von Chara-Rhizoiden. Ber Otsch Bot Ges 95: 353-360
  100. Sievers A and Heyder-Caspers L (1983) The effect of centrifugal acceleration on the polarity of statocytes and on the graviperception of cress roots. Planta 157: 64-70 https://doi.org/10.1007/BF00394541
  101. Sievers A and Busch MB (1992) An inhibitor of the $Ca^{2+}$-ATPases in the sarcoplasmic and endoplasmic reticula inhibits transduction of the gravity stimulus in cress roots. Planta 188: 619-622 https://doi.org/10.1007/BF00197057
  102. Sievers A and Braun M (1996) Root cap: structure and function. In: Waisel Y, Eshel A, and Kafkafi U (eds), Plant Roots-the Hidden Half. 2nd Ed. Marcel Dekker, New York, pp 31-49
  103. Sievers A, Heinemann B, and Rodriguez-Garcia MI (1979) Nachweis des subapikalen differentiellen Flankenwachstums im Chara-Rhizoid wahrend der Graviresponse. Z Pflanzenphysiol 91: 435-442
  104. Sievers A, Kruse S, Kuo-Huang L-L, and Wendt M (1989) Statoliths and microfilaments in plant cells. Planta 179: 275-278 https://doi.org/10.1007/BF00393699
  105. Sievers A, Kramer-Fischer M, Braun M, and Buchen B (1991a) The polar organization of the growing Chara rhizoid and the transport of statoliths are actin-dependent. Bot Acta 104: 103-109
  106. Sievers A, Buchen B, Volkmann D, and Hejnowicz Z (1991 b) Role of the cytoskeleton in gravity perception. In: Lloyd CW (eds), The Cytoskeletal Basis for Plant Growth and Form, Academic Press, London, pp 169-182
  107. Sievers A, Buchen B, and Hodick D (1996) Gravity sensing in tip-growing cells. Trends Plant Sci 1: 273-279 https://doi.org/10.1016/1360-1385(96)10028-5
  108. Staves MP, Wayne R, and Leopold AC (1997) Cytochalasin D does not inhibit gravitropism in roots. Am J Bot 84: 1530-1535 https://doi.org/10.2307/2446614
  109. Stephenson JLM and Hawes CR (1986) Stereology and stereometry of endoplasmic reticulum during differentiation in the maize root cap. Protoplasma 131: 32-46 https://doi.org/10.1007/BF01281685
  110. Stinemetz CL, Kuzmanoff KM, Evans ML, and Jarrett HW (1987) Correlation between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol 84: 1337-1342
  111. Taylor L T and Hepler PK (1997) Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 48: 461-491 https://doi.org/10.1146/annurev.arplant.48.1.461
  112. Tewinkel M, Kruse S, Quader H, Volkmann D, and Sievers A (1989) Visualization of actin filament pattern in plant cells without prefixation. A comparison of differently modified phallotoxins. Protoplasma 149: 178-182 https://doi.org/10.1007/BF01322990
  113. Volkmann D (1974) Amyloplasten und Endomembranen: das Geoperzeptionssystem er Primarwurzel. Protoplasma 79: 159-183 https://doi.org/10.1007/BF02055787
  114. Volkmann D and Sievers A (1979) Graviperception in multicellular organs. In: Haupt W, Feinleib ME (eds), Encyclopedia of Plant Physiology, New Series, Vol 7, Physiology of Movements, Springer-Verlag, Berlin, pp 573-600
  115. Volkmann D and Baluska F (1999) Actin cytoskeleton in plants: from transport networks to signalling networks. Microsc Res Tech 47: 135-154 https://doi.org/10.1002/(SICI)1097-0029(19991015)47:2%3C135::AID-JEMT6%3E3.0.CO;2-1
  116. Volkmann D, Behrens HM, and Sievers A (1986) Development and gravity sensing of cress roots under microgravity. Naturwissenschaften 73: 438-441 https://doi.org/10.1007/BF00367291
  117. 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 https://doi.org/10.1007/BF00194056
  118. Walker LM and Sack FD (1995) Microfilament distribution in protonemata of the moss Ceratodon. Protoplasma 189: 229-237 https://doi.org/10.1007/BF01280177
  119. Wang-Cahill F and Kiss JZ (1995) The statolith compartment in Chara rhizoids contains carbohydrate and protein. Am J Bot 83: 220-229 https://doi.org/10.2307/2445529
  120. Weise S and Kiss JZ (1999) Gravitropism of inflorescence stems in starch-deficient mutants of Arabidopsis. Int J Plant Sci 160: 521-527 https://doi.org/10.1086/314142
  121. Wendt M and Sievers A (1986) Restitution of polarity in statocytes from centrifuged roots. Plant Cell Environ 9: 17-23 https://doi.org/10.1111/j.1365-3040.1986.tb01718.x
  122. Wendt M and Sievers A (1989) The polarity of statocytes and the gravisensitivity of roots are dependent on the concentration of calcium in statocytes. Plant Cell Physiol 30: 929-932
  123. White RG and Sack FD (1990) Actin microfilaments in presumptive statocytes of root caps and coleoptiles. Am J Bot 77: 17-26 https://doi.org/10.2307/2444788
  124. Wilkins MB (1984) Gravitropism. In: Wilkins MB (ed), Advanced Plant Physiology. Pitman, London, pp 163-185
  125. Zieschang HE, Koehler K, and Sievers A (1993) Changing proton concentrations at the surfaces of gravistimulated Phleum roots. Planta 190: 546-554 https://doi.org/10.1007/BF00224794
  126. Planta v.190 Changing proton concentrations at the surfaces of gravistimulated phleum roots Zieschang HE;Koehler K;Sievers A