Abstract
Due to their sessile life style, an important ability of plants is to adjust their growth towards or away from environmental stimuli. Plant responses that involve directed movements are called tropisms. Among the best-known tropisms are phototropism, the response to light, and gravitropism, the response to gravity. Gravity is one of the major factors that govern root growth in plants. Since the emergence of land plants, gravitropism allowed plants to adjust root growth to maximize access to water and nutrients, and shoots to explore and exploit space on and above the surface of the Earth. In this chapter we discuss current knowledge and point out open questions like the nature of the gravireceptor, the role of secondary messengers, hormones and the cytoskeleton. We review the history of plant gravitropism research, from early experiments performed by naturalists like Charles Darwin to the utilization of clinostats, centrifuges and experimentation in the almost stimulus-free environment of microgravity provided by drop towers, parabolic flights of aircrafts and rockets, satellites and low earth orbit space stations, which are increasingly contributing to our understanding of plant gravity sensing and orientation.
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References
Andreeva Z, Barton D, Armour WJ et al (2010) Inhibition of phospholipase C disrupts cytoskeletal organization and gravitropic growth in Arabidopsis roots. Planta 232:1263–1279. https://doi.org/10.1007/s00425-010-1256-0
Audus L (1979) Plant geosensors. J Exp Bot 8:235–249
Baldwin KL, Strohm AK, Masson PH (2013) Gravity sensing and signal transduction in vascular plant primary roots. Am J Bot 100:126–142. https://doi.org/10.3732/ajb.1200318
Baluška F, Kreibaum A, Vitha S et al (1997) Central root cap cells are depleted of endoplasmic microtubules and actin microfilament bundles: implications for their role as gravity-sensing statocytes. Protoplasma 196:212–223. https://doi.org/10.1007/BF01279569
Band LR, Wells DM, Larrieu A et al (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc Natl Acad Sci 109:4668–4673. https://doi.org/10.1073/pnas.1201498109
Behrens HM, Gradmann D, Sievers A (1985) Membrane-potential responses following gravistimulation in roots of Lepidium sativum L. Planta 163:463–472. https://doi.org/10.1007/BF00392703
Bennett MJ, Marchant A, Green HG et al (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950. https://doi.org/10.1126/science.273.5277.948
Berridge MJ (2009) Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta, Mol Cell Res 1793:933–940
Blancaflor EB (2002) The cytoskeleton and gravitropism in higher plants. J Plant Growth Regul 21:120–136. https://doi.org/10.1007/s003440010041
Blancaflor EB, Fasano JM, 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
Boonsirichai K, Sedbrook JC, Chen R et al (2003) ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 15:2612–2625
Braun M, Limbach C (2006) Rhizoids and protonemata of characean algae: model cells for research on polarized growth and plant gravity sensing. Protoplasma 229:133–142. https://doi.org/10.1007/s00709-006-0208-9
Busch MB, 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
Cho M, Cho HT (2013) The function of ABCB transporters in auxin transport. Plant Signal Behav 8:2–4. https://doi.org/10.4161/psb.22990
Cholodny N (1929) Einige Bemerkungen zum Problem der Tropismen. Planta 7:461–481. https://doi.org/10.1007/BF01912159
Collings DA, Zsuppan G, Allen NS, Blancaflor EB (2001) Demonstration of prominent actin filaments in the root columella. Planta 212:392–403. https://doi.org/10.1007/s004250000406
Darwin CR (1880) The power of movement in plants. John Murray, London
Digby J, Firn RD (1995) The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant Cell Environ 18:1434–1440. https://doi.org/10.1111/j.1365-3040.1995.tb00205.x
Fasano JM (2001) Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 13:907–922. https://doi.org/10.1105/tpc.13.4.907
Ferl RJ, Paul A-L (2016) The effect of spaceflight on the gravity-sensing auxin gradient of roots: GFP reporter gene microscopy on orbit. NPJ Microgravity 2:15023. https://doi.org/10.1038/npjmgrav.2015.23
Frank AB (1868) Über die durch die Schwerkraft verursachten Bewegungen von Pflanzentheilen. Beiträge zur Pflanzenphysiologie 8:1–99
Friml J (2003) Auxin transport – shaping the plant. Curr Opin Plant Biol 6:7–12. https://doi.org/10.1016/S1369-5266(02)00003-1
Friml J, Palme K (2002) Polar auxin transport – old questions and new concepts? Plant Mol Biol 49:273–284. https://doi.org/10.1007/978-94-010-0377-3_2
Friml J, Wiśniewska J, Benková E et al (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809. https://doi.org/10.1038/415806a
Fukaki H, Wysocka-Diller J, Kato T et al (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
Gälweiler L, Guan C, Müller A et al (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230. https://doi.org/10.1126/science.282.5397.2226
Gutjahr C, Riemann M, Müller A et al (2005) Cholodny-went revisited: a role for jasmonate in gravitropism of rice coleoptiles. Planta 222:575–585. https://doi.org/10.1007/s00425-005-0001-6
Guyomarc’h S, Leran S, Auzon-Cape M et al (2012) Early development and gravitropic response of lateral roots in Arabidopsis thaliana. Philos Trans R Soc B Biol Sci 367:1509–1516. https://doi.org/10.1098/rstb.2011.0231
Haberlandt G (1900) Über die Perzeption des geotropischen Reizes. Ber Dtsch Bot Ges 18:261–272
Hamilton ES, Schlegel AM, Haswell ES (2015) United in diversity: mechanosensitive ion channels in plants. Annu Rev Plant Biol 66:113–137. https://doi.org/10.1146/annurev-arplant-043014-114700
Harrison BR, Masson PH (2008) ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 53:380–392. https://doi.org/10.1111/j.1365-313X.2007.03351.x
Heinowicz Z, Sondag C, Alt W, Sievers A (1998) Temporal course of graviperception in intermittently stimulated cress roots. Plant Cell Environ 21:1293–1300. https://doi.org/10.1046/j.1365-3040.1998.00375.x
Hensel W, Sievers A (1980) Effects of prolonged omnilateral gravistimulation on the ultrastructure of statocytes and on the graviresponse of roots. Planta 150:338–346. https://doi.org/10.1007/BF00384664
Hoson T, Kamisaka S, Masuda Y et al (1997) Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta 203:S187–S197. https://doi.org/10.1007/PL00008108
Hou G, Mohamalawari DR, Blancaflor EB (2003) Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol 131:1360–1373. https://doi.org/10.1104/pp.014423
Hou G, Kramer VL, Wang YS et al (2004) The promotion of gravitropism in Arabidopsis roots upon actin disruption is coupled with the extended alkalinization of the columella cytoplasm and a persistent lateral auxin gradient. Plant J 39:113–125. https://doi.org/10.1111/j.1365-313X.2004.02114.x
Ingber DE, Wang N, Stamenović D (2014) Tensegrity, cellular biophysics, and the mechanics of living systems. Reports Prog Phys 77. https://doi.org/10.1088/0034-4885/77/4/046603
Johannes E, Collings DA, Rink JC, Allen NS (2001) Cytoplasmic pH dynamics in maize pulvinal cells induced by gravity vector changes. Plant Physiol 127:119–130. https://doi.org/10.1104/pp.127.1.119
Juniper BE, Groves S, Landau-Schachar B, Audus LJ (1966) Root cap and the perception of gravity [35]. Nature 209:93–94
Kiss JZ, Sack FD (1989) Reduced gravitropic sensitivity in roots of a starch-deficient mutant of Nicotiana sylvestris. Planta 180:123–130. https://doi.org/10.1007/BF02411418
Kiss JZ, Hertel R, Sack FD (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177:198–206. https://doi.org/10.1007/BF00392808
Knight TA (1806) V. On the direction of the radicle and germen during the vegetation of seeds. By Thomas Andrew knight, Esq. F. R. S. In a letter to the right Hon. Sir Joseph banks, K. B. P. R. S. Philos Trans R Soc London 96:99–108. https://doi.org/10.1098/rstl.1806.0006
Konings H (1968) The significance of the root cap for geotropism. Acta Bot Neerl 17:203–211. https://doi.org/10.1111/j.1438-8677.1968.tb00074.x
Kuznetsov OA, Hasenstein KH (1996) Intracellular magnetophoresis of amyloplasts and induction of root curvature. Planta 198:87–94. https://doi.org/10.1007/BF00197590
Kuznetsov OA, Hasenstein KH (1997) Magnetophoretic induction of curvature in coleoptiles and hypocotyls. J Exp Bot 48:1951–1957. https://doi.org/10.1093/jexbot/48.316.1951
Kuznetsov OA, Schwuchow J, Sack FD, Hasenstein KH (1999) Curvature induced by amyloplast magnetophoresis in protonemata of the moss Ceratodon purpureus. Plant Physiol 119(2):645–650
Laurinavicius R, Stockus A, Buchen B, Sievers A (1996) Structure of cress root statocytes in microgravity (Bion-10 mission). Adv Space Res 17:91–94
Lee JS, Evans ML (1985) Polar transport of auxin across gravistimulated roots of maize and its enhancement by calcium. Plant Physiol 77:824–827
Lee JS, Mulkey TJ, Evans ML (1983a) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73:874–876. https://doi.org/10.1104/pp.73.4.874
Lee JS, Mulkey TJ, Evans ML (1983b) Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science 220:1375–1376
Leitz G, Kang B-H, Schoenwaelder MEA, Staehelin LA (2009) Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell Online 21:843–860. https://doi.org/10.1105/tpc.108.065052
Mei Y, Jia WJ, Chu YJ, Xue HW (2012) Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins. Cell Res 22:581–597. https://doi.org/10.1038/cr.2011.150
Meldolesi J, Pozzan T (1998) The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem Sci 23:10–14
Michniewicz M, Zago MK, Abas L et al (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056. https://doi.org/10.1016/j.cell.2007.07.033
Monshausen GB, Miller ND, Murphy AS, Gilroy S (2011) Dynamics of auxin-dependent Ca2+and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J 65:309–318. https://doi.org/10.1111/j.1365-313X.2010.04423.x
Mullen JL, Hangarter RP (2003) Genetic analysis of the gravitropic set-point angle in lateral roots of Arabidopsis. Adv Space Res 31:2229–2236
Neef M, Denn T, Ecke M, Hampp R (2016) Intracellular calcium decreases upon hyper gravity-treatment of Arabidopsis thaliana cell cultures. Microgravity Sci Technol 28:331–336. https://doi.org/10.1007/s12217-015-9457-6
Nemec B (1900) Ueber die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18:241–245
Palmieri M, Kiss JZ (2007) The role of plastids in gravitropism. In: The structure and function of plastids. Springer, Dordrecht, pp 507–525
Perbal G, Driss-Ecole D (1994) Sensitivity to gravistimulus of lentil seedling roots grown in space during the IML 1 mission of spacelab. Physiol Plant 90:313–318. https://doi.org/10.1111/j.1399-3054.1994.tb00393.x
Perbal G, Lefranc A, Jeune B, Driss-Ecole D (2004) Mechanotransduction in root gravity sensing cells. Physiol Plant 120:303–311. https://doi.org/10.1111/j.0031-9317.2004.0233.x
Perera IY (2006) A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol 140:746–760. https://doi.org/10.1104/pp.105.075119
Perera IY, Heilmann I, 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 U S A 96:5838–5843. https://doi.org/10.1073/pnas.96.10.5838
Pfeffer W (1904) Pflanzenphysiologie: ein Handbuch der Lehre vom Stoffwechsels und Kraftwechsels in der Pflanze. W. Engelmann, Leipzig
Robert HS, Offringa R (2008) Regulation of auxin transport polarity by AGC kinases. Curr Opin Plant Biol 11:495–502
Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118:101–121. https://doi.org/10.1007/BF00388387
Sachs J (1882) Über Ausschlieβung der geotropischen und heliotropischen Krümmungen während des Wachsens. Wilhelm Engelmann, Leipzig
Schüler O, Hemmersbach R, Böhmer M (2015) A bird’s-eye view of molecular changes in plant gravitropism using omics techniques. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.01176
Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous gydromedusan, Aequorea. J Cell Comp Physiol 59:223–239. https://doi.org/10.1002/jcp.1030590302
Sievers A, Volkmann D (1971) Verursacht differentieller Druck der Amyloplasten auf ein komplexes Endomembransystem die Geoperzeption in Wurzeln? Planta 102:160–172. https://doi.org/10.1007/BF00384870
Sievers A, Volkmann D (1977) Ultrastructure of gravity-perceiving cells in plant roots. Proc R Soc Lond B 199:525–536. https://doi.org/10.1098/rspb.1977.0160
Sievers A, Kruse S, Kuo-Huang LL, Wendt M (1989) Statoliths and microfilaments in plant cells. Planta 179:275–278. https://doi.org/10.1007/BF00393699
Spitzer C, Reyes FC, Buono R et al (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell Online 21:749–766. https://doi.org/10.1105/tpc.108.064865
Stinemetz CL, Kuzmanoff KM, Evans ML, Jarrett HW (1987) Correlation between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol 84:1337–1342. https://doi.org/10.1104/pp.84.4.1337
Toyota M, Gilroy S (2013) Gravitropism and mechanical signaling in plants. Am J Bot 100:111–125. https://doi.org/10.3732/ajb.1200408
Toyota M, Furuichi T, Tatsumi H, Sokabe M (2007) Hypergravity stimulation induces changes in intracellular calcium concentration in Arabidopsis seedlings. Adv Space Res 39:1190–1197. https://doi.org/10.1016/j.asr.2006.12.012
Tsugeki R, Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. Proc Natl Acad Sci U S A 96:12941–12946. https://doi.org/10.1073/pnas.96.22.12941
Vanneste S, Friml J (2013) Calcium: the missing link in auxin action. Plants 2:650–675
Vitha S, Yang M, Sack FD, Kiss JZ (2007) Gravitropism in the starch excess mutant of Arabidopsis thaliana. Am J Bot 94:590–598. https://doi.org/10.3732/ajb.94.4.590
Volkmann D, Tewinkel M (1996) Gravisensitivity of cress roots: investigations of threshold values under specific conditions of sensor physiology in microgravity. Plant Cell Environ 19:1195–1202. https://doi.org/10.1111/j.1365-3040.1996.tb00435.x
Volkmann D, Behrens HM, Sievers A (1986) Development and gravity sensing of cress roots under microgravity. Naturwissenschaften 73:438–441. https://doi.org/10.1007/BF00367291
Wayne R, Staves MP (1996) A down to earth model of gravisensing or Newton’s law of gravitation from the apple’s perspective. Physiol Plant 98:917–921. https://doi.org/10.1111/j.1399-3054.1996.tb06703.x
Wendt M, Sievers A (1986) Restitution of polarity in statocytes from centrifuged roots. Plant Cell Environ 9:17–23. https://doi.org/10.1111/1365-3040.ep11612684
Went FW, Thimann KV (1937) Phytohormones. The Macmillan Company, New York
Yoder TL (2001) Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiol 125:1045–1060. https://doi.org/10.1104/pp.125.2.1045
Zheng HQ, Staehelin LA (2001) Nodal endoplasmic reticulum, a specialized form of endoplasmic reticulum found in gravity-sensing root tip columella cells. Plant Physiol 125:252–265. https://doi.org/10.1104/pp.125.1.252
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Gadalla, D.S., Braun, M., Böhmer, M. (2018). Gravitropism in Higher Plants: Cellular Aspects. In: Gravitational Biology I. SpringerBriefs in Space Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-93894-3_6
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