Statoliths displacement in root statocytes in real and simulated microgravity

Authors

  • E. L. KORDYUM M. G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine
  • V. O. BRYKOV M. G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine

DOI:

https://doi.org/10.15407/knit2021.02.078

Keywords:

amyloplasts, fast clinorotation, gravity perception, microgravity, plant root, simulated microgravity, slow clinorotation

Abstract

Despite the long-term employment of different types of clinostats in space and gravitational biology, the discussions about their reliability to mimic microgravity in space flight are still ongoing. In this paper, we present some data about the behaviour of amyloplasts-statoliths in root cap statocytes of higher plant seedlings growing during 3–5 days under slow and fast 2-D clinorotation and real microgravity in orbital flight. In addition, data on the displacement of amyloplasts in the statocytes of seedlings subjected to vibration and acceleration in the launch mode of a spacecraft are also given. A comparative analysis showed sharp differences in statolith responses to slow and fast clinorotation with a speed of 50 rpm. In the first case, the behaviour of amyloplasts was more or less similar to that in space flight, they did not touch the plasmalemma. In the second case, the contacts of statoliths with the plasmalemma or its invaginations (plasmalomasomes), like those under the action of vibration and acceleration, were clearly observed. Thus, slow 2-D clinostat is more suitable to study gravity sensing by root cap amyloplasts-statoliths and their responses to microgravity in the ground-based experiments.

References

Dedolph R. R., Dipert M. H. (1971). The physical basis of gravity stimulus nullification by clinostat rotation. Plant Physiol., 47, 756—764.

https://doi.org/10.1104/pp.47.6.756

Brown A. H., Chapman D. K., Johnsson A., Heathcote D. (1995). Gravitropic responses of the Avena coleoptile in space and on clinostats. I. Gravitropic response thresholds. Physiol. plant., 95, 27—33.

https://doi.org/10.1111/j.1399-3054.1995.tb00803.x

Kraft T., van Loon J., Kiss J. Z. (2000). Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta, 211, 415—422.

https://doi.org/10.1007/s004250000302

van Loon J. (2007). Some history and use of the random positioning machine, RPM, in gravity related research. Adv. Space Res., 39, 1161—1165.

https://doi.org/10.1016/j.asr.2007.02.016

Beysens D., Carotenuto L., van Loon J., Zell M. (2011). Laboratory Science with Space Data. Berlin: Springer.

https://doi.org/10.1007/978-3-642-21144-7

Herranz R., Anken R. Boonstra J., Braun J. M., Christianen P. C. M., de Geest M., Hauslage J., Hilbig R., Hill R. J. A., Lebert M., Medina F. J., Vagt N., Ullrich O., van Loon J. J. W. A., Hemmersbach R. (2013). Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology, 13, 1—17.

https://doi.org/10.1089/ast.2012.0876

Kiss J. Z., Wolverton C., Wyatt S. E., Hasenstein K. H., van Loon J. J. W. A. (2019). Comparison of microgravity analogs to spaceflight in studies of plant growth and development. Front. Plant Sci.

https://doi.org/10.3389/fpls.2019.01577

Krause L. Braun M., Hauslage J., Hemmersbach R. (2018). Analysis of statolith displacement in Chara rhizoids for validating the microgravity-simulation quality of clinorotation modes. Microgravity Sci. and Technol., 30, 229—236.

https://doi.org/10.1007/s12217-017-9580-7

Cogoli M. (1992). The fast rotating clinostat: a history of its use in gravitational biology and a comparison of ground-based and flight experiment results. ASGSB Bull., 5, 59—67.

Hilaire E., Paulsen A. Q., Brown C. S., Guikema J. A. (1995). Effects of clinorotation and micrograyity on sweet clover columella cells treated with cytochalasin D. Physiol. plant., 95, 267—273.

https://doi.org/10.1111/j.1399-3054.1995.tb00837.x

Hoson T., Kamisaka S., Masuda Y., Yamashita M., Buchen B. (1997). Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta, 203, suppl., 187—197.

https://doi.org/10.1007/PL00008108

Hoson T., Soga K., Mori R., Saiki M., Wakabayashi K., Kamisaka S. (1999). Plant growth and morphogenesis under different gravity conditions: relevance to plant life in space. J. Plant Res., 112, 477—486.

https://doi.org/10.1007/PL00013903

John S. P., Hasenstein K. H. (2011). Effects of mechanostimulation on gravitropism and signal persistence in flax roots. Plant Signaling and Behaviour, 6, 1365—1370.

https://doi.org/10.4161/psb.6.9.16601

van Loon J. J. W. A. (2016). Centrifuges for microgravity simulation. The reduced gravity paradigm. Frontiers in Astron. and Space Sci.

https://doi.org/10.3389/fspas.2016.00021

Wang H., Li X., Krause L., et al. (2016). Erratum to: 2-D clinostat for simulated microgravity experiments with Arabidopsis seedlings. Microgravity Sci. and Technol., 28, 307.

https://doi.org/10.1007/s12217-016-9503-z

Chantseva V., Bilova T., Smolikova G., Frolov A., Medvedev S. (2019). 3-D clinirotation unduces specific alterations in metabolite profiles of germinating Brassica napus L. seeds. Biol. Communications, 54, 55—68.

https://doi.org/10.21638/spbu03.2019.107

Volkman D., Sievers A. (1979). Graviperception in multicellular organs. Encyclopedia of Plant Physiology. New Series. 7, 573—600.

Kiss J. (2000). Mechanisms of the early stages of plant gravitropism. Critical Reviews in Plant Sci., 19, 551—573.

https://doi.org/10.1080/07352680091139295

Perbal G. (2009). From ROOTS to GRAVI-1: twenty five years for understanding how plants sense gravity. Microgravity Sci. and Technol., 21, 3—10.

https://doi.org/10.1007/s12217-008-9064-x

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

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

Lorenzi G., 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

Sievers A., Buchen B., Volkmann D., Hejnowicz Z. (1991). Role of the cytoskeleton in gravity perception. The Cytoskeletal Basis of Plant Growth and Form. Lloyd C. W. (ed.). London: Acad. Press, 169—182.

Volkman D., Behrens H., Sievers A. (1986). Development and gravity sensing of cress roots under microgravity. Naturwissenschaften, 73, 438—441.

https://doi.org/10.1007/BF00367291

Klymchuk D. O., Kordyum E. L., Chapman D. K., Brown C. S., Vorobyova T. V. (2003). Changes in vacuolization in the root apex cells of soybean seedlings in microgravity. Adv. Space Res., 31, 2283—2288.

https://doi.org/10.1016/S0273-1177(03)00256-4

Driss-Ecole D., Legue V., Carnero-Diaza E., Perbal G. (2008). Gravisensitivity and automorphogenesis of lentil seedling roots grown on board the International Space Station. Physiol. plant., 134, 191—201.

https://doi.org/10.1111/j.1399-3054.2008.01121.x

Hensel W., Sievers A. (1980). Effects of prolonged omnilateral gravistimulation on the ultrastructure of statosytes and on the graviresponse of roots. Planta, 150, 338—346.

https://doi.org/10.1007/BF00384664

Sytnik K. M., Kordyum E. L., Nedukha E. M., Sidorenko P. G., Fomicheva V. M. (1984). Plant Cell under Changes of Geophysical Factors. Kyiv: Naukova Dumka.

Moore R. (1990). Comparative effectiveness of a clinostat and a slow-turning lateral vessel at mimicking the ultrastructural effects of microgravity in plant cells. Ann. Bot., 66, 541—549.

https://doi.org/10.1093/oxfordjournals.aob.a088063

Smith J. D. Todd P., Staehelin L. A. (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.

https://doi.org/10.1046/j.1365-313x.1997.12061361.x

Kordyum E. L. (1993). Effects of microgravity and clinostating on plants. Giornale Botanico Italiano, 27, 379—385.

https://doi.org/10.1080/11263509309431019

Kordyum E. L., Martyn G. I., Ovcharenko Yu. V. (2008). Growth and differentiation of root cap columella cells and a root proper in stationary conditions and under clinorotation. Cytology and Genetics, 42, 3—12.

https://doi.org/10.1007/s11956-008-1001-9

Moskvitin E. V. (1974). Effects of Space Flight and Dynamic Factors of Flight on Chlorella: Thesis of Ph.D. Moscow.

Lyon C. J. (1970). Choice of rotation rate for the horizontal clinostat. Plant Physiol., 46, 355—358.

https://doi.org/10.1104/pp.46.3.355

Merkys A. I. (1990). Gravity in Growth Processes of Plants. Moscow: Nauka.

Kordyum E. L. (1994). Effects of altered gravity on plant cell processes: Results of recent space and clinostatic experiments. Adv.Space Res., 14, 77 —85.

https://doi.org/10.1016/0273-1177(94)90388-3

Hemmersbach-Krause R., Briegleb W. (1994). Behavior of free-swimming cells under various accelerations. J. Gravit. Physiol., 1, 85—87.

Correll M. J., Pyle T. P., Millar K. D., Sun Y., Yao J., Edelmann R. E., Kiss J. Z. (2013). Transcriptome analyses of Arabidopsis thaliana seedlings grown in space: implications for gravity-responsive genes. Planta, 238, 519—533.

https://doi.org/10.1007/s00425-013-1909-x

Ferl R. J., Koh J., Denison F., Paul A. L. (2015). Spaceflight induces specific alterations in the proteomes of Arabidopsis. Astrobiology, 15, 32—56.

https://doi.org/10.1089/ast.2014.1210

Kwon T., Sparks J. A., Nakashima J., Allen S. N., Tang Y. Blancaflor E. B. (2015). Transcriptional response of Arabidopsis seedlings during space flight reveals peroxidase and cell wall remodelling genes associated with root hair development. Amer. J. Bot., 102, 21—35.

https://doi.org/10.3732/ajb.1400458

Soh H., Auh C., Soh W. Y., Han K., Kim D., Lee S., Rhee Y. (2011). Gene expression changes in Arabidopsis seedlings during short- to long-term exposure to 3-D clinorotation. Planta, 234, 255—270.

https://doi.org/10.1007/s00425-011-1395-y

Hoson T. (2014). Plant growth and morphogenesis under different gravity conditions: relevance to plant life in space. Life, 4, 205—216.

https://doi.org/10.3390/life4020205

Kordyum E. L. Chapman D. K. (2017). Plants and microgravity: Patterns of microgravity effects at the cellular and molecular levels. Cytology and Genetics, 51, 108—116.

https://doi.org/10.3103/S0095452717020049

Uchida A., Yamamoto K. T. (2002). Effects of mechanical vibration on seed germination of Arabidopsis thaliana (L.) Heynh. Plant Cell. Physiol., 43, 647—651.

https://doi.org/10.1093/pcp/pcf079

Downloads

Published

2024-05-14

How to Cite

KORDYUM, E. L., & BRYKOV, V. O. (2024). Statoliths displacement in root statocytes in real and simulated microgravity. Space Science and Technology, 27(2), 78–84. https://doi.org/10.15407/knit2021.02.078