Skip to main content
Log in

Lunar gravity affects leaf movement of Arabidopsis thaliana in the International Space Station

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Cyclic leaf ascent and descent occur in synchrony and phase congruence with the lunisolar tidal force under a broad range of conditions.

Digitized records of the vertical leaf movements of Arabidopsis thaliana were collected under space flight conditions in the International Space Station (ISS). Oscillations of leaf movements with periods of 45 and 90 min were found under light-adapted conditions, whereas in darkness, the periods were 45, 90, and 135 min. To demonstrate the close relationship between these oscillations and cyclical variations of the lunisolar gravitational force, we estimated the oscillations of the in-orbit lunisolar tide as they apply to the ISS, with the aid of the Etide software application. In general, in-orbit lunisolar gravitational profiles exhibited a periodicity of 45 min. Alignment of these in-orbit oscillations with the oscillations of Arabidopsis leaf movement revealed high degrees of synchrony and a congruence of phase. These data corroborate previous results which suggested a correlative relationship and a possible causal link between leaf movement rhythms obtained on ground and the rhythmic variation of the lunisolar tidal force.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ISS:

International Space Station

EMCS:

European Modular Cultivation System

References

  • Barlow P, Fisahn J (2012) Lunisolar tidal force and the growth of plant roots, and some other of its effects on plant movements. Ann Bot 110:301–318

    Article  PubMed Central  PubMed  Google Scholar 

  • Barlow PW, Klingelé E, Klein G, Mikulecký M Sr (2008) Leaf movements of bean plants and lunar gravity. Plant Signal Behav 3:1083–1090

    Article  Google Scholar 

  • Barlow PW, Mikulecký M Sr, Střeštík J (2010) Tree-stem diameter fluctuates with the lunar tides and perhaps with geomagnetic activity. Protoplasma 247:25–43

    Article  PubMed  Google Scholar 

  • Brinckmann E (2005) ESA hardware for plant research on the International Space Station. Adv Space Res 36:1162–1166

    Article  Google Scholar 

  • Brinckmann E, Brillouet C (2000) Space plant research on the ISS with the European Modular Cultivation System and with BIOLAB. SAE Tech Pap Ser Paper No. 2000-01-2472

  • Crossley D, Hinderer J, Boy JP (2005) Time variations of the European gravity field from superconducting gravimeters. Geophys J Int 161:257–264

    Article  Google Scholar 

  • de Mairan J (1729) Observation botanique. Hist Acad Roy Sci (Paris) 1729:35–36

  • Dodd AN, Parkinson K, Webb AAR (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol 162:63–70

    Article  Google Scholar 

  • Dorda G (2010) Quantisierte Zeit und die Vereinheitlichung von Gravitation und Elektromagnetismus. Cuvillier Verlag, Göttingen Germany. ISBN-10: 3869552409. http://www.cuvillier.de/flycms/de/html/30/-UickI3zKPS7xcE0=/Buchdetails.html

  • Dornbusch T, Michaud O, Xenarios I, Fankhauser C (2014) Differentially phased leaf growth and movements in Arabidopsis depend on coordinated circadian and light regulation. Plant Cell 26:3911–3921

    Article  CAS  PubMed  Google Scholar 

  • Engelmann W, Simon K, Phen CJ (1992) Leaf movement rhythm in Arabidopsis thaliana. Z Naturforsch 47:925–928

    Google Scholar 

  • Fisahn J, Yazdanbakhsh N, Klingelé E, Barlow PW (2012) Arabidopsis thaliana root growth kinetics and lunisolar tidal acceleration. New Phytol 195:346–355

    Article  PubMed  Google Scholar 

  • Flügel A (1949) Die Gesetzmässigkeiten der endogenen Tagesrhythmik. Planta 37:337–375

    Article  Google Scholar 

  • Fossum K, Kittang AI, Iversen T-H, Brinckmann E, Schiller P (2005) Testing the European Modular Cultivation System (EMCS) for ISS plant and cell research. In: International conference on environmental systems, Rome, ITALY. SAE Technical Paper Series 2005-01-2841

  • Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377

    Article  CAS  PubMed  Google Scholar 

  • Hennessey TL, Field CB (1992) Evidence of multiple circadian oscillators in bean plants. J Biol Rhyth 7:105–113

    Article  CAS  Google Scholar 

  • Hernandez MP, Arambarri AM (2010) Stomatal distribution, stomatal density and daily leaf movement in Acacia aroma (Leguminosae). Bol Soc Argent Bot 45:273–284

    Google Scholar 

  • Johnsson A, Solheim BGB, Iversen T-H (2009) Gravity amplifies and microgravity decreases circumnutations in Arabidopsis thaliana stems: results from a space experiment. New Phytol 182:621–629

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Ono N, Hayashi Y, Morimoto S, Nakamura S, Soda M, Kato Y, Ohnishi M, Nakano T, Inoue S, Shimazaki K (2011) FLOWERING LOCUS T regulates stomatal opening. Curr Biol 21:1232–1238

    Article  CAS  PubMed  Google Scholar 

  • Klein G (2007) Farewell to the internal clock. A contribution in the field of chronobiology. Springer, New York

    Google Scholar 

  • Konopliv AS, Binder AB, Hood LL, Kucinskas AB, Sjogren L, Williams JG (1998) Improved gravity field of the moon from Lunar Prospector. Science 281:1476–1480

    Article  CAS  PubMed  Google Scholar 

  • Konopliv AS, Asmar SW, Carranza E, Sjogren WL, Yuan DN (2001) Recent gravity models as a result of the Lunar Prospector mission. Icarus 150:1–18

    Article  Google Scholar 

  • Lasceve G, Leymarie J, Vavasseur A (1997) Alterations in light-induced stomatal opening in a starch deficient mutant of Arabidopsis thaliana L. deficient in chloroplast phosphoglucomutase activity. Plant, Cell Environ 20:350–358

    Article  CAS  Google Scholar 

  • Longman IM (1959) Formulas for computing the tidal accelerations due to the moon and the sun. J Geophys Res 64:2351–2355

    Article  Google Scholar 

  • Lüttge U (2003) Circadian rhythmicity: Is the “biological clock” hardware or software? Prog Bot 64:277–319

    Article  Google Scholar 

  • Mayer W-E (1981) Energy-dependent phases of the circadian clock and the clock-controlled leaf movements of Phaseolus coccineus L. Planta 152:292–301

    Article  CAS  PubMed  Google Scholar 

  • Moran N (2007) Osmoregulation of leaf motor cells. FEBS Lett 581:2337–2347

    Article  CAS  PubMed  Google Scholar 

  • Paul AL, Zupanska AK, Ostrow DT, Zhang Y, Sun Y, Li JL, Shanker S, Farmerie WG, Amalfitano CF, Ferl RJ (2012) Spaceflight transcriptomes: unique responses to a novel environment. Astrobiology 12:40–56

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paul AL, Zupanska AK, Schultz ER, Ferl RJ (2013) Organ-specific remodeling of the Arabidopsis transcriptome in response to spaceflight. BMC Plant Biol 13:112

    Article  PubMed Central  PubMed  Google Scholar 

  • Rascher U, Hütt MT, Siebke K, Osmond B, Beck F, Lüttge U (2001) Spatiotemporal variation of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators. Proc Nat Acad Sci USA 98:11801–11805

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rauf M, Arif M, Fisahn J, Xue G-P, Balazadeh S, Mueller-Roeber B (2013) NAC transcription factor speedy hyponastic growth regulates flooding-induced leaf movement in Arabidopsis. Plant Cell 25:4941–4955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roenneberg T, Morse D (1993) Two circadian oscillators in one cell. Nature 362:362–364

    Article  Google Scholar 

  • Rosa LM, Dillenbur LR, Irwin N, Forseth IN (1991) Responses of soybean leaf angle, photosynthesis and stomatal conductance to leaf and soil water potential. Ann Bot 67:51–58

    Google Scholar 

  • Solheim BGB, Kittang AI, Iversen T-H, Johnsson A (2006) Preparatory experiments for long-term observation of Arabidopsis circumnutations in microgravity. Acta Astronaut 59:46–53

    Article  Google Scholar 

  • Solheim BGB, Johnsson A, Iversen T-H (2009) Ultradian rhythms in Arabidopsis thaliana leaves in microgravity. New Phytol 183:1043–1052

    Article  CAS  PubMed  Google Scholar 

  • Somers DE, Schultz TF, Milnamow M, Kay SA (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101:319–329

    Article  CAS  PubMed  Google Scholar 

  • Sweeney BM (1969) Rhythmic phenomena in plants. Academic Press, London

    Google Scholar 

  • Uehlein N, Kaldenhoff R (2008) Aquaporins and plant leaf movements. Ann Bot 101:1–4

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xu J, Sun H, Ducarme BA (2004) A global experimental model for gravity tides of the Earth. J Geodynamics 38:293–306

    Article  Google Scholar 

  • Zürcher E, Cantiani M-G, Sorbetti Guerri F, Michel D (1998) Tree stem diameters fluctuate with tide. Nature 392:665–666

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. Dr. Anders Johnsson (Department of Physics, Norwegian University of Science and Technology, N-7491 Trondheim, Norway), Dr. Bjarte Solheim (Department of Physics, Norwegian University of Science and Technology, N-7491 Trondheim, Norway), and Prof. Dr. Tor-Henning Iversen (Department of Biology, The Plant BioCentre, Norwegian University of Science and Technology, N-7491 Trondheim, Norway) for providing additional results and details of the conditions in the ISS during the in-orbit experiments, for reading the manuscript and providing valuable comments. We would like to thank Prof. Dr. Nima Yazdanbakhsh for critical discussion of the described experiments. Special thanks to Prof. Dr. em. Enno Brinckmann for providing valuable further details on the construction of the EMCS.

Conflict of interest

We declare no conflict of interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joachim Fisahn.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fisahn, J., Klingelé, E. & Barlow, P. Lunar gravity affects leaf movement of Arabidopsis thaliana in the International Space Station. Planta 241, 1509–1518 (2015). https://doi.org/10.1007/s00425-015-2280-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-015-2280-x

Keywords

Navigation