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Phototropism of Arabidopsis thaliana in microgravity and fractional gravity on the International Space Station

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Abstract

While there is a great deal of knowledge regarding plant growth and development in microgravity aboard orbiting spacecraft, there is little information available about these parameters in reduced or fractional gravity conditions (less than the nominal 1g on Earth). Thus, in these experiments using the European Modular Cultivation System on the International Space Station, we studied the interaction between phototropism and gravitropism in the WT and mutants of phytochrome A and B of Arabidopis thaliana. Fractional gravity and the 1g control were provided by centrifuges in the spaceflight hardware, and unidirectional red and blue illumination followed a white light growth period in the time line of the space experiments. The existence of red-light-based positive phototropism in hypocotyls of seedlings that is mediated by phytochrome was confirmed in these microgravity experiments. Fractional gravity studies showed an attenuation of red-light-based phototropism in both roots and hypocotyls of seedlings occurring due to gravitational accelerations ranging from 0.l to 0.3g. In contrast, blue-light negative phototropism in roots, which was enhanced in microgravity compared with the 1g control, showed a significant attenuation at 0.3g. In addition, our studies suggest that the well-known red-light enhancement of blue-light-induced phototropism in hypocotyls is likely due to an indirect effect by the attenuation of gravitropism. However, red-light enhancement of root blue-light-based phototropism may occur via a more direct effect on the phototropism system itself, most likely through the phytochrome photoreceptors. To our knowledge, these experiments represent the first to examine the behavior of flowering plants in fractional or reduced gravity conditions.

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Abbreviations

EC:

Experimental container

EMCS:

European Modular Cultivation System

ISS:

International Space Station

LED:

Light-emitting diode

PHY:

Phytochrome

References

  • Baskin TI (1986) Redistribution of growth during phototropism and nutation in the pea epicotyl. Planta 169:406–414

    Article  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, Schiller P (2002) Experiments with small animals in BIOLAB and EMCS on the International Space Station. Adv Space Res 30:809–814

    Article  PubMed  CAS  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  PubMed  CAS  Google Scholar 

  • Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J, Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR, Adamec J, Peer WA, Murphy AS (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9(6):e1001076. doi:10.1371/journal.pbio.1001076

    Article  PubMed  CAS  Google Scholar 

  • Correll MJ, Kiss JZ (2002) Interactions between gravitropism and phototropism in plants. J Plant Growth Reg 21:89–101

    Article  CAS  Google Scholar 

  • Correll MJ, Coveney KM, Raines SV, Mullen JL, Hangarter RP, Kiss JZ (2003) Phytochromes play a role in phototropism and gravitropism in Arabidopsis roots. Adv Space Res 31:2203–2210

    Article  PubMed  CAS  Google Scholar 

  • Correll MJ, Edelmann RE, Hangarter RP, Mullen JL, Kiss JZ (2005) Ground-based studies of tropisms in hardware developed for the European Modular Cultivation System (EMCS). Adv Space Res 36:1203–1210

    Article  Google Scholar 

  • Ferl RJ, Wheeler R, Levine HG, Paul A-L (2002) Plants in space. Curr Opin Plant Biol 5:258–263

    Article  PubMed  Google Scholar 

  • Franklin KA, Larner VS, Whitelam GC (2005) The signal transducing photoreceptors of plants. Int J Dev Biol 49:653–666

    Article  PubMed  CAS  Google Scholar 

  • Haddy FJ (2007) NASA—has its biological groundwork for a trip to Mars improved? FASEB J 21:643–646

    Article  PubMed  CAS  Google Scholar 

  • Haeder D-P, Lebert M (2001) Graviperception and gravitaxis in algae. Adv Space Res 27:861–870

    Article  Google Scholar 

  • Haeder D-P, Rosum A, Schaefer J, Hemmersbach R (1996) Graviperception in the flagellate Euglena gracilis during a shuttle space flight. J Biotechnol 47:261–269

    Article  CAS  Google Scholar 

  • Halstead TW, Dutcher FR (1987) Plants in space. Annu Rev Plant Physiol 38:317–345

    Article  PubMed  CAS  Google Scholar 

  • Hangarter RP (1997) Gravity, light and plant form. Plant Cell Environ 20:796–800

    Article  PubMed  CAS  Google Scholar 

  • Heathcote DG, Brown AH, Chapman DK (1995) The phototropic response of Triticum aestivum coleoptiles under conditions of low gravity. Plant Cell Environ 18:53–60

    Article  Google Scholar 

  • Janoudi A-K, Poff KL (1997) Multiple phytochromes are involved in red light-induced enhancement of first positive curvature in Arabidopsis thaliana. Plant Physiol 113:975–979

    Article  PubMed  CAS  Google Scholar 

  • Kern VD, Sack FD (1999) Irradiance dependent regulation of gravitropism by red light in protonemata of the moss Ceratodon purpureus. Planta 209:299–307

    Article  PubMed  CAS  Google Scholar 

  • Kiss JZ (1994) Negative phototropism in young gametophytes of the fern Schizaea pusilla. Plant Cell Environ 17:1339–1343

    Article  Google Scholar 

  • Kiss JZ (2006) Up, down, and all around: how plants sense and respond to environmental stimuli. Proc Natl Acad Sci USA 103:829–830

    Article  PubMed  CAS  Google Scholar 

  • Kiss JZ, Mullen JL, Correll MJ, Hangarter RP (2003) Phytochromes A and B mediate red-light-induced positive phototropism in roots. Plant Physiol 131:1411–1417

    Article  PubMed  CAS  Google Scholar 

  • Kiss JZ, Kumar P, Bowman RN, Steele MK, Eodice MT, Correll MJ, Edelmann RE (2007) Biocompatibility studies in preparation for a spaceflight experiment on plant tropisms (TROPI). Adv Space Res 39:1154–1160

    Article  Google Scholar 

  • Kiss JZ, Kumar P, Millar KDL, Edelmann RE, Correll MJ (2009) Operations of a spaceflight experiment to investigate plant tropisms. Adv Space Res 44:879–886

    Article  Google Scholar 

  • Kiss JZ, Millar KDL, Kumar P, Edelmann RE, Correll MJ (2011) Improvements in the re-flight of spaceflight experiments on plant tropisms. Adv Space Res 47:545–552

    Article  CAS  Google Scholar 

  • Kumar P, Montgomery CE, Kiss JZ (2008) The role of phytochrome C in gravitropism and phototropism in Arabidopsis thaliana. Funct Plant Biol 35:298–305

    Article  CAS  Google Scholar 

  • Lariguet P, Fankhauser C (2004) Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. Plant J 40:826–834

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Iino M (1996) Effect of red light on the fluence-response relationship for pulse-induced phototropism of maize coleoptiles. Plant Cell Environ 19:609–614

    Article  Google Scholar 

  • Millar KDL, Kumar P, Correll MJ, Mullen JL, Hangarter RP, Edelmann RE, Kiss JZ (2010) A novel phototropic response to red light is revealed in microgravity. New Phytol 186:648–656

    Article  PubMed  Google Scholar 

  • Millar KDL, Johnson CM, Edelmann RE, Kiss JZ (2011) An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology 11:787–797

    Article  PubMed  CAS  Google Scholar 

  • Mittmann F, Dienstbach S, Weisert A, Forreiter C (2009) Analysis of the phytochrome gene family in Ceratodon purpureus by gene targeting reveals the primary phytochrome responsible for photo- and polarotropism. Planta 230:27–37

    Article  PubMed  CAS  Google Scholar 

  • Molas ML, Kiss JZ (2008) PKS1 plays a role in red-light-based positive phototropism in roots. Plant Cell Environ 31:842–849

    Article  PubMed  CAS  Google Scholar 

  • Molas ML, Kiss JZ (2009) Phototropism and gravitropism in plants. Adv Bot Res 49:1–34

    Article  CAS  Google Scholar 

  • Parks BM, Quail PH, Hangarter RP (1996) Phytochrome A regulates the induction of phototropic enhancement in Arabidopsis thaliana. Plant Physiol 110:155–162

    Article  PubMed  CAS  Google Scholar 

  • Quail PH (2002) Phytochrome photosensory signaling networks. Nat Rev Mol Cell Biol 3:85–93

    Article  PubMed  CAS  Google Scholar 

  • Richter PR, Lebert M, Tahedl H, Haeder D-P (2001) Physiological characterization of gravitaxis in Euglena gracilis and Astasia longa studied on sounding rocket flights. Adv Space Res 27:983–988

    Article  PubMed  CAS  Google Scholar 

  • Sakai T, Wada T, Ishiguro S, Okada K (2000) RPT2: a signal transducer of the phototropic response in Arabidopsis. Plant Cell 12:225–236

    PubMed  CAS  Google Scholar 

  • SAS Institute (2004) SAS/STAT 9.1 user’s guide. SAS Institute Inc., Cary

  • Suetsugu N, Wada M (2007) Phytochrome-dependent photomovement responses mediated by phototropin family proteins in cryptogam plants. Photochem Photobiol 83:87–93

    PubMed  CAS  Google Scholar 

  • Tanaka K, Gotoh TM, Awazu C, Morita H (2005) Regional difference of blood flow in anesthetized rats during reduced gravity induced by parabolic flight. J Appl Physiol 99:2144–2148

    Article  PubMed  Google Scholar 

  • Tsuchida-Mayama T, Sakai T, Hanada A, Uehara Y, Asami T, Yamaguchi S (2010) Role of the phytochrome and cryptochrome signaling pathways in hypocotyl phototropism. Plant J 62:653–662

    Article  PubMed  CAS  Google Scholar 

  • Whippo CW, Hangarter RP (2003) Second positive phototropism results from coordinated co-action of the phototropins and crypotchromes. Plant Physiol 132:1499–1507

    Article  PubMed  CAS  Google Scholar 

  • Wolverton SC, Kiss JZ (2009) An update on plant space biology. Gravit Space Biol Bull 22:13–20

    Google Scholar 

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Acknowledgments

This work was supported by the National Aeronautics and Space Administration [NNX10AF44G to J.Z.K.]. The authors gratefully acknowledge the support of NASA’s Ames Research Center (Mountain View, CA, USA), especially Marianne Steele, Kenny Vassigh, Ken Souza, Sid Sun, Bob Bowman, Kris Vogelsong, and Dave Heathcote. They also thank the Norwegian User Support and Operations Center (especially Carina Helle Berg, Gjert Aanes, and Knut Olav Helleseng), the European Space Agency, and the EADS team (especially Thomas Niedermaier and Anna Grinberg) for their excellent technical support during spaceflight operations. In addition, Caitlin Bregitzer, Maggie Brown, Jessie Hall, and Katie Huntoon aided in the data collection at Miami University. Special thanks to Astronauts Jeffrey Williams and T.J. Creamer and other crew members for performing their experiments on board the ISS.

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Authors and Affiliations

  1. Department of Botany, Miami University, Oxford, OH, 45056, USA

    John Z. Kiss, Katherine D. L. Millar & Richard E. Edelmann

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  1. John Z. Kiss
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  2. Katherine D. L. Millar
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  3. Richard E. Edelmann
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Correspondence to John Z. Kiss.

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J. Z. Kiss and K. D. L. Millar contributed equally to this work.

Electronic supplementary material

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425_2012_1633_MOESM1_ESM.doc

Supplementary material 1 Suppl. Table S1 Additional data on the statistical variations in Fig. 5 and 6 Suppl. Table S2 Additional data on the statistical variations in Fig. 7 and 8 Suppl. Table S3 Additional data on the statistical variations in Fig. 9 (DOC 48 kb)

Supplementary material 2 Suppl. 1 Fig S1 A time-lapse movie of phototropic curvature in hypocotyls of phyB seedlings in response to the unilateral red light from the left of the screen. The movie was compiled from digital still images taken over the 40-h photostimulation period. Note the active nutation of the hypocotyls during the phototropic curvature (MPG 3972 kb)

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Kiss, J.Z., Millar, K.D.L. & Edelmann, R.E. Phototropism of Arabidopsis thaliana in microgravity and fractional gravity on the International Space Station. Planta 236, 635–645 (2012). https://doi.org/10.1007/s00425-012-1633-y

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