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The combined effects of real or simulated microgravity and red-light photoactivation on plant root meristematic cells

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Abstract

Main conclusion

Red light is able to compensate for deleterious effects of microgravity on root cell growth and proliferation. Partial gravity combined with red light produces differential signals during the early plant development.

Light and gravity are environmental cues used by plants throughout evolution to guide their development. We have investigated the cross-talk between phototropism and gravitropism under altered gravity in space. The focus was on the effects on the meristematic balance between cell growth and proliferation, which is disrupted under microgravity in the dark. In our spaceflight experiments, seedlings of three Arabidopsis thaliana genotypes, namely the wild type and mutants of phytochrome A and B, were grown for 6 days, including red-light photoactivation for the last 2 days. Apart from the microgravity and the 1g on-board control conditions, fractional gravity (nominally 0.1g, 0.3g, and 0.5g) was created with on-board centrifuges. In addition, a simulated microgravity (random positioning machine, RPM) experiment was performed on ground, including both dark-grown and photostimulated samples. Photoactivated samples in spaceflight and RPM experiments showed an increase in the root length consistent with phototropic response to red light, but, as gravity increased, a gradual decrease in this response was observed. Uncoupling of cell growth and proliferation was detected under microgravity in darkness by transcriptomic and microscopic methods, but red-light photoactivation produced a significant reversion. In contrast, the combination of red light and partial gravity produced small but consistent variations in the molecular markers of cell growth and proliferation, suggesting an antagonistic effect between light and gravity signals at the early plant development. Understanding these parameters of plant growth and development in microgravity will be important as bioregenerative life support systems for the colonization of the Moon and Mars.

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Abbreviations

EMCS:

European Modular Cultivation System

ISS:

International Space Station

RPM:

random positioning machine

SG:

seedling growth

WT-Ler:

wild type of the Landsberg erecta ecotype of Arabidopsis thaliana

References

  • Borst A, van Loon JJ (2009) Technology and development for the random positioning machine, RPM. Microgravity Sci Technol 21:287–292

    Article  Google Scholar 

  • Boucheron-Dubuisson E, Manzano AI, Le Disquet I, Matia I, Saez-Vasquez J, van Loon JJ, Herranz R, Carnero-Diaz E, Medina FJ (2016) Functional alterations of root meristematic cells of Arabidopsis thaliana induced by a simulated microgravity environment. J Plant Physiol 207:30–41

    Article  CAS  Google Scholar 

  • Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191–1205

    Article  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 

  • Griffiths J, Halliday K (2011) Plant development: light exposure directs meristem fate. Curr Biol 21:R817–R819

    Article  CAS  Google Scholar 

  • Herranz R, Anken R, Boonstra J, Braun M, Christianen PCM, Geest Md, Hauslage J, Hilbig R, Hill RJA, Lebert M, Medina FJ, Vagt N, Ullrich O, Loon JJWAV, Hemmersbach R (2013) Ground-based facilities for simulation of microgravity, including terminology and organism-specific recommendations for their use. Astrobiology 13:1–17

    Article  Google Scholar 

  • Herranz R, Valbuena MA, Youssef K, Medina FJ (2014) Mechanisms of disruption of meristematic competence by microgravity in Arabidopsis seedlings. Plant Signal Behav 9:e28289

    Article  Google Scholar 

  • Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8:217–230

    Article  CAS  Google Scholar 

  • Kiss JZ (2014) Plant biology in reduced gravity on the Moon and Mars. Plant Biol 16(Suppl 1):12–17

    Article  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  CAS  Google Scholar 

  • Kiss JZ, Millar KD, Edelmann RE (2012) Phototropism of Arabidopsis thaliana in microgravity and fractional gravity on the International Space Station. Planta 236:635–645

    Article  CAS  Google Scholar 

  • Kraft TF, van Loon JJ, Kiss JZ (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211:415–422

    Article  CAS  Google Scholar 

  • Laxmi A, Pan J, Morsy M, Chen R (2008) Light plays an essential role in intracellular distribution of auxine carrier PIN2 in Arabidopsis thaliana. PLoS ONE 3:e1510

    Article  Google Scholar 

  • López-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JAH, Beemster GTS, Bögre L, Shanahan H (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:947–968

    Article  Google Scholar 

  • Manzano AI, Larkin O, Dijkstra C, Anthony P, Davey M, Eaves L, Hill R, Herranz R, Medina FJ (2013) Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings. BMC Plant Biol 13:124

    Article  Google Scholar 

  • Manzano AI, Herranz R, Manzano A, Van Loon JJWA, Medina FJ (2016) Early effects of altered gravity environments on plant cell growth and cell proliferation: characterization of morphofunctional nucleolar types in an Arabidopsis cell culture system. Front Astron Space Sci 3:2. https://doi.org/10.3389/fspas.2016.00002

    Article  Google Scholar 

  • Matía I, González-Camacho F, Herranz R, Kiss JZ, Gasset G, van Loon JJWA, Marco R, Medina FJ (2010) Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. J Plant Physiol 167:184–193

    Article  Google Scholar 

  • Medina FJ, Herranz R (2010) Microgravity environment uncouples cell growth and cell proliferation in root meristematic cells: the mediator role of auxin. Plant Signal Behav 5:176–179

    Article  CAS  Google Scholar 

  • Millar KD, 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  Google Scholar 

  • Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspect Biol 2:a001446

    Article  Google Scholar 

  • Reichler SA, Balk J, Brown ME, Woodruff K, Clark GB, Roux SJ (2001) Light differentially regulates cell division and the mRNA abundance of pea nucleolin during de-etiolation. Plant Physiol 125:339–350

    Article  CAS  Google Scholar 

  • Silva-Navas J, Moreno-Risueno MA, Manzano C, Pallero-Baena M, Navarro-Neila S, Tellez-Robledo B, Garcia-Mina JM, Baigorri R, Gallego FJ, del Pozo JC (2015) D-Root: a system for cultivating plants with the roots in darkness or under different light conditions. Plant J 84:244–255

    Article  CAS  Google Scholar 

  • Silva-Navas J, Moreno-Risueno MA, Manzano C, Tellez-Robledo B, Navarro-Neila S, Carrasco V, Pollmann S, Gallego FJ, Del Pozo JC (2016) Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition. Plant Cell 28:1372–1387

    Article  CAS  Google Scholar 

  • Vandenbrink JP, Kiss JZ, Herranz R, Medina FJ (2014) Light and gravity signals synergize in modulating plant development. Front Plant Sci 5:563

    Article  Google Scholar 

  • Vandenbrink JP, Herranz R, Medina FJ, Edelmann RE, Kiss JZ (2016) A novel blue-light phototropic response is revealed in roots of Arabidopsis thaliana in microgravity. Planta 244:1201–1215

    Article  CAS  Google Scholar 

  • Yoshida S, Mandel T, Kuhlemeier C (2011) Stem cell activation by light guides plant organogenesis. Genes Dev 25:1439–1450

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding for this study was provided mainly by the Spanish National Plan for Research and Development (MINECO-ERDF co-funding) Grant ESP2015-64323-R to FJM. The access to ISS and RPM facilities was granted by ESA-ELIPS ILSRA-2009-0932 to FJM and GBF Program GIA Project (contract# 4000105761) to RH. This research was supported also by grants (NNX12A0656 and 80NSSC17K0546) from NASA to JZK and the French Space Agency—CNES to ECD and VPL. MAV and AM were recipients of grants of the Spanish National Program for Young Researchers Training (Refs. BES-2010-035741 and BES-2013-063933, respectively). We would like to thank the skillful technical assistance of Mrs. Mercedes Carnota (CIB-CSIC), the fine support of NASA’s Ames Research Center in the use of TROPI hardware, and the European Space Agency and the Norwegian User Support and Operations Center (N-USOC) for their continuous support throughout the entire “Seedling Growth” space project. Finally, we would like to thank the astronauts on board the ISS for their work, without whom these experiments would have not been possible.

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    Authors and Affiliations

    1. Centro de Investigaciones Biológicas (CSIC), Ramiro de Maeztu, 9, 28040, Madrid, Spain

      Miguel A. Valbuena, Aránzazu Manzano, Raúl Herranz & F. Javier Medina

    2. Institut Systématique, Evolution, Biodiversité (ISYEB), Museum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE.57 rue Cuvier CP39, 75005, Paris, France

      Miguel A. Valbuena & Eugénie Carnero-Diaz

    3. Department of Biology, University of North Carolina at Greensboro, Greensboro, NC, 27402, USA

      Joshua P. Vandenbrink & John Z. Kiss

    4. Faculté de Médécine Rangeuil, Université de Toulouse III UPS, GSBMS-AMIS, Toulouse, France

      Veronica Pereda-Loth

    5. Department of Biology, Miami University, Oxford, OH, 45056, USA

      Richard E. Edelmann

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    1. Miguel A. Valbuena
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    Correspondence to Raúl Herranz or F. Javier Medina.

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    Miguel A. Valbuena and Aránzazu Manzano contributed equally to this work.

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    Valbuena, M.A., Manzano, A., Vandenbrink, J.P. et al. The combined effects of real or simulated microgravity and red-light photoactivation on plant root meristematic cells. Planta 248, 691–704 (2018). https://doi.org/10.1007/s00425-018-2930-x

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