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The Impact of Simulated Microgravity on the Growth of Different Genotypes of the Model Legume Plant Medicago truncatula

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Abstract

Simulated microgravity has been a useful tool to help understand plant development in altered gravity conditions. Thirty-one genotypes of the legume plant Medicago truncatula were grown in either simulated microgravity on a rotating clinostat, or in a static, vertical environment. Twenty morphological features were measured and compared between these two gravity treatments. Within-species genotypic variation was a significant predictor of the phenotypic response to gravity treatment in 100% of the measured morphological and growth features. In addition, there was a genotype–environment interaction (G × E) for 45% of the response variables, including shoot relative growth rate (p < 0.0005), median number of roots (p ∼ 0.02), and root dry mass (p < 0.005). Our studies demonstrate that genotype does play a significant role in M. truncatula morphology and affects the response of plants to the gravity treatment, influencing both the magnitude and direction of the gravity response. These findings are discussed in the context of improving future studies in plant space biology by controlling for genotypic differences. Thus, manipulation of genotype effects, in combination with M. truncatula’s symbiotic relationships with bacteria and fungi, will be important for optimizing legumes for cultivation on long-term space missions.

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References

  • Aarrouf, J., Demandre, C., Darbelley, N., Villard, C., Perbal, G.: Development of the primary root and mobilisation of reserves in etiolated seedlings of Brassica napus grown on a slowly rotating clinostat. J. Plant Physiol. 160(4), 409–413 (2003)

    Article  Google Scholar 

  • Ansdell, M., Ehrenfreund, P., McKay, C.: Stepping stones toward global space exploration. Acta Astronaut. 68(11-12), 2098–2113 (2011)

    Article  Google Scholar 

  • Babuscia, A., Cheung, K.-M., Divsalar, D., Lee, C.: Development of cooperative communication techniques for a network of small satellites and CubeSats in deep space: the SOLARA/SARA test case. Acta Astronaut. 115 (C), 349–355 (2015)

    Article  Google Scholar 

  • Barker, D.G., Pfaff, T., Moreau, D.: Choice of substrates and growth conditions. In: Medicago truncatula Handbook, pp. 1–26 (2006)

  • Branca, A., Paape, T.D., Zhou, P., Briskine, R., Farmer, A.D., Mudge, J., Bharti, A.K., Woodward, J.E., May, G.D., Gentzbittel, L., Ben, C., Denny, R., Sadowsky, M.J., Ronfort, J., Bataillon, T., Young, N.D., Tiffin, P.: Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc. Natl. Acad. Sci. U.S.A. 108(42), E864–70 (2011)

    Article  Google Scholar 

  • Brungs, S., Petrat, G., von der Wiesche, M., Anken, R., Kolanus, W., Hemmersbach, R.: Simulating parabolic flight like g-profiles on ground - a combination of centrifuge and clinostat. Microgravity Sci. Technol. 28(3), 231–235 (2016)

    Article  Google Scholar 

  • Ciaralli, S., Coletti, M., Gabriel, S.B.: Performance and lifetime testing of a pulsed plasma thruster for Cubesat applications. Aerosp. Sci. Technol. 47(C), 291–298 (2015)

    Article  Google Scholar 

  • Ciaralli, S., Coletti, M., Gabriel, S.B.: Results of the qualification test campaign of a pulsed plasma thruster for Cubesat propulsion (PPTCUP). Acta Astronaut. 121(C), 314–322 (2016)

    Article  Google Scholar 

  • Cowles, J.R., Scheld, H.W., Lemay, R., Peterson, C.: Growth and lignification in seedlings exposed to eight days of microgravity. Ann. Bot. 54(S3), 33–48 (1984)

    Article  Google Scholar 

  • Dauzart, A.J.C., Vandenbrink, J.P., Kiss, J.Z.: The effects of clinorotation on the host plant, Medicago truncatula, and its microbial symbionts. Front. Astron. Space Sci. 3(3), 1–10 (2016)

    Google Scholar 

  • Duncan, E.J., Gluckman, P.D., Dearden, P.K.: Epigenetics, plasticity, and evolution: how do we link epigenetic change to phenotype. J. Exp. Zool. (Mol. Dev. Evol.) 322(B), 208–220 (2014)

    Article  Google Scholar 

  • Ferl, R., Wheeler, R., Levine, H.G., Paul, A.L.: Plants in space. Curr. Opin. Plant Biol. 5(3), 258–263 (2002)

    Article  Google Scholar 

  • Galkovskyi, T., Mileyko, Y., Bucksch, A., Moore, B., Symonova, O., Price, C.A., Topp, C.N., Iyer-Pascuzzi, A.S., Zurek, P.R., Fang, S., Harer, J., Benfey, P.N., Weitz, J.S.: GiA roots: software for the high throughput analysis of plant root system architecture. BMC Plant Biol. 12(1), 1–12 (2012)

    Article  Google Scholar 

  • Gan, X., Stegle, O., Behr, J., Steffen, J.G., Drewe, P., Hildebrand, K.L., Lyngsoe, R., Schultheiss, S.J., Osborne, E.J., Sreedharan, V.T., Kahles, A., Bohnert, R., Jean, G., Derwent, P., Kersey, P., Belfield, E.J., Harberd, N.P., Kemen, E., Toomajian, C., Kover, P.X., Clark, R.M., Rätsch, G., Mott, R.: Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477(7365), 419–423 (2011)

    Article  Google Scholar 

  • Garcia, J., Barker, D.G., Journet, E.-P.: Seed storage and germination. In: Medicago truncatula Handbook, pp. 1–9 (2006)

  • Graham, P.H.: Legumes: importance and constraints to greater use. Plant Physiol. 131(3), 872–877 (2003)

    Article  Google Scholar 

  • Herranz, R., Anken, R., Boonstra, J., Braun, 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.: Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology 13(1), 1–17 (2013)

    Article  Google Scholar 

  • Hilaire, E., Peterson, B.V., Guikema, J.A., Brown, C.S.: Clinorotation affects morphology and ethylene production in soybean seedlings. Plant Cell Physiol. 37(7), 929–934 (1996)

    Article  Google Scholar 

  • Hoshino, T., Miyamoto, K., Ueda, J.: Gravity-controlled asymmetrical transport of auxin regulates a gravitropic response in the early growth stage of etiolated pea (Pisum sativum) epicotyls: studies using simulated microgravity conditions on a three-dimensional clinostat and using an agravitropic mutant, ageotropum. J. Plant Res. 120(5), 619–628 (2007)

    Article  Google Scholar 

  • Hoson, T., Kamisaka, S., Masuda, Y., Yamashita, M., Buchen, B.: Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta 203(1), S187–S197 (1997)

    Article  Google Scholar 

  • Hou, G., Mohamalawari, D.R., Blancaflor, E.B.: Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol. 131(3), 1360–1373 (2003)

    Article  Google Scholar 

  • Iversen, T.E., Odegaard, E., Beisvag, T., Johnsson, A., Rasmussen, O.: The behaviour of normal and agravitropic transgenic roots of rapeseed (Brassica napus L.) under microgravity conditions. J. Biotechnol. 47(2-3), 137–154 (1996)

    Article  Google Scholar 

  • Kern, V.D., Schwuchow, J.M., Reed, D.W., Nadeau, J.A., Lucas, J., Skripnikov, A., Sack, F.D.: Gravitropic moss cells default to spiral growth on the clinostat and in microgravity during spaceflight. Planta 221 (1), 149–157 (2005)

    Article  Google Scholar 

  • Kiss, J.Z.: Mechanisms of the early phases of plant gravitropism. CRC Crit. Rev. Plant Sci. 19(6), 551–573 (2000)

    Article  Google Scholar 

  • Kiss, J.Z.: Plant biology in reduced gravity on the Moon and Mars. Plant Biol J. 16(1), 12–17 (2013)

    Google Scholar 

  • Kiss, J.Z.: Conducting plant experiments in space. In: Plant Gravitropism, pp 255–283. Springer, New York (2015)

  • Kiss, J.Z., Aanes, G., Schiefloe, M., Coelho, L.H.F., Millar, K.D.L., Edelmann, R.E.: Changes in operational procedures to improve spaceflight experiments in plant biology in the European Modular Cultivation System. Adv. Space Res. 53(5), 818–827 (2014)

    Article  Google Scholar 

  • Kiss, J.Z., Brinckmann, E., Brillouet, C.: Development and growth of several strains of Arabidopsis seedlings in microgravity. Int. J. Plant Sci. 161(1), 55–62 (2000)

    Article  Google Scholar 

  • Kooke, R., Johannes, F., Wardenaar, R., Becker, F., Etcheverry, M., Colot, V., Vreugdenhil, D., Keurentjes, J.J.B.: Epigenetic basis of morphological variation and phenotypic plasticity in Arabidopsis thaliana. Plant Cell. 27(2), 337–348 (2015)

    Article  Google Scholar 

  • Korte, A., Farlow, A.: The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9(29), 1–9 (2013)

    Google Scholar 

  • Kraft, T., van Loon, J., Kiss, J.Z.: Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211(3), 415–422 (2000)

    Article  Google Scholar 

  • Lehto, K.M., Lehto, H.J., Kanervo, E.A.: Suitability of different photosynthetic organisms for an extraterrestrial biological life support system. Res. Microbiol. 157(1), 69–76 (2006)

    Article  Google Scholar 

  • Levine, H.G., Piastuch, W.C.: Growth patterns for etiolated soybeans germinated under spaceflight conditions. Adv Space Res. 36(7), 1237–1243 (2005)

    Article  Google Scholar 

  • Massa, G.D., Mitchell, C.A.: Sweetpotato vine management for confined food production in a space life-support system. Adv. Space Res. 49(2), 262–270 (2012)

    Article  Google Scholar 

  • Matia, I., Gonzalez-Camacho, F., Herranz, R., Kiss, J.Z., Gasset, G., van Loon, J.J.W.A., Marco, R., Medina, F.J.: Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. J Plant Phys. 167(3), 184–193 (2010)

    Article  Google Scholar 

  • Miransari, M.: Interactions between arbuscular mycorrhizal fungi and soil bacteria. Appl. Microbiol. Biotechnol. 89(4), 917–930 (2010)

    Article  Google Scholar 

  • Miyamoto, K., Yamamoto, R., Fujii, S., Soga, K., Hoson, T., Shimazu, T., Masuda, Y., Kamisaka, S., Ueda, J.: Growth and development in Arabidopsis thaliana through an entire life cycle under simulated microgravity conditions on a clinostat. J. Plant Res. 112(1108), 413–418 (1999)

    Article  Google Scholar 

  • Monje, O., Stutte, G.W., Goins, G.D., Porterfield, D.M.: Farming in space: environmental and biophysical concerns. Adv. Space Res. 31(1), 151–167 (2003)

    Article  Google Scholar 

  • Nadeem, S.M., Ahmad, M., Zahir, Z.A., Javaid, A., Ashraf, M.: The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol. Adv. 32(2), 429–448 (2014)

    Article  Google Scholar 

  • Nakajima, S., Shiraga, K., Suzuki, T., Kondo, N., Ogawa, Y.: Chlorophyll, carotenoid and anthocyanin accumulation in mung bean seedling under clinorotation. Microgravity Sci. Technol. 29(6), 427–432 (2017)

    Article  Google Scholar 

  • National Research Council: Recapturing a Future for Space Exploration. National Academies Press, Washington (2015)

    Google Scholar 

  • Perbal, G., Driss-Ecole, D., Rutin, J., Salle, G.: Graviperception of lentil roots grown in space (Spacelab D1 Mission). Physiol. Plant. 70(2), 119–126 (1987)

    Article  Google Scholar 

  • Pletser, V., Frischauf, N., Cohen, D., Foster, M., Spannagel, R., Szeszko, A., Laufer, R.: First Middle East aircraft parabolic flights for ISU participant experiments. Microgravity Sci. Technol. 29(3), 209–219 (2017)

    Article  Google Scholar 

  • R Core Team: R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2016)

  • Scholz, A., Juang, J.-N.: Toward open source CubeSat design. Acta Astronaut. 115(C), 384–392 (2015)

    Article  Google Scholar 

  • Sherwood, B.: Comparing future options for human space flight. Acta Astronaut. 69(5-6), 346–353 (2011)

    Article  Google Scholar 

  • Soh, H., Srikanth, K., Whang, S.S., Lee, S.: Morphological and gene expression pattern changes in wrky46 mutant Arabidopsis thaliana under altered gravity conditions. Botany 93(6), 333–343 (2015)

    Article  Google Scholar 

  • Song, Y., Wang, X.-D., Rose, R.J.: Oil body biogenesis and biotechnology in legume seeds. Plant Cell Rep. 36(10), 1519–1532 (2017)

    Article  Google Scholar 

  • Stanton-Geddes, J., Paape, T., Epstein, B., Briskine, R., Yoder, J., Mudge, J., Bharti, A.K., Farmer, A.D., Zhou, P., Denny, R., May, G.D., Erlandson, S., Yakub, M., Sugawara, M., Sadowsky, M.J., Young, N.D., Tiffin, P.: Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by Whole-Genome, Sequence-Based Association Genetics in Medicago truncatula. PLoS ONE 8(5), e65688 (2013)

    Article  Google Scholar 

  • Vandenbrink, J.P., Kiss, J.Z.: Space, the final frontier: a critical review of recent experiments performed in microgravity. Plant Sci. 243, 115–119 (2016)

    Article  Google Scholar 

  • Varshney, R.K., Kudapa, H.: Legume biology: the basis for crop improvement. Funct. Plant Biol. 40(12), v–viii (2013)

    Article  Google Scholar 

  • Volkmann, D., Behrens, H.M., Sievers, A.: Development and gravity sensing of cress roots under microgravity. Naturwiss 73(7), 438–441 (1986)

    Article  Google Scholar 

  • Wang, D., Yang, S., Tang, F., Zhu, H.: Symbiosis specificity in the legume - rhizobial mutualism. Cell. Microbiol. 14(3), 334–342 (2012)

    Article  Google Scholar 

  • Wolverton, C., Kiss, J.Z.: An update on plant space biology. Grav. Space Biol. 22(2), 13–20 (2009)

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Mississippi, Oxford, MS, 38677, USA

    Gemma Lionheart & Jason D. Hoeksema

  2. Department of Biology, University of North Carolina-Greensboro, Greensboro, NC, 27412, USA

    Joshua P. Vandenbrink & John Z. Kiss

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  1. Gemma Lionheart
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  2. Joshua P. Vandenbrink
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  3. Jason D. Hoeksema
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  4. John Z. Kiss
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Correspondence to John Z. Kiss.

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Lionheart, G., Vandenbrink, J.P., Hoeksema, J.D. et al. The Impact of Simulated Microgravity on the Growth of Different Genotypes of the Model Legume Plant Medicago truncatula. Microgravity Sci. Technol. 30, 491–502 (2018). https://doi.org/10.1007/s12217-018-9619-4

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