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Higher Plants in Space: Microgravity Perception, Response, and Adaptation

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Abstract

Microgravity is a major abiotic stress in space. Its effects on plants may depend on the duration of exposure. We focused on two different phases of microgravity responses in space. When higher plants are exposed to short-term (seconds to hours) microgravity, such as on board parabolic flights and sounding rockets, their cells usually exhibit abiotic stress responses. For example, Ca 2+-, lipid-, and pH-signaling are rapidly enhanced, then the production of reactive oxygen species and other radicals increase dramatically along with changes in metabolism and auxin signaling. Under long-term (days to months) microgravity exposure, plants acclimatize to the stress by changing their metabolism and oxidative response and by enhancing other tropic responses. We conclude by suggesting that a systematic analysis of regulatory networks at the molecular level of higher plants is needed to understand the molecular signals in the distinct phases of the microgravity response and adaptation.

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References

  • Andreeva, Z., Barton, D., Armour, W.J., Li, M.Y., Liao, L.F., McKellar, H.L., Marc, J.: Inhibition of phospholipase C disrupts cytoskeletal organization and gravitropic growth in Arabidopsis roots. Planta 232, 1263–1279 (2010)

    Article  Google Scholar 

  • Aubry-Hivet, D., Nziengui, H., Rapp, K., Oliveira, O., Paponov, I.A., Li, Y., Hauslage, J., Vagt, N., Braun, M., Ditengou, F.A., Dovzhenko, A., Palme, K.: Analysis of gene expression during parabolic flights reveals distinct early gravity responses in Arabidopsis roots. Plant Biol. 16, 129–141 (2014)

    Article  Google Scholar 

  • Babbick, M., Dijkstra, C., Larkin, O.J., Anthony, P., Davey, M.R., Power, J.B., Lowe, K.C., Cogoli-Greuter, M., Hampp, R.: Expression of transcription factors after short-term exposure ofArabidopsis thaliana cell culture to hypergravity and simulated microgravity (2-D/3-D clinorotation, magnetic levitation). Adv. Space Res. 39, 1182–1189 (2007)

    Article  Google Scholar 

  • Barjaktarović, ž., Schütz, W., Madlung, J., Fladerer, C., Nordheim, N., Hampp, R.: Changes in theeffective gravitational field strength affect the state of phosphorylation of stress related proteins in callus cultures of Arabidopsis thaliana. J. Exp. Bot. 60, 779–789 (2009)

    Article  Google Scholar 

  • Barjaktarović, ž., Nordheim, A., Lamkemeyer, T., Fladerer, C., Hampp, R., Madlung, J.: Time-course of changes in protein amounts of specific proteins upon exposure to hyper-g, 2-D clinorotation and random positioning of Arabidopsis cell cultures. J. Exp. Bot. 58, 4357–4363 (2007)

    Article  Google Scholar 

  • Boonsirichai, K., Sedbrook, J.C., Chen, R., Gilroy, S., Masson, P.H.: ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and laterial auxin transport in plant statocytes. Plant Cell 15, 2612–2625 (2006)

    Article  Google Scholar 

  • Boutté, Y., Grebe, M.: Cellular processes relying on sterol function in plants. Curr. Opin. Plant Biol. 12, 705–13 (2009)

    Article  Google Scholar 

  • Briarty, L.G., Maher, E.P.: Reserve utilization in seeds of Arabidopsis thaliana germinating in microgravity. Int. J. Plant Sci. 165, 545–551 (2004)

    Article  Google Scholar 

  • Briegleb, W.: Some qualitative and quantitative aspects of the fast-rotating clinostat as a research tool. ASGSB Bull. 5, 23–30 (1992)

    Google Scholar 

  • Claassen, D.E., Spooner, B.S.: Impact of altered gravity on aspects of cell biology. Int. Rev. Cytol. 156, 301–373 (1994)

    Article  Google Scholar 

  • Chebli, Y., Geitmann, A.: Gravity research on plants: use of single-cell experiment models. Front Plant Sci. 2, 56 (2011)

    Article  Google Scholar 

  • Correll, M.J., Kiss, J.Z.: Space-based research on plant tropisms. In: Gilroy, S., Masson, P.H. (eds.) Plant tropisms, pp 161–182. Blackwell, Ames, USA (2008)

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

    Article  Google Scholar 

  • Cowles, J.R., Lemay, R., Jahns, G.: Microgravity effects on plant growth and lignification. Astro. Phys. Lett. Commun. 27, 223–228 (1988)

    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, 33–48 (1984)

    Google Scholar 

  • De Micco, V., Arena, C., Pignalosa, D., Durante, M.: Review. Effects of sparsely and densely ionizing radiation on plants. Rad. Env. Biophy. 50, 1–19 (2011)

    Article  Google Scholar 

  • De Micco, V., De Pascale, S., Paradiso, R., Arone, G.: Microgravity effects on different stages of higher plant life cycle and completion of the seed-to -seed cycle. Plant Biol. 16, 31–38 (2014)

    Article  Google Scholar 

  • Driss-Ecole, D.L.V., Carnero-Diaz, E., Perbal, G.: Gravisensitivity and automorphogenesis of lentil seedling roots grown on board the international space station. Physiol. Plant 134, 191–201 (2008)

    Article  Google Scholar 

  • Fasano, J.M., Swanson, S.J., Blancaflor, E.B., Dowd, P.E., Kao, T.H., Gilroy, S.: Changes in root cap pH are required for the gravity response of the Arabidopsisroot. Plant Cell 13, 907–921 (2001)

    Article  Google Scholar 

  • Fengler, S., Spirer, I., Neef, M., Ecke, M., Nieselt, K., Hampp, R.: A whole-genome microarray study of Arabidopsis thaliana semisolid callus cultures exposed to microgravity and nonmicrogravity related spaceflight conditions for 5 days on board of Shenzhou 8. BioMed Res. Int. Article ID 547495 (2015)

  • Geilfus, C.M., Mühling, K.H., Kaiser, H., Plieth, C.: Bacterially produced Pt-GFP as ratiometric dual-excitation sensor for in planta mapping of leaf apoplastic pH in intact Avena sativa and Vicia faba. Plant Methods 10, 31 (2014)

    Article  Google Scholar 

  • Gillaspy, G.E.: The cellular language of myo-inositol signaling. New Phytol. 192, 823–839 (2011)

    Article  Google Scholar 

  • Gjetting, K.S., Ytting, C.K., Schulz, A., Fuglsang, A.T.: Live imaging of intra- and extracellular pH in plants using pH usion, a novel genetically encoded biosensor. J. Exp. Bot. 63, 3207–3218 (2012)

    Article  Google Scholar 

  • Hampp, R., Hoffmann, E., Schönherr, K., Johann, P., De Filippis, L.: Fusion and metabolism of plant cells as affected by microgravity. Planta 203, S42–53 (1997)

    Article  Google Scholar 

  • Hausmann, N., Fengler, S., Hennig, A., Franz-Wachtel, M., Hampp, R., Neef, M.: Cytosolic calcium, hydrogen peroxide and related gene expression and protein modulation in Arabidopsis thaliana cell cultures respond immediately to altered gravitation: parabolic flight data. Plant Biol. 16, 120–128 (2014)

    Article  Google Scholar 

  • Hejnowicz, Z., Sondag, C., Alt, W., Sievers, A.: Temporal course of graviperception in intermittently stimulated cress roots. Plant Cell Environ. 21, 1293–300 (1998)

    Article  Google Scholar 

  • Herranz, R., Manzano, A.I., van Loon, J.J., Christianen, P.C., Medina, F.J.: Proteomic signature of Arabidopsis cell cultures exposed to magnetically induced hyper- and microgravity environments. Astrobiology 13, 217–224 (2013)

    Article  Google Scholar 

  • Hoshino, T., Miyamoto, K., Ueda, J.: Automorphosis and auxin polar transport of etiolated pea seedlings under microgravity conditions. Biol. Sci. Space 18, 94–95 (2004)

    Google Scholar 

  • Hoson, T., Soga, K., Wakabayashi, K., Hashimoto, T., Karahara, I., Yano, S., Tanigaki, F., Shimazu, T., Kasahara, I., Masuda, D., Kamisaka, S.: Growth stimulation in inflorescences of an Arabidopsis tubulin mutant under microgravity conditions in space. Plant Bio. Supp. 1, 91–96 (2014)

    Article  Google Scholar 

  • Hoson, T., Saiki, M., Kamisaka, S., yamashita, M.: Automorphogenesis and gravitropism of plant seedlings grown under microgravity conditions. Adv. Space Res. 27, 933–940 (2001)

    Article  Google Scholar 

  • Hoson, T.K.S., Yamamoto, R., Yamashita, M., Masuda, Y.: Automorphosis of maize shoots under simulated microgravity on a three-dimensional clinostat. Physiol. Plant 93, 346–351 (1995)

    Article  Google Scholar 

  • Im, Y.J., Phillippy, B.Q., Perera, I.Y.: InsP3 in plant cells. In: Munnik, T (ed.) Lipid signaling in plants, pp 145–160. Springer, Berlin, Germany (2010)

  • Inglis, P.W., Ciampi, A.Y., Salomão, A.N., Costa Tda, S., Azevedo, V.C.: Expression of stress-related genes in zebrawood (Astronium fraxinifolium, Anacardiaceae) seedlings following germination in microgravity. Gene. Mol. Biol. 37, 81–92 (2014)

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Joo, J.H., Bae, Y.S., Lee, J.S.: Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126, 1055–1060 (2001)

    Article  Google Scholar 

  • Kittang, A.I., van Loon, J.J., Vorst, O., Hall, R.D., Fossum, K., Iversen, T.H.: Ground based studies of gene expression in Arabidopsis exposed to gravity stresses. J Gravit. Physiol. 11, 223–224 (2004)

    Google Scholar 

  • Kliss, M., Macelroy, R., Borchers, B., Farrance, M., Nelson, T., Blackwell, C., Yendler, B., et al.: Controlled ecological life support systems (CELSS) flight experimentation. Adv. Space. Res. 14, 61–69 (1994)

    Article  Google Scholar 

  • Kozeko, L., Kordyum, E.: Effect of hypergravtiy on the level of heat shock protein 70 and 90 in pea seedlings. Microgravitity Sci. Technol. 21, 175–178 (2009)

    Article  Google Scholar 

  • Kriegs, B., Theisen, R., Schnabl, H.: Inositol 1,4,5-trisphosphate and Ran expression during simulated and real microgravity. Protoplasma 229, 163–174 (2006)

    Article  Google Scholar 

  • Krinke, O., Novotná, Z., Valentová, O., Martinec, J.: Inositol trisphosphate receptor in higher plants: is it real. J. Exp. Bot. 58, 361–376 (2007)

    Article  Google Scholar 

  • Leitz, G., Kang, B.H., Schoenwaelder, M.E., Staehelin, L.A.: Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell 21, 843–60 (2009)

    Article  Google Scholar 

  • Link, B.M., Wagner, E.R., Cosgrove, D.J.: The effect of a microgravity (space) environment on the expression of expansins from the peg and root tissues of Cucumis sativus. Physiol. Plant 113, 292–300 (2001)

    Article  Google Scholar 

  • Manzano, A.I., van Loon, J.J., Christanen, P.C., Gonzalez-Rubio, J.M., Medina, F.J., Herranz, R.: Gravitational and magnetic field variations synergize to cause subtle variations in the global transcriptional state of Arabidopsis in vitro callus cultures. BMC Genomics 13, 105 (2012)

    Article  Google Scholar 

  • Martzivanou, M., Babbick, M., Cogoli-Greuter, M., Hampp, R.: Microgravity-related changes in gene expression after short-term exposure of Arabidopsi thaliana cell cultures. Protoplasma 229, 155–162 (2006)

    Article  Google Scholar 

  • Matía, I., Van Loon, J.J.W.A., Carnero-Díaz, E., Marco, R., Medina, F.J.: Seed germination and seedling growth under simulated microgravity causes alterations in plant cell proliferation and ribosome biogenesis. Microgravity Sci. Technol. 21, 169–174 (2009)

    Article  Google Scholar 

  • Mazars, C., Brière, C., Grat, S., Pichereaux, C., Rossignol, M., Pereda-Loth, V., Eche, B., Boucheron-Dubuisson, E., Disquet, I.L., Medina, F.J., Graziana, A., Carnero-Diaz, E.: Microgravity induces changes in microsome-associated proteins of Arabidopsis seedlings grown on board the international space station. Plos one e91814, 9 (2014)

    Google Scholar 

  • Millar, K.D.L., Kumar, P., Correll, M.J., Mullen, J.L., Hangarter, R.P., Edelmann, R.E., Kiss, J.Z.: A novel phototropic response to red light is revealed in microgravity. New Phytol. 186, 648–656 (2010)

    Article  Google Scholar 

  • Monshausen, G.B., Miller, N.D., Murphy, A.S., Gilroy, S.: Dynamics of auxin-dependent Ca2 + and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J. 65, 309–318 (2011)

    Article  Google Scholar 

  • Moriwaki, T., Miyazawa, Y., Kobayashi, A., Takahashi, H.: Molecular mechanisms of hydrotropism in seedling roots of Arabidopsis thaliana (Brassicaceae). Amer. J. Bot. 100, 25–34 (2013)

    Article  Google Scholar 

  • Nasir, A., Strauch, S.M., Becker, I., Sperling, A., Schuster, M., Richter, P.R., WeiSSkopf, M., Ntefidou, M., Daiker, V., An, Y.A., Li, X.Y., Liu, Y.D., Lebert, M.: The influence of microgravity on Euglena gracilis as studied on Shenzhou 8. Plant Biol. Suppl. 1, 113–119 (2014)

  • Nedukha, E.: Effects of microgravity on the structure and function of plant cell walls. Int. Rev. Cytol. 170, 39–77 (1997)

    Article  Google Scholar 

  • Paul, A-L., Daugherty, C.J., Bihn, E.A., Chapman, D.K., Norwood, K.L.L., Ferl, R.J.: Transgene expression patterns indicate that spaceflight affects stress signal perception and transduction in Arabidopsis. Plant Physiol. 126, 613–621 (2001)

    Article  Google Scholar 

  • Paul, A-L., Popp, M.P., Gurley, W.B., Guy, C., Norwood, K.L., Ferl, R.J.: Arabidopsis gene expression patterns are altered during spaceflight. Adv. Space Res. 36, 1175–1181 (2005)

    Article  Google Scholar 

  • Paul, A-L., Wheeler, R.M., Levine, H.G., Jerl, R.J.: Fundamental plant biology enabled by the space shuttle. Amer. J. Bot. 100, 226–234 (2013a)

    Article  Google Scholar 

  • Paul, A-L., Zupanska, A.K., Schultz, E., Rerl, R.J.: Organ-specific remodeling of the Arabidopsis transcriptome in response to space flight. BMC Plant Biol. 13, 112 (2013b)

    Article  Google Scholar 

  • Paul, A.L., Amalfitano, C.E., Ferl, R.J.: Plant growth strategies are remodeled by spaceflight. BMC Plant Biol. 12, 232 (2012)

    Article  Google Scholar 

  • Paul, A-L., Manak, M.S., Mayfield, J.D., Reyes, M.F., Gurley, W.B., Ferl, R.J.: Parabolic flight induces changes in gene expression patterns in Arabidopsis thaliana. Astrobiology 11, 743–758 (2011)

    Article  Google Scholar 

  • Perbal, G., Driss-Ecole, D.: Mechanotransduction in gravisensing cells. Trends Plant Sci. 8, 498–504 (2003)

    Article  Google Scholar 

  • Perbal, G., Jeune, B., Lefranc, A., Carnero-Diaz, E., Driss-Ecole, D.: The dose-response curve of the gravitropic reaction: a re-analysis. Physiol. Plant 114, 336–42 (2002)

    Article  Google Scholar 

  • Perera, I.Y., Heilmann, I., Boss, W.F.: Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. PNAS 96, 5838–5843 (1999)

    Article  Google Scholar 

  • Perera, I.Y., Heilmann, I., Chang, S.C., Boss, W.F.: A role for inositol 1,4,5-trisphosphate in gravitropic signaling and the retention of cold-perceived gravistimulation of oat shoot pulvini. Plant Physiol. 125, 1499–1507 (2001)

    Article  Google Scholar 

  • Plieth, C.: Calcium: just another regulator in the machinery of life. Ann. Bot. 96, 1–8 (2005)

    Article  Google Scholar 

  • Poovaiah, B.W., Yang, T., van Loon, J.J.: Calcium/calmodulin-mediated gravitropic response in plants. J. Gravit. Physiol. 9, 211–214 (2002)

    Google Scholar 

  • Ruyters, G., Braun, M.: Plant biology in space: recent accomplishments and recommendations for future research. Plant Biol. Suppl. 1, 4–11 (2014)

    Article  Google Scholar 

  • Salisbury, F.B., Bugbee, B.: Plant productivity in controlled environments. HortScience 23, 293–299 (1988)

    Google Scholar 

  • Salinas-Mondragon, R.E., Kajla, J.D., Perera, I.Y., Brown, C.S., Sederoff, H.W.: Role of inositol 1,4,5-triphosphate signalling in gravitropic and phototropic gene expression. Plant Cell Environ. 33, 2041–2055 (2010)

    Article  Google Scholar 

  • Sato, E.M., Hijazi, H., Bennett, M.J., Vissenberg, K., Swarup, R.: New insights into root gravitropic signalling. J. Exp. Bot. 515, 511–515 (2014)

    Google Scholar 

  • Sato, F., Takeda, S., Matsushima, H., Yamada, Y.: Cell growth and organ differentiation in cultured tobacco cells under spaceflight condition. Biol. Sci. Space 13, 18–24 (1999)

    Article  Google Scholar 

  • Smith, C.M., Desai, M., Land, E.S., Perera, I.Y.: A role for lipid-mediated signaling in plant gravitropism. Am. J. Bot. 100, 153–160 (2013)

    Article  Google Scholar 

  • Soga, K., Wakabayashi, K., Kamisaka, S., hoson, T.: Stimulation of elongation growth and xyloglucan breakdown in Arabidopsis hypocotyls under microgravity conditions in space. Planta 215, 1040–1046 (2002)

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Stanković, B., Volkmann, D., Sack, F.D.: Autotropism, automorphogenesis, and gravity. Physiol. Plant 102, 328–335 (1998)

    Article  Google Scholar 

  • Stutte, G.W., Monje, O., Hatfield, R.D., Paul, A-L., Ferl, R.J., Simone, C.G.: Microgravity effects on leaf morphology, cell structure, carbon metabolism and mRNA expression of dwarf wheat. Planta 224, 1038–1049 (2006)

    Article  Google Scholar 

  • Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K., Dolan, L.: Local positive feedback regulation determines cell shape in root hair cells. Science 319, 1241–1244 (2008)

    Article  Google Scholar 

  • Tako, Y., Arai, R., Tsuga, S., Komatsubara, O., Masuda, T., Nozoe, S., Nitta, K.: CEEF, closed ecology experiment facilities. Gravit. Space Biol. 23, 13–24 (2010)

    Google Scholar 

  • Tan, C., Wang, H., Zhang, Y., Qi, B., Xu, G., Zheng, H.Q.: A proteomic approach to analyzing responses of Arabidopsis thaliana root cells to different gravitational conditions using an agravitropic mutant, pin2 and its wild type. Proteome Sci. 9, 72 (2011)

    Article  Google Scholar 

  • Toker, A.: Phosphoinositides and signal transduction. Cell Mol. Life Sci. 59, 761–779 (2002)

    Article  Google Scholar 

  • Toyota, M., Furuichi, T., Tatsumi, H., Sokabe, M.: Cytoplasmic calcium increases in response to changes in the gravity vector in hypocotyls and petioles of Arabidopsis seedlings. Plant Physiol. 146, 505–14 (2008)

    Article  Google Scholar 

  • Tripathy, B.C., Brown, C.S., Levine, H.G., Krikorian, A.D.: Growth and photosynthetic responses of wheat plants grown in space. Plant Physiol. 110, 801–806 (1996)

    Article  Google Scholar 

  • Vandenbrink, J.P., Kiss, J.Z., Herranz, R., Medina, F.J.: Light and gravity signals synergize in modulating plant development. Front. Plant Sci. 5, 563 (2014)

    Article  Google Scholar 

  • Volovik, O.I., Kordyum, E.L., Guikema, J.A.: Some characteristics of photosynthetic apparatus under conditions of spaceflight. J. Gravit. Physiol. 6, P127–128 (1999)

    Google Scholar 

  • Wang, H., Zheng, H.Q., Sha, W., Zeng, R., Xia, Q.C.: A proteomic approach to analyzing responses of Arabidopsis thaliana callus cells to clinostat rotation. J. Exp. Bot. 57, 827–835 (2006)

    Article  Google Scholar 

  • Wheeler, R.M.: Plants for human life support in space: from Myers to Mars. Gravit. Space Biol. 23, 25–35 (2010)

    Google Scholar 

  • Wolff, S.A., Coelho, L.H., Karoliussen, I., Jost, A-I. K.: Effects of the extraterrestrial environment on plants: recommendations for future space experiments for the MELiSSA higher plant compartment. Life 4, 189–204 (2014)

    Article  Google Scholar 

  • Wong, H.L., Pinontoan, R., Hayashi, K., Tabata, R., Yaeno, T., Hasegawa, K., Kojima, C., Yoshioka, H., Iba, K., Kawasaki, T., Shimamoto, K.: Regulation of rice NADPH oxidase by binding of rac GTPase to its N-terminal extension. Plant Cell 19, 4022–4034 (2007)

    Article  Google Scholar 

  • Xu, D., Guo, S., Liu, M.: Identification of miRNAs involved in long-term simulated microgravity response in Solanum lycopersicum. Plant Physiol. Biochem. 66, 10–19 (2013)

    Article  Google Scholar 

  • Zenko, C., Komatu, K., Yokoyama, R., Nishitani, K., Kamisaka, S.: Effect of hypergravity stimulus on XTH gene expression in Arabidopsis thaliana. Biol. Sci. Space 17, 259–260 (2003)

    Google Scholar 

  • Zhang, Y., Wang, L., Xie, J., Zheng, H.Q.: Differential protein expression profiling of Arabidopsis thaliana callus under microgravity on board the Chinese SZ-8 spacecraft. Planta 241, 475–488 (2015)

    Article  Google Scholar 

  • Zheng, H.Q., Wang, H., Wei, N., Chen, A.D., Wang, L.F., Zheng, W.B., Zhang, T.: Live imaging technique for studies of growth and development of Chinese cabbage under microgravity in a recoverable satellite (SJ-8). Microgravity Sci. Tech. 20, 137–143 (2008)

    Article  Google Scholar 

  • Zupanska, A.K., Denison, F.C., Ferl, R.J., Paul, A-L.: Spaceflight engages heat shock protein and other molecular chaperone genes in tissue culture cells of Arabidopsis thaliana. Am. J. Bot. 100, 235–248 (2013)

    Article  Google Scholar 

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Acknowledgments

The authors are indebted to Professor Mian Long for helpful suggestion and comments on the manuscript. This work was supported by the National Basic Research Program of China (2011CB710902), the China Manned Space Flight Technology project, and the Strategic Pioneer Projects of the Chinese Academy of Sciences (XDA04020202).

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Correspondence to Hui Qiong Zheng.

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Zheng, H.Q., Han, F. & Le, J. Higher Plants in Space: Microgravity Perception, Response, and Adaptation. Microgravity Sci. Technol. 27, 377–386 (2015). https://doi.org/10.1007/s12217-015-9428-y

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