Summary
Plans by the space program to use plants for food supply and environmental regeneration have led to an examination of how plants grow in microgravity. Because secondary metabolic compounds are so important in determining the nutritional and flavor characteristics of plants—as well as making plants more resistant to biotic and abiotic stresses—their responses to altered gravity are now being studied. These experiments are technically challenging because temperature, humidity, atmospheric composition, light, and water status must be maintained around the plant while simultaneously altering the g-load, either in the free-fall of orbital spacecraft or on a centrifuge rotor. In general, plants have shown increased accumulation of small secondary metabolites in microgravity (<10−3 g), while these have decreased in hypergravity (>1-g). Gravity-related changes in the plant environment as well as mechanical loading effects account for these responses.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ferl, R., Wheeler, R., Levine, H.G. and Paul, A. (2002). Plants in space. Curr. Opin. Plant Biol. 5, 258–263.
Wink, M. (1999). Functions of plant secondary metabolites and their exploitation in biotechnology. Annual Plant Review, Vol. 3. Sheffield Academic, England.
Musgrave, M.E. (2002). Seeds in space. Seed Sci. Res. 12, 1–16.
Musgrave, M.E., Kuang, A., Tuominen, L.K., Levine, L.H. and Morrow, R.C. (2005). Seed storage reserves and glucosinolates in Brassica rapa L. grown on the International Space Station. J. Am. Soc. Hort. Sci. 130, 848–856.
Pence, B.C. and Yang, T.C. (2000). Antioxidants: radiation and stress. In: Nutrition in Space-Flight and Weightlessness Models (Lane, H.W. and Schoeller, D.A., eds.) CRC Press, Boca Raton, FL, pp. 233–251.
Fang, Y., Yang, S. and Wu, G. (2002). Free radicals, antioxidants, and nutrition. Nutrition 18, 872–879.
Olabi, A.A., Lawless, H.T., Hunter, J.B., Levitsky, D.A. and Halpern, B.P. (2002). The effect of microgravity and space flight on the chemical senses. J. Food Sci. 67(2), 468–478.
Ryba-White, M., Nedukha, O., Hilaire, E., Guikema, J.A., Kordyum, E. and Leach, J.E. (2001). Growth in microgravity increases susceptibility of soybean to a fungal pathogen. Plant Cell Physiol. 42, 657–664.
Bishop, D.L., Levine, H.G., Kropp, B.R. and Anderson, A.J. (1997). Seedborne fungal contamination: consequences in space-grown wheat. Phytopathology 87, 1125–1133.
Durzan, D.J. (1999). Gravisensing, apoptosis, and drug recovery in Taxus cell suspensions. Gravit. Space Biol. Bull. 12, 47–55.
Demain, A.L. and Fang, A. (2001). Secondary metabolism in simulated microgravity. Chem. Rec. 1, 333–346.
Gao, Q., Fang, A., Pierson, D.L., Mishra, S.K. and Demain, A.L. (2001). Shear stress enhances microcin B17 production in a rotating wall bioreactor, but ethanol stress does not. Appl. Environ. Microbiol. 56, 384–387.
Moore, R. (1990). Comparative effectiveness of a clinostat and a slow-turning lateral vessel at mimicking the ultrastructural effects of microgravity in plant cells. Ann. Bot. 66, 541–549.
Levine, L.H., Levine, H.G., Stryjewski, E.C., Prima, V. and Piastuch, W.C. (2001). Effect of spaceflight on isoflavonoid accumulation in etiolated soybean seedlings. J. Gravit. Physiol. 8, 21–27.
Voeste, D., Levine, L.H., Levine, H.G. and Blüm, V. (2003). Pigment composition and concentrations within the plant (Ceratophyllum demersum L.) component of the STS-89 C.E.B.A.S. Mini-Module spaceflight experiment. Adv. Space Res. 31(1), 211–214.
Darnell, R.D., Levine, L.H., Bisbee, P.A., Allen, J. and Musgrave, M.E. (2007). Glucosinolate production in hypergravity in Brassica rapa. Gravit. Space Biol. 21, 33.
Levinskikh, M.A., Sytchev, V.N., Podolsky, I.G. and Bingham, G.E. (2001). Pioneering space experiments aimed at obtaining plant biomass to supplement crew food rations. Gravit. Space Biol. Bull. 15(1), 53.
O’Hare, T.J., Wong, L.S. and Force, L.E. (2007). Glucosinolate composition and anti-cancer potential of seed-sprouts from horticultural members of the Brassicaceae. In: Proceedings of the First International Symposium on Human Health Effects of Fruits and Vegetables (Desjardins, Y., ed.) ISHS Acta Horticulturae, Belgium, 744, 181–187.
Porterfield, D.M. (2002). The biophysical limitations in physiological transport and exchange in plants grown in microgravity. J. Plant Growth Regul. 21, 177–190.
Stutte, G.W., Monje, O., Goins, G.C. and Tripathy, B.C. (2005). Microgravity effects on thylakoid, single leaf, and whole canopy photosynthesis of dwarf wheat. Planta 223, 46–56.
Musgrave, M.E., Kuang, A., Xiao, Y., Stout, S.C., Bingham, G.E., Briarty, L.G., Levinskikh, M.A., Sychev, V.N. and Podolski, I.G. (2000). Gravity independence of seed-to-seed cycling in Brassica rapa. Planta 210, 400–406.
Bryant, J.P., Chapin, F.S. III and Klein, D.R. (1983). Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368.
Lambers, H. (1993). Rising CO2, secondary plant metabolism, plant–herbivore interactions and litter decomposition. Theore-tical considerations. Vegetation 104/105, 263–271.
Penuelas, J. and Estiarte, M. (1998). Can elevated CO2 affect secondary metabolism and ecosystem function? Trends Ecol. Evol. 13, 20–24.
Lavola, A. and Julkunen-Tiitto, R. (1994). The effect of elevated carbon dioxide and fertilization on primary and secondary metabolites in birch, Betula pendula (Roth). Oecologia 99, 315–321.
Idso, S.B. and Idso, K.E. (2001). Effects of atmospheric CO2 enrichment on plant constituents related to animal and human health. Environ. Exp. Bot. 45, 179–199.
Tuominen, L.K. and Musgrave, M.E. (2006). Tissue culture in synthetic atmospheres: diffusion rate effects on cytokinin-induced callus growth and isoflavonoid production in soybean (Glycine max (L.) Merr. cv. Acme) Plant Growth Regul. 49, 167–175.
Pan, Z., Wang, H. and Zhong, J. (2000). Scale-up study on suspension cultures of Taxus chinensis cells for production of taxane diterpene. Enzyme Microb. Technol. 27, 714–723.
Schlatmann, J.E., Nuutila, A.M., van Gulik, W.M., ten Hoopen, H.J.G., Verpoorte, R. and Heijnen, J.J. (1993). Scaleup of ajmalicine production by plant cell cultures of Catharanthus roseus. Biotech. Bioeng. 41, 253–262.
Schlatmann, J.E., Moreno, P.R.H., Vinke, J.L., ten Hoopen, H.J.G., Verpoorte, R. and Heijnen, J.J. (1997). Gaseous metabolites and the ajmalicine production rate in high density cell cultures of Catharanthus roseus. Enzyme Microb. Technol. 20, 107–115.
Linden, J.C., Mirjalili, N., Haigh, J.R. and Sun, X. (1995). An examination of dissolved gas effects on growth and secondary metabo-lism of Taxus and Artemisia cell cultures. Abstr. Pap. Am. Chem. Soc. 209, 082.
Tate, J.L. and Payne, G.E. (1991). Plant cell growth under different levels of oxygen and carbon dioxide. Plant Cell Rep. 10, 22–25.
Tisserat, B., Vaughn, S.F. and Silman, R. (2002). Influence of modified oxygen and carbon dioxide atmospheres on mint and thyme plant growth, morphogenesis, and secondary metabolism in vitro. Plant Cell Rep. 20, 912–916.
Nan, R., Carman, J.G. and Salisbury, F.B. (2002). Water stress, CO2 and photoperiod influence hormone levels in wheat. J. Plant Physiol. 159, 307–312.
Campbell, W.F., Salisbury, F.B., Bugbee, B., Klassen, S., Naegle, E., Strickland, D.T., Bingham, G.E., Levinskikh, M., Iljina, G.M., Veselova, T.D., Sytchev, V.N., Podolsky, I., McManus, W.R., Bubenheim, D.L., Stieber, J. and Jahns, G. (2001). Comparative floral development of Mir-grown and ethylene-treated, earth-grown Super Dwarf wheat. J. Plant Physiol. 158, 1051–1060.
Werner, T., Motyka, V., Strnad, M. and Schmülling, T. (2001). Regulation of plant growth by cytokinin. Proc. Natl Acad. Sci. U. S. A. 98, 10487–10492.
Hoson, T., Soga, K., Mori, R., Saiki, M., Nakamura, Y., Wakabayashi, K. and Kamisaka, S. (2002). Stimulation of elongation growth and cell wall loosening in rice coleoptiles under microgravity conditions in space. Plant Cell Physiol. 43, 1067–1071.
Deikman, J. and Hammer, P.E. (1995). Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana. Plant Physiol. 108, 47–57.
Taiz, L. and Zeiger, E. (1998). Plant Physiology, 2nd edn, Sunderland, MA: Sinauer Associates, Inc.
Rudat, A. and Göring, H. (1995). Induction of betacyanin formation in cell cultures of Chenopodium album under UV-light irradiation. J. Exp. Bot. 282, 129–134.
Miller, C.O. (1969). Control of deoxyisoflavone synthesis in soybean tissue. Planta 87, 26–35.
Miller, C.O. (1972). Modification of the cytokinin promotion of deoxyisoflavone synthesis in soybean tissue. Plant Physiol. 49, 310–313.
Imbault, N., Thiersault, M., Dupéron, P., Benabdelmouna, A. and Doireau, P. (1996). Pravastatin: a tool for investigating the availability of mevalonate metabolites for primary and secondary metabolism in Catharanthus roseus cell suspensions. Physiol. Plant. 98, 803–809.
Girod, P. and Zryd, J. (1991). Secondary metabolism in cultured red beet (Beta vulgaris L.) cells: differential regulation of betaxanthin and betacyanin biosynthesis. Plant Cell Tiss. Organ Cult. 25, 1–12.
Vanhala, L., Eeva, M., Lapinjoki, S., Hiltunen, R. and Oksman-Caldentey, K. (1998). Effect of growth regulators on transformed root cultures of Hyoscyamus muticus. J. Plant Physiol. 153, 475–481.
Van der Plas, L.H.W., Eijkelboom, C. and Hagendoorn, M.J.M. (1995). Relation between primary and secondary metabolism in plant cell suspensions: competition between secondary metabolite production and growth in a model system (Morinda citrifolia). Plant Cell Tiss. Organ Cult. 43, 111–116.
Canel, C., Lopes-Cardoso, M.I., Whitmer, S., van der Fits, L., Pasquali, G., van der Heijden, R., Hoge, J.H.C. and Verpoorte, R. (1998). Effects of over-expression of strictosidine synthase and tryptophan decarboxylase on alkaloid production by cell cultures of Catharanthus roseus. Planta 205, 414–419.
Arroo, R.R.J., Develi, A., Meijers, H., Vandewesterlo, E., Kemp, A.K., Croes, A.F. and Wullems, G.J. (1995). Effect of exogenous auxin on root morphology and secondary metabolism in Tagetes patula hairy root cultures. Physiol. Plant. 93, 233–240.
Klaus, D.M. (2004). Gravitational influence on biomolecular engineering processes. Gravit. Space Biol. Bull. 17(2), 51–65.
Higuchi, T. (1997). Biochemistry and molecular biology of wood. Springer, New York, pp 263–290.
Ko, J.H., Han, K.H., Park, S. and Yang, J. (2004). Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole transcriptome profiling. Plant Physiol. 135, 1069–1083.
Braam, J. (1992). Regulated expression of the calmodulin-related TCH genes in cultured Arabidopisis cells: induction by calcium and heat shock. Proc. Natl Acad. Sci. U. S. A. 99, 3213–3216.
Levine, L.H., Heyenga, A.G., Levine, H.G., Choi, J., Davin, L.B., Krikorian, A.D. and Lewis, N.G. (2001). Cell-wall architecture and lignin composition of wheat developed in a microgravity environment. Phytochemistry 57, 835–846.
Cowles, J.R., Scheld, H.W., LeMay, R. and Peterson, C. (1984). Experiments on plants grown in space: growth and lignification in seedlings exposed to eight days of microgravity. Ann. Bot. 54(S3), 33–48.
Tamaoki, D., Karahara, I., Schreiber, L., Wakasugi, T., Yamada, K. and Kamisaka, S. (2006). Effects of hypergravity conditions on elongation growth and lignin formation in the inflorescence stem of Arabidopsis thaliana L. J. Plant Res. 119(2), 79–84.
Wakabayashi, K., Soga, K., Kamisaka, S. and Hoson, T. (2005). Changes in levels of cell wall constituents in wheat seedlings grown under continuous hypergravity conditions. Space life sciences: gravity-related effects on plants and spaceflight and man-made environments on biological systems. Adv. Space Res. 36(7) 1292–1297, Special Issue 2005.
Hoffmann, E., Schonherr, K. and Hampp, R. (1996). Regeneration of plant cell protoplasts under microgravity: investigation of protein patterns by SDS–PAGE and immunoblotting. Plant Cell Rep. 15, 914–919.
Kwon, M., Bedgar, D.L., Piastuch, W., Davin, L.B. and Lewis, N.G. (2001). Induced compression wood formation in Douglas fir (Pseudotsuga menziesii) in microgravity. Phytochemistry 57, 847–857.
Soga, K., Wakabayashi, K., Kamisaka, S. and Hoson, T. (2005). Mechanoreceptors rather than sedimentable amyloplasts perceive the gravity signal in hypergravity-induced inhibition of root growth in azuki bean. Funct. Plant Biol. 32, 175–179.
Nakabayashi, I., Karahara, I., Tamaoki, D., Masuda, K., Wakasugi, T., Yamada, K., Soga, K., Hoson, T. and Kamisaka, S. (2006). Hypergravity stimulus enhances primary xylem development and decreases mechanical properties of secondary cell walls in inflorescence stems of Arabidopsis thaliana. Ann. Bot. 97, 1083–1090.
Allen, J., Kuang, A., Regan, M. and Musgrave, M.E. (2007). Gravity effects on growth form of Brassica rapa L. and Arabidopsis thaliana (L.) Heyhn. Gravit. Space Biol. 21(1), 32.
Soga, K., Wakabayashi, K., Kamisaka, S. and Hoson, T. (2004). Graviperception in growth inhibition of plant shoots under hypergravity condition produced by centrifugation is independent of that in gravitropism and may involve mechanoreceptors. Planta 218, 1054–1061.
Benoit, M.R., Li, W., Stodieck, L.S., Lam, K.S., Winther, C.L., Roane, T.M. and Klaus, D.M. (2006). Microbial antibiotic production aboard the International Space Station. Appl. Microbiol. Biotech. 70, 403–411.
Lam, K.S., Marnber, S.W., Pack, E.J., Forenza, S., Fernandes, P.B. and Klaus, D.M. (1998). The effects of space flight on the production of monorden by Humicola fuscoatra WC5157 in solid-state fermentation. Appl. Microbiol. Biotech. 49, 579–583.
Allen, J., Bisbee, P.A., Darnell, R.L., Kuang, A., Levine, L.H., Musgrave, M.E. and van Loon, J.J.W.A. (2009). Gravity control of growth form in Brassica rapa and Arabidopsis thaliana (Brassicaceae): Consequences for secondary metabolism. Am. J. Bot. 96, in press.
Acknowledgments
This research is supported by NASA grants NAG 10-329 and NNX07AT77G to MEM.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Humana Press, a part of Springer Science+Business Media, LLC
About this protocol
Cite this protocol
Tuominen, L.K., Levine, L.H., Musgrave, M.E. (2009). Plant Secondary Metabolism in Altered Gravity. In: Jain, S.M., Saxena, P.K. (eds) Protocols for In Vitro Cultures and Secondary Metabolite Analysis of Aromatic and Medicinal Plants. Methods in Molecular Biology, vol 547. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60327-287-2_30
Download citation
DOI: https://doi.org/10.1007/978-1-60327-287-2_30
Published:
Publisher Name: Humana Press, Totowa, NJ
Print ISBN: 978-1-60327-286-5
Online ISBN: 978-1-60327-287-2
eBook Packages: Springer Protocols