, Volume 224, Issue 5, pp 1038–1049 | Cite as

Microgravity effects on leaf morphology, cell structure, carbon metabolism and mRNA expression of dwarf wheat

  • G. W. Stutte
  • O. Monje
  • R. D. Hatfield
  • A. -L. Paul
  • R. J. Ferl
  • C. G. Simone
Original Article


The use of higher plants as the basis for a biological life support system that regenerates the atmosphere, purifies water, and produces food has been proposed for long duration space missions. The objective of these experiments was to determine what effects microgravity (μg) had on chloroplast development, carbohydrate metabolism and gene expression in developing leaves of Triticum aestivum L. cv. USU Apogee. Gravity naive wheat plants were sampled from a series of seven 21-day experiments conducted during Increment IV of the International Space Station. These samples were fixed in either 3% glutaraldehyde or RNAlater or frozen at −25°C for subsequent analysis. In addition, leaf samples were collected from 24- and 14-day-old plants during the mission that were returned to Earth for analysis. Plants grown under identical light, temperature, relative humidity, photoperiod, CO2, and planting density were used as ground controls. At the morphological level, there was little difference in the development of cells of wheat under μg conditions. Leaves developed in μg have thinner cross-sectional area than the 1 g grown plants. Ultrastructurally, the chloroplasts of μg grown plants were more ovoid than those developed at 1 g, and the thylakoid membranes had a trend to greater packing density. No differences were observed in the starch, soluble sugar, or lignin content of the leaves grown in μg or 1 g conditions. Furthermore, no differences in gene expression were detected leaf samples collected at μg from 24-day-old leaves, suggesting that the spaceflight environment had minimal impact on wheat metabolism.


Bioregeneration Bioregenerative life support Lignin Carbohydrate metabolism Microarray Triticum aestivum L. 



Bioregenerative life support system


Biomass production system


Biological Research in Canisters


Communication and data system


Days after imbibition


International Space Station


Kennedy Space Center


Liquid nitrogen


National Aeronautics and Space Association


Orbiter environment simulator


Net photosynthesis rate


Photosynthetically active radiation


Photosynthesis experiment system testing and operation


Plant growth chamber


Photosynthetic photon flux


Photosystem I


Photosystem II


Quantum yield


Space transport system


Whole chain electron transport



This research was funded in whole or in part by a grant from the Office of Biological and Physical Research of the National Aeronautics and Space Administration. The authors gratefully acknowledge support of Sylvia Anderson for data collection and summarization, F. Bennett, Electron Microscopy Core Facility, University of Florida, Gainesville for preparation of electron micrographs, M. Giroux, Montana State University, Bozeman MT for wheat microarrays, D. Laudencia-Chingcuanco, USDA, Albany, CA for hybridization of microarray chips, M. Popp, Molecular Biology Core Facility, University of Florida, Gainesville, for analysis of gene expression data, N. Chatterdon, USDA-ARS, Logan, UT for soluble sugar analysis. The authors acknowledge the support of personnel at Orbitec (Madison, WI), Ames Research Center, Moffett Field, CA, Kennedy Space Center, FL, Johnson Space Center, TX, and Marshall Space Flight Center, Huntsville, AL. Finally, the authors wish to express their gratitude to ISS Increment IV Flight Engineer Dan Bursch for his commitment to microgravity research.

Supplementary material

425_2006_290_MOESM1_ESM.pdf (967 kb)
Supplementary material


  1. Adamchuk NI, Mikaylenko NF, Zolotareva EK, Hilaire E, Guikema JA (1999) Spaceflight effects on structural and some biochemical parameters of Brassica rapa photosynthetic apparatus. J Gravitat Physiol 6:95–96Google Scholar
  2. Aliyev AA, Abilov ZK, Mahinksy AL, Ganiyeva RA, Ragimova GK (1987) The ultrastructure and physiological characteristics of the photosynthesis system of shoots of garden pea grown for 29 days on the “Salyut-7” space station. USSR Space Life Sci Digest 10:15–16Google Scholar
  3. Blakeney AB, Harris PJ, Henery RJ, Stone BA (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr Res 113:291–299CrossRefGoogle Scholar
  4. Brown CS, Tibbitts TW, Croxdale JG, Wheeler RM (1997) Potato tuber formation in the spaceflight environment. Life Support Biosph Sci 4:71–76PubMedGoogle Scholar
  5. Brown CS, Tripathy BC, Stutte GW (1996) Photosynthesis and carbohydrate metabolism in microgravity. In: Suge H (ed) Plants in space biology. Institute of Ecology, pp 127–134Google Scholar
  6. Brown CS, Piastuch WC (1994) Starch metabolism in germinating soybean cotyledons is sensitive to clinorotation and centrifugation. Plant Cell Environ 17:341–344PubMedCrossRefGoogle Scholar
  7. Bugbee B, Koerner G (1997) Yield comparisons and unique characteristics of the dwarf wheat cultivar “USU-Apogee”. Adv Space Res 20:1891–1894PubMedCrossRefGoogle Scholar
  8. Cook ME, Croxdale JM (2003) Ultrastructure of potato tubers formed in microgravity under controlled environmental conditions. J Exp Bot 54:2157–2164PubMedCrossRefGoogle Scholar
  9. Cowles JR, Scheld HW, LeMay R, Peterson C (1984) Experiments on plants grown in space: growth and lignification in seedlings exposed to eight days of microgravity. Ann bot [Supple 3] 54:33–48Google Scholar
  10. Croxdale JM, Cook ME, Tibbitts TW, Brown CS, Wheeler RM (1997) Structure of potato tubers formed during spaceflight. J Exp Bot 48:2037–2043PubMedGoogle Scholar
  11. Eley JH, Myers J (1964) Study of a photosynthetic gas exchanger: a quantitative repetition of the Priestley experiment. Tex J Sci 16:296–333Google Scholar
  12. Fukushima RS, Hatfield RD (2001) Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. J Agric Food Chem 49:3133–3139PubMedCrossRefGoogle Scholar
  13. Fukushima RS, Hatfield RD (2004) Comparison of the acetyl bromide spectrophotmeteric method with other lignin methods for determining lignin concentration in forage samples. J Agric Food Chem 52:3713–3720PubMedCrossRefGoogle Scholar
  14. Halstead TW, Dutcher FR (1987) Plants in space. Ann Rev Plant Phys 38:317–345CrossRefGoogle Scholar
  15. Hatfield R, Fukushima RS (2005) Can lignin be accurately measured? Crop Sci 45:832–839CrossRefGoogle Scholar
  16. Hegde P, Rong Q, Abernathy K, Gay C, Dharap S, Gaspard R, Earle-Huges J, Snesrud E, Lee N, Quackenbush J (2000) A concise guide to cDNA microarray analysis-II. Biotechniques 29:548–562PubMedGoogle Scholar
  17. Hoson T, Soga K, Mori R, Asiki M, Nakamura Y, Wakabayashi K, Kamisaka S (2002) Stimulation of elongation growth and cell wall loosening in rice coleoptiles under microgravity conditions in space. Plant Cell Physiol 43:1067–1071PubMedCrossRefGoogle Scholar
  18. Hoson T, Soga K, Wakabayashi K, Kamisaka S, Tanimoto E (2003) Growth and cell wall changes in rice roots during spaceflight. Plant Soil 255:19–26PubMedCrossRefGoogle Scholar
  19. Iverson JT, Crabb TM, Morrow RC, Lee MC (2003) Biomass production system hardware performance. SAE Technical Paper 2003-01-2484Google Scholar
  20. Jiao S, Hilaire E, Paulsen AQ, Guikema JA (1999) Ultrastructural observation of chloroplast morphology in space-grown Brassica rapa cotyledons. J Grav Physiol 6:93–94Google Scholar
  21. Kimbrough JM, Salinas-Mondragon R, Boss WF, Brown CS, Sederoff HW (2004) The fast and transient transcriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol 136:2790–2805PubMedCrossRefGoogle Scholar
  22. Kordyum EL, Nedukha EM, Sytnik KM, Mashinsky AL (1981) Optical and electron-microscopic studies of the Funaria hygrometrica protonema after cultivation for 96 days in space. Adv Space Res 1:159–162PubMedCrossRefGoogle Scholar
  23. Kraft TFB, van Loon JJWA, Kiss JZ (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211:415–422PubMedCrossRefGoogle Scholar
  24. Kuang A, Xiao Y, Musgrave ME (1996) Cytochemical localization of reserves during seed development in Arabidopsis thaliana under spaceflight conditions. Ann Bot 78:343–351PubMedCrossRefGoogle Scholar
  25. Levine LL, Heyenga AG, Levine HG, Choi J-W, Davin LB, Krikorian AD, Lewis NG (2001) Cell-wall architecture and lignin composition of wheat developed in a micro gravity environment. Phytochemistry 57:835–846PubMedCrossRefGoogle Scholar
  26. Liu F, VanToai T, Moy LP, Bock G, Linfor LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129PubMedCrossRefGoogle Scholar
  27. Miller RL, Ward CH (1966) Algal bioregenerative sytems. In: Kammermeyer E (ed) Atmosphere in space cabins and closed environments. Appleton-Century-Croft Pub, New YorkGoogle Scholar
  28. Moseyko N, Zhu T, Chang H-S, Wang X, Feldman LJ (2002) Transcription profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol 130:720–728PubMedCrossRefGoogle Scholar
  29. Merkys AJ, Laurinavičius RS, Jarosius AV, Rupainiene OJ (1987) Growth, development, anatomy and morphological structure of Arabidopsis thaliana (l.) Heynh. under spaceflight conditions. Institute of Botany, Academy of Science of the Lithuanian SSR, Vilnius, pp 105–116Google Scholar
  30. Monje O, Bugbee B (1998) Adaptation to high CO2 concentration in an optimal environment: radiation capture, canopy quantum yield and carbon use efficiency. Plant Cell Environ 21:315–324PubMedCrossRefGoogle Scholar
  31. Monje O, Stutte GW, Goins GD, Porterfield DM, Bingham GE (2003) Farming in space: environmental and biophysical concerns. Adv Space Res 31:151–167PubMedCrossRefGoogle Scholar
  32. Monje O, Stutte GW, Chapman D (2005) Microgravity does not alter plant stand gas exchange of wheat at moderate light levels and saturating CO2 concentration. Planta 222:336–345PubMedCrossRefGoogle Scholar
  33. Monje O, Wang HT, Kelly C, Stutte GW (2001) Nutrient delivery system water pressures affect growth rate by changes in leaf area, not single leaf photosynthesis. SAE Technical Paper 2001-02-2207Google Scholar
  34. Moore R, Fondren WM, McClelen CE, Wang C-L (1987) Influence of microgravity on cellular differentiation in root caps of Zea mays. Am J Bot 74:1006–1007PubMedCrossRefGoogle Scholar
  35. Morrow RC, Crabb TM (2000) Biomass production system (BPS) plant growth unit. Adv Space Res 26:289–298PubMedCrossRefGoogle Scholar
  36. Musgrave ME, Kuang A, Matthews SW (1997) Plant reproduction during spaceflight: importance of the gaseous environment. Planta 203:S177–184PubMedCrossRefGoogle Scholar
  37. Musgrave ME, Kuang A, Brown CS, Matthews S (1998) Changes in Arabidopsis leaf ultrastructure, chlorophyll content and carbohydrate content during spaceflight depend on ventilation. Ann Bot 81:503–512PubMedCrossRefGoogle Scholar
  38. Myers J (1954) Basic remarks on the use of plants as biological gas exchanges in a closed system. J Aviat Med 35:507–411Google Scholar
  39. Nechitailo GS, Mashinsky AL (1993) Space biology: studies at orbital stations. Mir Publishers, MoscowGoogle Scholar
  40. Nedukha EM (1996) Possible mechanisms of plant cell wall changes at microgravity. Adv Space Res 1:109–111Google Scholar
  41. Nedukha OM (1997) Effects of weightlessness on photosynthesizing cells structure of plants. J Gravit Physiol 4:79–80Google Scholar
  42. Paul A-L, Daugherty CJ, Bihn EA, Chapman DK, Norwood KLL, Ferl RJ (2001) Transgene expression patterns indicates that spaceflight affects stress signal perception and transduction in Arabidopsis. Plant Physiol 126:613–621PubMedCrossRefGoogle Scholar
  43. Paul A-L, Levine HG, McLamb W, Norwood KL, Reed D, Stutte GW, Wells HW, Ferl RJ (2005a) Plant molecular biology in the space station ere: utilization of KSC fixation tubes with RNALater. Acta Astronaut 56:623–628CrossRefGoogle Scholar
  44. Paul A-L, Popp MP, Gurley WB, Guy C, Norwood KL, Ferl RJ (2005b) Arabidopsis gene expression patterns are altered during spaceflight. Adv Space Res 36:1175–1181CrossRefGoogle Scholar
  45. Paul A-L, Schuerger AC, Popp M, Richards JT, Manak M, Ferl RJ (2004) Arabidopsis gene expression at low atmospheric pressure—hypobaria does not equal hypoxia. Plant Physiol 134:215–223PubMedCrossRefGoogle Scholar
  46. Porterfield DM (2002) The biophysical limitations in physiological transport and exchange in plants grown in microgravity. J Plant Growth Regul 21:177–190PubMedCrossRefGoogle Scholar
  47. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2002) Stimulation of elongation growth and xyloglucan breakdown in Arabidopsis hypocotyls under microgravity conditions in space. Planta 215:1040–1046PubMedCrossRefGoogle Scholar
  48. Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43PubMedCrossRefGoogle Scholar
  49. Stryjewski E, Peterson BV, Stutte GW (2000) Long term storage of what plants for light microscopy. SAE technical paper 200-01-2231Google Scholar
  50. Stutte GW, Yorio NC, Wheeler GW (1996) Interacting effects of photoperiod and photosynthetic photon flux on net carbon assimilation and starch accumulation in potato leaves. J Am Soc Hortic Sci 121:264–268PubMedGoogle Scholar
  51. Stutte GW, Monje O, Goins GD, Chapman DK (2000) Measurement of gas exchange characteristics of developing wheat in the biomass production chamber. SAE technical paper 2001-01-424Google Scholar
  52. Stutte GW, Monje O, Goins G, Ruffe L (2001) Evapotranspiration and photosynthesis characteristics of two wheat cultivars grown in the biomass production system. SAE technical paper 2001-01-2180Google Scholar
  53. Stutte GW, Monje O, Anderson S (2003) Wheat growth on board the international space station: germination and early development. Proc Plant Growth Regul Soc Am 30:66–71Google Scholar
  54. Stutte GW, Monje O, Goins GD, Tripathy BC (2005) Microgravity effects on thylakoid, single leaf, and whole canopy photosynthesis of dwarf wheat 2005. Planta 223:46–56PubMedCrossRefGoogle Scholar
  55. Sytnik KM, Popova AF, Nichitailo GS, Machinsky AL (1992) Peculiarities of the submicroscopic organization of Chlorella cells cultivated on a solid medium in microgravity. Adv Space Res 12:103–106PubMedCrossRefGoogle Scholar
  56. Tairbekov MG, Parfyonov GP, Platonova RW, Aramova VM, Golov VK, Rostopshina AV, Lyubchenko VYU, Chuchkin VG (1981) Biological Investigations aboard the biosatellite Cosmos-1129. Adv Space Res 1:89–94PubMedCrossRefGoogle Scholar
  57. Tripathy BC, Brown CS, Levine HG, Krikorian AD (1996) Growth and photosynthetic responses of wheat plants grown in space. Plant Physiol 110:801–806PubMedCrossRefGoogle Scholar
  58. Ward CH, King JM (1978) Effects of simulated hypogravity on respiration and photosynthesis of higher plants. In: Holmquist R (eds) Life sciences and space research. Pergamon, Oxford, pp 291–296Google Scholar
  59. Ward CH, Wilks SS, Craft HL (1970) Effects of prolonged near weightlessness on growth and gas exchange of photosynthetic plants. Dev Ind Microbiol 11:276–295Google Scholar
  60. Wells HW (1999) Portable device for chemical fixation of a biological sample. NasaTech Briefs, July; KSC-11993Google Scholar
  61. Wheeler RM, Mackowiak CL, Yorio NC, Sager JC (1999) Effects of CO2 on stomatal conductance: do stomata open at very high CO2 concentrations. Ann Bot 83:243–251PubMedCrossRefGoogle Scholar
  62. Wheeler RM, Stutte GW, Subbarao GV, Yorio NC (2001) Plant growth and human life support for space travel. In: Passarakli M (eds) Handbook of plant and crop physiology, 2nd edn. Marcel Dekker Inc, New York, pp 925–941Google Scholar
  63. Wheeler RM, Sager JC, Prince RP, Knott WM, Mackowiak CL, Yorio NC, Ruffe LM, Peterson BV, Gins GD, Hinkle CR, Berry WL (2003) Crop production for life support systems. NASA TM-20032-11184Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • G. W. Stutte
    • 1
  • O. Monje
    • 1
  • R. D. Hatfield
    • 2
  • A. -L. Paul
    • 3
  • R. J. Ferl
    • 3
  • C. G. Simone
    • 4
  1. 1.Space Life Sciences Laboratory, Dynamac Corporation, Mail Code Dyn-3Kennedy Space CenterKennedyUSA
  2. 2.US Dairy Forage Research CenterUSDA-Agricultural Research ServiceMadisonUSA
  3. 3.Department of Horticultural SciencesUniversity of FloridaGainesvilleUSA
  4. 4.Department of BiologyUniversity of South FloridaTampaUSA

Personalised recommendations