Skip to main content

Advertisement

Log in

Hypobaria and hypoxia affects phytochemical production, gas exchange, and growth of lettuce

  • Published:
Photosynthetica

Abstract

Hypobaria (low total atmospheric pressure) is essential in sustainable, energy-efficient plant production systems for long-term space exploration and human habitation on the Moon and Mars. There are also critical engineering, safety, and materials handling advantages of growing plants under hypobaria, including reduced atmospheric leakage from extraterrestrial base environments. The potential for producing crops under hypobaria and manipulating hypoxia (low oxygen stress) to increase health-promoting bioactive compounds is not well characterized. Here we showed that hypobaric-grown lettuce plants (25 kPa ≈ 25% of normal pressure) exposed to hypoxia (6 kPa pO2 ≈ 29% of normal pO2) during the final 3 d of the production cycle had enhanced antioxidant activity, increased synthesis of anthocyananins, phenolics, and carotenoids without reduction of photosynthesis or plant biomass. Net photosynthetic rate (P N) was not affected by total pressure. However, 10 d of hypoxia reduced P N, dark respiration rate (R D), P N/R D ratio, and plant biomass. Growing plants under hypobaria and manipulating hypoxia during crop production to enhance health-promoting bioactive compounds is important for the health and well-being of astronauts exposed to space radiation and other stresses during long-term habitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

CA :

CO2 assimilation

Car:

carotenoids

Chl:

chlorophyll

DPR:

dark-period respiration

FL:

fluorescein

LPPG:

low pressure plant growth system

ORAC:

antioxidant activity

P N :

net photosynthetic rate

P N/R D ratio:

net photosynthesis/dark respiration rate ratio

pO2 :

partial pressure of O2

R D :

dark respiration rate

ROS:

reactive oxygen species

TP:

total soluble phenolics

References

  • Beckwith, A.G., Zhang, Y., Seeram, N.P. et al.: Relationship of light quantity and anthocyanin production in Pennisetum setaceum (cvs Rubrum and Red Riding Hood). — J. Agr. Food Chem. 52: 456–461, 2004.

    Article  CAS  Google Scholar 

  • Bucklin, R.A., Fowler, P.A., Rygalov, V.Y. et al.: Greenhouse design for the Mars environment: Development of a prototype deployable dome. — Acta Hort. 659: 127–134, 2004.

    Google Scholar 

  • Burg, S.P.: Postharvest Physiology and Hypobaric Storage of Fresh Produce. — CAB International, Wallingford, Oxfordshire 2004.

    Book  Google Scholar 

  • Campbell, W.F., Salisbury, F.B., Bugbee, B. et al.: Comparative floral development of Mir-grown and ethylene-treated earth-grown Super Dwarf wheat. — J. Plant Physiol. 158:1051–1060, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Cisneros-Zevallos, L.: The use of controlled post-harvest abiotic stresses as a tool for enhancing the nutraceutical content and adding-value to fresh fruits and vegetables. — J. Food Sci. 68: 1560–1565, 2003.

    Article  CAS  Google Scholar 

  • Davies, F.T., Calderon, C.M., Huaman, Z., Gomez, R.: Influence of a flavonoid (formononetin) on mycorrhizal activity and potato crop productivity in the highlands of Peru. — Sci. Hort. 106: 318–329, 2005.

    Article  CAS  Google Scholar 

  • Dixon, R.A., Paiva, N.L.: Stress-induced phenylpropanoid metabolism. — Plant Cell 7: 1085–1097, 1995.

    CAS  PubMed  Google Scholar 

  • Drew, M.C.: Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 223–250, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Dumas, Y., Dadomo, M., Lucca, G.D., Groller, P.: Effects of environmental factors and agricultural techniques on antioxidant content of tomatoes. — J. Sci. Food Agr. 83: 369–382, 2003.

    Article  CAS  Google Scholar 

  • Fukao, F., Bailey-Serrer, J.: Plant response to hypoxia — is survival a balancing act? — Trends Plant Sci. 9: 449–456, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Fuleki, T., Francis, F. J.: Quantitative methods for anthocyanins. 1. Extraction and determinationm of total anthocyanin in cranberries. — J. Food Sci. 33: 72–77, 1968.

    Article  CAS  Google Scholar 

  • Gale, J.: Availability of carbon dioxide for photosynthesis at high altitudes: theoretical considerations. — Ecology 53: 494–497, 1972.

    Article  Google Scholar 

  • He, C., Davies, F.T.: Ethylene reduces plant gas exchange and growth of lettuce grown from seed to harvest under hypobaric and ambient total pressure. — J. Plant Physiol. 169: 369–378, 2012.

    Article  CAS  PubMed  Google Scholar 

  • He, C., Davies, F.T., Lacey, R.E. et al.: Effect of hypobaric conditions on ethylene evolution and growth of lettuce and wheat. — J. Plant Physiol. 160: 1341–1350, 2003.

    Article  CAS  PubMed  Google Scholar 

  • He, C., Davies, F.T., Lacey, R.E.: Hypobaric conditions effect gas exchange, ethylene evolution and growth of lettuce for advanced life support systems (ALS). — Habitation 11: 49–61, 2006.

    Article  Google Scholar 

  • He, C., Davies, F.T., Lacey, R.E.: Separating the effects of hypobaria and hypoxia on lettuce: growth and gas exchange. — Physiol. Plant. 131: 226–240, 2007.

    CAS  PubMed  Google Scholar 

  • He, C., Davies, F.T., Lacey, R.E.: Ethylene reduces gas exchange and growth of lettuce plants under hypobaric and normal atmospheric conditions. — Physiol. Plant. 135: 258–271, 2009a.

    Article  CAS  PubMed  Google Scholar 

  • He, C., Davies, F.T., Lacey, R.E.: Hypobaria, hypoxia and light affect gas exchange, and the CO2 compensation and saturation points of lettuce (Lactuca sativa) L. — Botany 87: 712–721, 2009b.

    Article  CAS  Google Scholar 

  • Kubota, C., Thomson, C.A., Wu, M., Javanmardi, J.: Controlled environments for production of value-added food crops with high phytochemical concentrations: lycopene in tomato as an example. — HortScience 41: 522–525, 2006.

    CAS  Google Scholar 

  • Levine, L.H., Bisbee, P.A., Richards, J.T. et al.: Quality characteristics of the radish grown under reduced atmospheric pressure. — Adv. Space Res. 41: 754–762, 2008.

    Article  Google Scholar 

  • Lichtenthaler, H.K, Buschmann, C.: Extraction of photosynthetic tissues: Chlorophylls and carotenoids. — In: Wrolstad, R.E., Acree, T.E., Decker, E.A. et al. (ed.): Handbook of Food Analytical Chemistry, Current Protocols in Food Analytical Chemistry. Pp. 165–170. John Wiley &Sons, Madison 2001.

    Google Scholar 

  • Musgrave, M.E., Gerth, W.A., Scheid, H.W., Strain, B.R.: Growth and mitochondrial respiration of mungbeans (Phaseolus aureus Roxb.) germinated at low pressure. — Plant. Physiol. 86: 19–22, 1988.

    Article  CAS  PubMed  Google Scholar 

  • Paul, A.L., Ferl, R.F.: The biology of low atmospheric pressure — implications for exploration mission design and advanced life support. — Gravit. Space Biol. Bull. 19: 3–18, 2006.

    Google Scholar 

  • Paul, A.L., Schuerger, A.C., Popp, M.P., Richards, J.T., Manak M.S., Ferl R.I.: Hypobaric biology: Arabidopsis gene expression at low atmospheric pressure. — Plant Physiol. 134: 215–223, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Rajapakse, N.C., He, C., Cisneros-Zevallos, L., Davies, F.T.: Hypobaria and hypoxia affects growth and phytochemical contents of lettuce. — Sci. Hort. 122: 171–178, 2009.

    Article  CAS  Google Scholar 

  • Richards, J.T., Corey, K.A., Paul, A.L. et al.: Exposure of Arabidopsis thaliana to hypobaric environments: implications for low-pressure bioregenerative life support systems for human exploration missions and terraforming on Mars. — Astrobiology 6: 851–866, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Rygalov, V.Y., Fowler, P.A., Wheeler, R.M., Bucklin, R.A.: Water cycle and its management for plant habitats at reduced pressures. — Habitation 10: 49–59, 2004.

    Article  PubMed  Google Scholar 

  • Schwartzkopf, S.H., Mancinelli, R.L.: Germination and growth of wheat in simulated Martian atmospheres. — Acta Astronaut. 25: 245–247, 1991.

    Article  CAS  PubMed  Google Scholar 

  • Smith, B.N., Lytle, E.M., Hansen, L.D.: Predicting plant growth rates from dark respiration rates: an experimental approach. — In: Roundy, B.A., McArthur, E.D., Haley, J.S. et al. (ed.): Proceedings: Wildland Shrub and Arid Land Restoration Symposium. Oct 19–21, 1993, Las Vegas, Nevada. Gen Tech Rep. INT-GTR-315. USDA For. Serv., Intermountain Research Station, Ogden, Utah, US. Pp.243–245, 1995.

    Google Scholar 

  • Swain, T., Hillis, W.E.: The phenolics constituents of Prunus domestica. I. The quantitative analysis of phenolics constituents. — J. Sci. Food Agr. 10: 63–68, 1959.

    Article  CAS  Google Scholar 

  • Villarreal-Lozoya, J.E., Lombardini, L., Cisneros-Zevallos, L.: Phytochemical constituents and antioxidant capacity of different pecan [Carya illinoinensis (Wangenh.) K. Koch] cultivars. — Food Chem. 102: 1241–1249, 2007.

    Article  CAS  Google Scholar 

  • Wargovich, M.J.: Anticancer properties of fruits and vegetables. — HortScience 35: 573–575, 2000.

    CAS  Google Scholar 

  • Wheeler, R.M.: Roadmaps and Strategies for Crop Research for Bioregenerative Life Support Systems: A Compilation of Findings from NASA’s Advanced Life Support Meetings. NASA Kennedy Space Center Biological Sciences Office. NASA/TM — 2009-214768, 2009.

    Google Scholar 

  • Wheeler, R.M., Mackowiak, C.L., Sager, J.C., Yorio, N.C., Knott, W.M.: Growth and gas exchange by lettuce stands in a closed, controlled environment. — J. Amer. Soc. Hort. Sci. 119: 610–615, 1994.

    CAS  Google Scholar 

  • Wu, X., Beecher, G.R., Holden, J.M. et al.: Lipophilic and hydrophilic antioxidant capacities of common foods in the United States. — J. Agr. Food. Chem. 52: 4026–4037, 2004.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. T. Davies.

Additional information

Acknowledgements: We thank Tom Boutton, Ray Wheeler, and Mark Tjoelker for critical review of the manuscript. Supported in part by the National Aeronautics and Space Administration (NASA) through grants No. NAG-9-1067 (Plant Growth and Metabolism at Sub-Ambient Atmospheric Pressures), and No. NAJ04HF31G (Plant Growth at Sub-Ambient Atmospheric Pressures with Control of the Partial Pressures of Constituent Gases), and the Texas AgriLife Research.

Rights and permissions

Reprints and permissions

About this article

Cite this article

He, C., Jacobo-Velázquez, D.A., Cisneros-Zevallos, L. et al. Hypobaria and hypoxia affects phytochemical production, gas exchange, and growth of lettuce. Photosynthetica 51, 465–473 (2013). https://doi.org/10.1007/s11099-013-0047-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-013-0047-9

Additional key words

Navigation