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Microgravity Effects on Thylakoid, Single Leaf, and Whole Canopy Photosynthesis of Dwarf Wheat

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Microgravity Effects on Thylakoid, Single Leaf, and Whole Canopy Photosynthesis of Dwarf Wheat Planta (2005) 223: 46–56 DOI 10.1007/s00425-005-0066-2 ORIGINAL ARTICLE G. W. Stutte Æ O. Monje Æ G. D. Goins Æ B. C. Tripathy Microgravity effects on thylakoid, single leaf, and whole canopy photosynthesis of dwarf wheat Received: 4 May 2005 / Accepted: 9 June 2005 / Published online: 14 September 2005 Ó Springer-Verlag 2005 Abstract The concept of using higher plants to maintain ground treatments were similar. The reduction in whole a sustainable life support system for humans during chain electron transport (13%), PSII (13%), and PSI long-duration space missions is dependent upon photo- (16%) activities observed under saturating light condi- synthesis. The effects of extended exposure to micro- tions suggests that microgravity-induced responses at gravity on the development and functioning of the canopy level may occur at higher PPF intensity. photosynthesis at the leaf and stand levels were exam- ined onboard the International Space Station (ISS). The Keywords Bioregeneration Æ Bioregenerative Life PESTO (Photosynthesis Experiment Systems Testing Support Æ Photosystem II Æ Photosystem I Æ and Operations) experiment was the first long-term Space Æ Triticum aestivum L replicated test to obtain direct measurements of canopy photosynthesis from space under well-controlled condi- Abbreviations BLSS: Bioregenerative Life Support tions. The PESTO experiment consisted of a series of System Æ BPS: Biomass Production System Æ BRIC: 21–24 day growth cycles of Triticum aestivum L. cv. Biological Research in Canisters Æ USU Apogee onboard ISS. Single leaf measurements CDS: Communication and Data System Æ DAI: Days showed no differences in photosynthetic activity at the After Imbibition Æ ISS: International Space moderate (up to 600 lmol mÀ2 sÀ1) light levels, but Station Æ KSC: Kennedy Space Center Æ LN2: Liquid reductions in whole chain electron transport, PSII, and Nitrogen Æ NASA: National Aeronautics and Space PSI activities were measured under saturating light Association Æ OES: Orbiter Environment Simulator Æ À2 À1 À1 (>2,000 lmol m s )andCO2 (4000 lmol mol ) Pnet: Net Photosynthesis rate Æ PAR: Photosynthetically conditions in the microgravity-grown plants. Canopy Active Radiation Æ PESTO: Photosynthesis Experiment level photosynthetic rates of plants developing in System Testing and Operation Æ PGC: Plant Growth microgravity at 280 lmol mÀ2 sÀ1 were not different Chamber Æ PPF: Photosynthetic Photon Flux Æ PSI: from ground controls. The wheat canopy had appar- Photosystem I Æ PSII: Photosystem II Æ QY: quantum ently adapted to the microgravity environment since the yield Æ STS: Space Transport System Æ WCE: À1 CO2 compensation (121 vs. 118 lmol mol )andPPF Whole Chain Electron transport compensation (85 vs. 81 lmol mÀ2 sÀ1) of the flight and G. W. Stutte (&) Æ O. Monje Introduction Space Life Sciences Laboratory, Dynamac Corporation, Mail Code DYN-3 Kennedy Space Center, FL, 32899 USA Using higher plants as the basis for a biological life E-mail: [email protected] support system (BLSS) that regenerates the atmosphere, Tel.: +1-321-861-3493 purifies water and produces food during long-duration Fax: +1-321-861-2925 space missions has been researched for over 40 years G. D. Goins (Myers 1954; Eley and Myers 1964; Miller and Ward North Caroline AT University, 1966; Halstead and Durcher 1987; Wheeler et al. 2001). Greensboro, NC, USA The photosynthetic rate of higher plants is the critical component of plant-based atmospheric regeneration B. C. Tripathy systems being proposed for long-duration space mis- School of Life Sciences, Jawaharlal Nehru University, sions since it is the fundamental biological process New Delhi, India driving atmospheric regeneration and food production 47 processes (Gitelson and Okladnikov 1994; Wheeler et al. Canopy gas exchange measurements of Triticum 2001). Because of that criticality, it is essential to aestivum L. cv Super Dwarf were made over a 12-day determine the impacts of the microgravity (lg) envi- period during the SVET Greenhouse IIB experiment ronment on the development of the photosynthetic onboard the Orbital Station Mir, but fluctuating envi- apparatus and its functioning in space. It is only through ronmental conditions on Mir and unknown contribu- direct measurement of photosynthesis under adequate tions from respiration of decaying plant material light and controlled CO2 in lg that an informed decision precluded calculations of canopy photosynthesis can be made on the suitability and design of biologically (Monje et al. 2000). In addition, those measurements based subsystems for use in a BLSS. lacked a high-fidelity ground control from which to The limited direct information on photosynthesis make comparisons of gas exchange rates. from spaceflight experiments suggests that lg has neg- Post-flight analysis of wheat cv. Super Dwarf germi- ative effects on the development of the photosynthetic nated on Earth and grown for 14 days during STS-63 by apparatus and the efficiency of photosynthesis of Tripathy et al. (1996) indicated a 27% reduction in developing tissue (Brown et al. 1996). This conclusion wheat cv. Super Dwarf leaf disc O2 evolution rates at significantly impacts the feasibility of using higher plants saturating light and CO2 conditions. This result was for atmospheric regeneration under lg conditions consistent with the 25% reduction in fresh weight of the (Wheeler et al. 2001; Drysdale et al. 2003) since the total space-grown plants observed in that study. Microgravity mass and volume of a BLSS would have to be increased apparently increased leaf respiration rates and disrupted by an appropriate factor to meet the minimum crew electron transport through PSI and PSII (Tripathy et al. requirements for a long-duration mission. The associ- 1996) in these studies with whole chain electron (WCE) ated increase in size, mass, and cost ultimately, has far transport being reduced 28%. It is important to note reaching implications in the overall design and feasibility that plants used in these experiments were grown under of a BLSS. However, none of the data on photosynthetic low light (50–60 lmol mÀ2 sÀ1 PPF), not much greater rates in lg being used to make these assessments, either than the light compensation point (10–20 lmol mÀ2 sÀ1 direct or indirect, has been obtained in the relevant PPF) and the electron transport rates were subsequently environmental conditions (moderate light levels, ele- monitored at saturating light intensities À2 À1 vated CO2, temperature, and RH control) anticipated (2,000 lmol m s PPF). Similarly, Jiao (1999) ob- for growing plants on long-duration missions (Goins served a 30% decrease in PSI electron transport rate in et al. 2003). Brassica rapa cotyledons that had been exposed to Although NASA’s interest in plant biology is over 40- 14 day of lg during STS-87. Jiao (1999) also reported a years-old and extensive research has been conducted to 16–35% reduction in the abundance of PSII proteins in understand the basic physiological responses of plants in the flight leaf tissue. As with Tripathy (1996), these space, there is a paucity of information on photosyn- cotyledons were grown at relatively low light levels (50– thesis per se. Long-term experiments to determine bio- 60 lmol mÀ2 sÀ1 PPF) and the PSI and II was then logical adaptations of higher plants are not possible with characterized at saturating light conditions. The plant drop towers (1–2 s lg), parabolic flights (20–35 s lg)or growth chambers used in both these experiments pro- space shuttle (5–16 day lg) experiments. In addition, vided limited environmental control, and the plants were limited power for supplying adequate levels of photo- exposed to high relative humidity (RH) (85–100%), synthetic photon flux (PPF), coupled with a lack of on- fluctuating temperature (23–28°C), and fluctuating CO2 orbit instrumentation for measuring photosynthesis (1,500 to 8,000 lmol molÀ1) conditions, making differ- during spaceflight experiments, has hindered our ability entiation of effects between lg and environmental stress to obtain real-time, non-destructive data. As a result, difficult. most of the information on photosynthetic responses of Photosynthetic measurements of clinorotated plants plants in lg has been derived from post-flight analysis of (i.e., altered gravity conditions) also suggested an effect tissue upon landing or from clinostat experiments of gravity on photosynthesis. Brown et al. (1996) re- (Brown et al. 1995; Tripathy et al. 1996; Jiao 1999). ported that Pisum sativum grown on a horizontal The first attempt to measure photosynthesis directly clinostat had greater CO2 assimilation rates than verti- in space was conducted on algae flown on the OV1–4 cally rotated or stationary control plants, and no Satellite in 1966 (Ward et al. 1970). No differences in apparent differences in respiration rate between the photosynthesis or respiration between ground controls treatments were observed. In contrast, horizontal rota- and space-grown Chlorella sorokiniana or Spirodella tion had no effect on photosynthesis of maize plants, but polyrhiza were found, but technical issues during the resulted in a decrease in respiration rate. These results experiment made the interpretation complex (Halstead are in partial agreement with the findings of Ward and and Dulcher 1987). During STS-73, a 16-day space- King (1978), who found both increased photosynthetic flight experiment using Solanum tuberosum leaf and respiratory gas exchange rates in horizontally ro- explants, photosynthesis and respiration were observed tated
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