USDA ARS

Molecular biochemical basis for environmental effects on photosynthesis and photosynthetic energy transduction

The Ort Lab

Recent Publications:

Ort DR, Long SP (2014) Limits on Yields in the Corn Belt, Science 344, pp. 484

Slattery, RA, Ainsworth, EA, Ort, DR (2013)A meta-analysis of responses of canopy photosynthetic conversion efficiency to environmental factors reveals major causes of yield gap Journal of Experimental Botany 64 (12), pp. 3723-3733

Locke, AM, Sack, L, Bernacchi, CJ, Ort, DR (2013) Soybean leaf hydraulic conductance does not acclimate to growth at elevated [CO2] or temperature in growth chambers or in the field Annals of Botany 112 (5), pp. 911-918

Zhu, X-G, Wang, Y, Ort, DR, Long, SP (2013) e-photosynthesis: A comprehensive dynamic mechanistic model of C3 photosynthesis: From light capture to sucrose synthesis. Plant, Cell and Environment 36 (9), pp. 1711-1727

Borak, B, Ort, DR, Burbaum, JJ (2013) Energy and carbon accounting to compare bioenergy crops. Current Opinion in Biotechnology 24 (3), pp. 369-375

Grennan AK, Ort DR (2011) Measurement of Chloroplast ATP Synthesis Activity in Arabidopsis. Methods in Molecular Biology, 2011, Volume 775, Part 4, 343-355

There are numerous options for monitoring ATP synthesis in chloroplasts using isolated thylakoid membranes, intact chloroplasts, and even whole leaves. Currently, the most commonly used method employs isolated thylakoids coupling the synthesis of ATP to light emission from luciferin in a reaction catalyzed by luciferase. The luciferin-luciferase assay can be highly sensitive and is a direct measure of ATP. Another direct measurement of ATP is the incorporation of 32P into ATP, which, while more technically difficult, has the advantage over the luciferin-luciferase assay of being able to distinguish newly synthesized from total ATP. The phosphorylation of ADP results in a net decrease in pK a (acid disassociation constant) between the reactants and the product ATP, resulting in an increase in the pH of the assay media, which can be used as a convenient, continuous measurement of ATP synthesis. The formation of ΔμH+ across the thylakoid membrane and its concomitant dissipation as ATP is synthesized can be measured by an electrochromic absorption band shift (ECS) of thylakoid pigments measured at 518 nm (Witt, Biochim. Biophys. Acta 505:355-427, 1979; Petty and Jackson, Biochim. Biophys. Acta: Bioenergetics 547:463-473, 1979). The first-order decay time of the ESC can be used to estimate the rate of ATP synthesis providing a noninvasive, indirect method for measuring ATP synthase activity that can be used with intact leaves.

Hatfield JL Boote KJ Kimball BA, Ziska LH, Izaurralde RC, Ort D, Thomson AM, Wolfe D (2011) Climate Impacts on Agriculture: Implications for Crop Production. Agronomy Journal 103: 351-370

Changes in temperature, CO(2), and precipitation under the scenarios of climate change for the next 30 yr present a challenge to crop production. This review focuses on the impact of temperature, CO2, and ozone on agronomic crops and the implications for crop production. Understanding these implications for agricultural crops is critical for developing cropping systems resilient to stresses induced by climate change. There is variation among crops in their response to CO(2), temperature, and precipitation changes and, with the regional differences in predicted climate, a situation is created in which the responses will be further complicated. For example, the temperature effects on soybean [Glycine max (L.) Merr.] could potentially cause yield reductions of 2.4 % in the South but an increase of 1.7 % in the Midwest. The frequency of years when temperatures exceed thresholds for damage during critical growth stages is likely to increase for some crops and regions. The increase in CO(2) contributes significantly to enhanced plant growth and improved water use efficiency (WUE); however, there may be a downscaling of these positive impacts due to higher temperatures plants will experience during their growth cycle. A challenge is to understand the interactions of the changing climatic parameters because of the interactions among temperature, CO(2), and precipitation on plant growth and development and also on the biotic stresses of weeds, insects, and diseases. Agronomists will have to consider the variations in temperature and precipitation as part of the production system if they are to ensure the food security required by an ever increasing population.

Bernacchi CJ, Leakey ADB, Kimball BA, Ort DR (2011) Growth of soybean at future tropospheric ozone concentrations decreases canopy evapotranspiration and soil water depletion. Environmental Pollution 149: 1464-1472

Tropospheric ozone is increasing in many agricultural regions resulting in decreased stomatal conductance and overall biomass of sensitive crop species. These physiological effects of ozone forecast changes in evapotranspiration and thus in the terrestrial hydrological cycle, particularly in intercontinental interiors. Soybean plots were fumigated with ozone to achieve concentrations above ambient levels over five growing seasons in open-air field conditions. Mean season increases in ozone concentrations ([O(3)]) varied between growing seasons from 22 to 37 % above background concentrations. The objective of this experiment was to examine the effects of future [O(3)] on crop ecosystem energy fluxes and water use. Elevated [O(3)] caused decreases in canopy evapotranspiration resulting in decreased water use by as much as 15% in high ozone years and decreased soil water removal. In addition, ozone treatment resulted in increased sensible heat flux in all years indicative of day-time increase in canopy temperature of up to 0.7 degrees C.

Ort DR, Zhu XG, Melis A (2011) Optimizing Antenna Size to Maximize Photosynthetic Efficiency. Plant Physiology, 155: 79-85 (Open Access Article)

Wu X, Oh M-H, Schwarz EM, Larue CT, Sivaguru M, Imai BS, Yau PM, Ort DR, Huber SC (2011) Lysine acetylation is a widespread protein modification for diverse proteins in Arabidopsis. Plant Physiology 155: 1769-1778 (Open Access Article)

Lysine acetylation (LysAc), a form of reversible protein posttranslational modification previously known only for histone regulation in plants, is shown to be widespread in Arabidopsis (Arabidopsis thaliana). Sixty-four Lys modification sites were identified on 57 proteins, which operate in a wide variety of pathways/processes and are located in various cellular compartments. A number of photosynthesis-related proteins are among this group of LysAc proteins, including photosystem II (PSII) subunits, light-harvesting chlorophyll a/b-binding proteins (LHCb), Rubisco large and small subunits, and chloroplastic ATP synthase (beta-subunit). Using two-dimensional native green/sodium dodecyl sulfate gels, the loosely PSII-bound LHCb was separated from the LHCb that is tightly bound to PSII and shown to have substantially higher level of LysAc, implying that LysAc may play a role in distributing the LHCb complexes. Several potential LysAc sites were identified on eukaryotic elongation factor-1A (eEF-1A) by liquid chromatography/mass spectrometry and using sequence- and modification-specific antibodies the acetylation of Lys-227 and Lys-306 was established. Lys-306 is contained within a predicted calmodulin-binding sequence and acetylation of Lys-306 strongly inhibited the interactions of eEF-1A synthetic peptides with calmodulin recombinant proteins in vitro. These results suggest that LysAc of eEF-1A may directly affect regulatory properties and localization of the protein within the cell. Overall, these findings reveal the possibility that reversible LysAc may be an important and previously unknown regulatory mechanism of a large number of nonhistone proteins affecting a wide range of pathways and processes in Arabidopsis and likely in all plants.

Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, Moser CC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, Sayre RT (2011) Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement. Science 332: 805-809

Comparing photosynthetic and photovoltaic efficiencies is not a simple issue. Although both processes harvest the energy in sunlight, they operate in distinctly different ways and produce different types of products: biomass or chemical fuels in the case of natural photosynthesis and nonstored electrical current in the case of photovoltaics. In order to find common ground for evaluating energy-conversion efficiency, we compare natural photosynthesis with present technologies for photovoltaic-driven electrolysis of water to produce hydrogen. Photovoltaic-driven electrolysis is the more efficient process when measured on an annual basis, yet short-term yields for photosynthetic conversion under optimal conditions come within a factor of 2 or 3 of the photovoltaic benchmark. We consider opportunities in which the frontiers of synthetic biology might be used to enhance natural photosynthesis for improved solar energy conversion efficiency.

Feng ZZ, Pang J, Kobayashi K, Zhu JG, Ort DR (2011) Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open-air field conditions. Global Change Biology, 17: 580-591

Two modern cultivars [Yangmai16 (Y16) and Yangfumai 2 (Y2)] of winter wheat (Triticum aestivum L.) with almost identical phenology were investigated to determine the impacts of elevated ozone concentration (E-O-3) on physiological characters related to photosynthesis under fully open-air field conditions in China. The plants were exposed from the initiation of tillering to final harvest, with E-O-3 of 127 percent of the ambient ozone concentration (A-O-3). Measurements of pigments, gas exchange rates, chlorophyll a fluorescence and lipid oxidation were made in three replicated plots throughout flag leaf development. In cultivar Y2, E-O-3 significantly accelerated leaf senescence, as indicated by increased lipid oxidation as well as faster declines in pigment amounts and photosynthetic rates. The lower photosynthetic rates were mainly due to nonstomatal factors, e.g. lower maximum carboxylation capacity, electron transport rates and light energy distribution. In cultivar Y16, by contrast, the effects of E-O-3 were observed only at the very last stage of flag leaf ageing. Since the two cultivars had almost identical phenology and very similar leaf stomatal conductance before senescence, the greater impacts of E-O-3 on cultivars Y2 than Y16 cannot be explained by differential ozone uptake. Our findings will be useful for scientists to select O-3-tolerant wheat cultivars against the rising surface [O-3] in East and South Asia.

Ainsworth EA, Ort DR (2010) How Do We Improve Crop Production in a Warming World? Plant Physiology, 154: 526-530 (Open Access Article)

Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell and Environment, 33: 1597-1613

To determine if damage to foliage by biotic agents, including arthropods, fungi, bacteria and viral pathogens, universally downregulates the expression of genes involved in photosynthesis, we compared transcriptome data from microarray experiments after twenty two different forms of biotic damage on eight different plant species. Transcript levels of photosynthesis light reaction, carbon reduction cycle and pigment synthesis genes decreased regardless of the type of biotic attack. The corresponding upregulation of genes coding for the synthesis of jasmonic acid and those involved in the responses to salicylic acid and ethylene suggest that the downregulation of photosynthesis-related genes was part of a defence response. Analysis of the sub-cellular targeting of co-expressed gene clusters revealed that the transcript levels of 84 percent of the genes that carry a chloroplast targeting peptide sequence decreased. The majority of these downregulated genes shared common regulatory elements, such as G-box (CACGTG), T-box (ACTTTG) and SORLIP (GCCAC) motifs. Strong convergence in the response of transcription suggests that the universal downregulation of photosynthesis-related gene expression is an adaptive response to biotic attack. We hypothesize that slow turnover of many photosynthetic proteins allows plants to invest resources in immediate defence needs without debilitating near term losses in photosynthetic capacity.

Long SP, Ort DR (2010) More than taking the heat: crops and global change. Current Opinion in Plant Biology, 13: 241-248

Grain production per unit of land will need to more than double over this century to address rising population and demand. This at a time when the procedures that have delivered increased yields over the past 50 years may have reached their ceiling for some of the world's most important crops. Rising global temperature and more frequent droughts will act to drive down yields. The projected rise in atmospheric [CO2] by mid-century could in theory increase crop photosynthesis by over 30 percent, but this is not realized in grain yields in current C-3 cultivars in the field. Emerging understanding of gene networks controlling responses to these environmental changes indicates biotechnological opportunities for adaptation. Considerably more basic research, particularly under realistic field conditions, is critical before these opportunities can be adequately understood and validated. Given the time needed between discovery in a model plant species and translation to traits or stacked changes in a commercial grain crop cultivar, there is an urgent need to vigorously pursue and develop these opportunities now.

Zhu XG, Long SP, Ort DR (2010) Improving Photosynthetic Efficiency for Greater Yield. Annual Review of Plant Biology, 61: 235-261

Increasing the yield potential of the major food grain crops has contributed very significantly to a rising food supply over the past 50 years, which has until recently more than kept pace with rising global demand. Whereas improved photosynthetic efficiency has played only a minor role in the remarkable increases in productivity achieved in the last half century, further increases in yield potential will rely in large part on improved photosynthesis. Here we examine inefficiencies in photosynthetic energy transduction in crops from light interception to carbohydrate synthesis, and how classical breeding, systems biology, and synthetic biology are providing new opportunities to develop more productive germplasm. Near-term opportunities include improving the display of leaves in crop canopies to avoid light saturation of individual leaves and further investigation of a photorespiratory bypass that has already improved the productivity of model species. Longer-term opportunities include engineering into plants carboxylases that are better adapted to current and forthcoming CO2 concentrations, and the use of modeling to guide molecular optimization of resource investment among the components of the photosynthetic apparatus, to maximize carbon gain without increasing crop inputs. Collectively, these changes have the potential to more than double the yield potential of our major crops.

cfqSun JD, Yang LX, Wang YL, Ort DR (2009) FACE-ing the global change: Opportunities for improvement in photosynthetic radiation use efficiency and crop yield. Plant Science, 177: 511-522

The earth is rapidly changing through processes such as rising CO2, O3, and increased food demand. By 2050 the projected atmospheric [CO2] and ground level [O3] will be 50% and 20% higher than today. To meet future agricultural demand, amplified by an increasing population and economic progress in developing countries, crop yields will have to increase by at least 50% by the middle of the century. FACE (Free Air Concentration Enrichment) experiments have been conducted for more than 20 years in various parts of world to estimate, under the most realistic agricultural conditions possible, the impact of the CO2 levels projected for the middle of this century on crops. The stimulations of crop seed yields by the projected CO2 levels across FACE studies are about 18% on average and up to approximately 30% for the hybrid rice varieties and vary among crops, cultivars, nitrogen levels and soil moisture. The observed increase in crop yields under the projected CO2 levels fall short of what would be required to meet the projected future food demand, even with the most responsive varieties. Crop biomass production and seed yield is the product of photosynthetic solar energy conversion. Improvement in photosynthetic radiation use efficiency stands as the most promising opportunity allowing for major increases in crop yield in a future that portends major changes in climate and crop growing environments. Our advanced understanding of the photosynthetic process along with rapidly advancing capabilities in functional genomics, genetic transformation and synthetic biology promises new opportunities for crop improvement by greater photosynthesis and crop yield. Traits and genes that show promise for improving photosynthesis are briefly reviewed, including enhancing leaf photosynthesis capacity and reducing photorespiration loss, manipulating plant hormones' responses for better ideotypes, extending duration of photosynthesis, and increasing carbon partitioning to the sink to alleviate feedback inhibition of photosynthesis.

cfqLeakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. Journal of Experimental Botany, 60: 2859-2876

Plant responses to the projected future levels of CO2 were first characterized in short-term experiments lasting days to weeks. However, longer term acclimation responses to elevated CO2 were subsequently discovered to be very important in determining plant and ecosystem function. Free-Air CO2 Enrichment (FACE) experiments are the culmination of efforts to assess the impact of elevated CO2 on plants over multiple seasons and, in the case of crops, over their entire lifetime. FACE has been used to expose vegetation to elevated concentrations of atmospheric CO2 under completely open-air conditions for nearly two decades. This review describes some of the lessons learned from the long-term investment in these experiments. First, elevated CO2 stimulates photosynthetic carbon gain and net primary production over the long term despite down-regulation of Rubisco activity. Second, elevated CO2 improves nitrogen use efficiency and, third, decreases water use at both the leaf and canopy scale. Fourth, elevated CO2 stimulates dark respiration via a transcriptional reprogramming of metabolism. Fifth, elevated CO2 does not directly stimulate C-4 photosynthesis, but can indirectly stimulate carbon gain in times and places of drought. Finally, the stimulation of yield by elevated CO2 in crop species is much smaller than expected. While many of these lessons have been most clearly demonstrated in crop systems, all of the lessons have important implications for natural systems.

cfqLeakey ADB, Xu F, Gillespie KM, McGrath JM, Ainsworth EA, Ort DR (2009) The genomic basis for stimulated respiratory carbon loss to the atmosphere by plants growing under elevated [CO2].Proceedings of the National Academy of Sciences, USA (2009) 106:3597\0x20133602 (Open Access Article)

Photosynthetic and respiratory exchanges of CO2 by plants with the atmosphere are significantly larger than anthropogenic CO2 emissions, and these fluxes will change as growing conditions are altered by climate change. Understanding feedbacks in CO2 exchange is important to predicting future atmospheric [CO2] and climate change. At the tissue and plant scale, respiration is a key determinant of growth and yield. Although the stimulation of C-3 photosynthesis by growth at elevated [CO2] can be predicted with confidence, the nature of changes in respiration is less certain. This is largely because the mechanism of the respiratory response is insufficiently understood. Molecular, biochemical and physiological changes in the carbon metabolism of soybean in a free-air CO2 enrichment experiment were investigated over 2 growing seasons. Growth of soybean at elevated [CO2] (550 mu mol.mol(-1)) under field conditions stimulated the rate of nighttime respiration by 37%. Greater respiratory capacity was driven by greater abundance of transcripts encoding enzymes throughout the respiratory pathway, which would be needed for the greater number of mitochondria that have been observed in the leaves of plants grown at elevated [CO2]. Greater respiratory quotient and leaf carbohydrate content at elevated [CO2] indicate that stimulated respiration was supported by the additional carbohydrate available from enhanced photosynthesis at elevated [CO2]. If this response is consistent across many species, the future stimulation of net primary productivity could be reduced significantly. Greater foliar respiration at elevated [CO2] will reduce plant carbon balance, but could facilitate greater yields through enhanced photoassimilate export to sink tissues.

cfqLeakey ADB, Ainsworth EA, Bernard SM, Markelz RJC, Ort DR, Placella SA, Rogers A, Smith MD, Sudderth EA, Weston DJ, Wullschleger SD, Yuan SH (2009) Gene expression profiling: opening the black box of plant ecosystem responses to global change. Global Change Biology 15: 1201-1213

The use of genomic techniques to address ecological questions is emerging as the field of genomic ecology. Experimentation under environmentally realistic conditions to investigate the molecular response of plants to meaningful changes in growth conditions and ecological interactions is the defining feature of genomic ecology. Because the impact of global change factors on plant performance are mediated by direct effects at the molecular, biochemical, and physiological scales, gene expression analysis promises important advances in understanding factors that have previously been consigned to the 'black box' of unknown mechanism. Various tools and approaches are available for assessing gene expression in model and nonmodel species as part of global change biology studies. Each approach has its own unique advantages and constraints. A first generation of genomic ecology studies in managed ecosystems and mesocosms have provided a testbed for the approach and have begun to reveal how the experimental design and data analysis of gene expression studies can be tailored for use in an ecological context.

cfqLi PH, Ainsworth EA, Leakey ADB, Ulanov A, Lozovaya V, Ort DR, Bohnert HJ (2008) Arabidopsis transcript and metabolite profiles: ecotype-specific responses to open-air elevated [CO2]. Plant Cell and Environment 31: 1673-1687

A Free-Air CO2 Enrichment (FACE) experiment compared the physiological parameters, transcript and metabolite profiles of Arabidopsis thaliana Columbia-0 (Col-0) and Cape Verde Island (Cvi-0) at ambient (similar to 0.375 mg g(-1)) and elevated (similar to 0.550 mg g(-1)) CO2 ([CO2]). Photoassimilate pool sizes were enhanced in high [CO2] in an ecotype-specific manner. Short-term growth at elevated [CO2] stimulated carbon gain irrespective of down-regulation of plastid functions and altered expression of genes involved in nitrogen metabolism resembling patterns observed under N-deficiency. The study confirmed well-known characteristics, but the use of a time course, ecotypic genetic differences, metabolite analysis and the focus on clusters of functional categories provided new aspects about responses to elevated [CO2]. Longer-term Cvi-0 responded by down-regulating functions favouring carbon accumulation, and both ecotypes showed altered expression of genes for defence, redox control, transport, signalling, transcription and chromatin remodelling. Overall, carbon fixation with a smaller commitment of resources in elevated [CO2] appeared beneficial, with the extra C only partially utilized possibly due to disturbance of the C : N ratio. To different degrees, both ecotypes perceived elevated [CO2] as a metabolic perturbation that necessitated increased functions consuming or storing photoassimilate, with Cvi-0 emerging as more capable of acclimating. Elevated [CO2] in Arabidopsis favoured adjustments in reactive oxygen species (ROS) homeostasis and signalling that defined genotypic markers.

Qiu Q-S, Huber JL, Booker FL, Jain V, Leakey ADB, Fiscus EL, Yau PM, Ort DR, Huber SC (2008) Increased protein carbonylation in leaves of Arabidopsis and soybean in response too elevated [CO2]. Photosynthesis Research 97: 155-166

While exposure of C3 plants to elevated [CO2] would be expected to reduce production of reactive oxygen species (ROS) in leaves because of reduced photorespiratory metabolism, results obtained in the present study suggest that exposure of plants to elevated [CO2] can result in increased oxidative stress. First, in Arabidopsis and soybean, leaf protein carbonylation, a marker of oxidative stress, was often increased when plants were exposed to elevated [CO2]. In soybean, increased carbonyl content was often associated with loss of leaf chlorophyll and reduced enhancement of leaf photosynthetic rate (Pn) by elevated [CO2]. Second, two-dimensional (2-DE) difference gel electrophoresis (DIGE) analysis of proteins extracted from leaves of soybean plants grown at elevated [CO2] or [O3] revealed that both treatments altered the abundance of a similar subset of proteins, consistent with the idea that both conditions may involve an oxidative stress. The 2-DE analysis of leaf proteins was facilitated by a novel and simple procedure to remove ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) from soluble soybean leaf extracts. Collectively, these findings add a new dimension to our understanding of global change biology and raise the possibility that oxidative signals can be an unexpected component of plant response to elevated [CO2].

cfqZhu X-G, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Current Opinion in Biotechnology 19: 153-159

Photosynthesis is the source of our food and fiber. Increasing world population, economic development, and diminishing land resources forecast that a doubling of productivity is critical in meeting agricultural demand before the end of this century. A starting point for evaluating the global potential to meet this goal is establishing the maximum efficiency of photosynthetic solar energy conversion. The potential efficiency of each step of the photosynthetic process from light capture to carbohydrate synthesis is examined. This reveals the maximum conversion efficiency of solar energy to biomass is 4.6% for C3 photosynthesis at 30'C and today's 380 ppm atmospheric [CO2], but 6% for C4 photosynthesis. This advantage over C3 will disappear as atmospheric [CO2] nears 700 ppm.

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