Constraints to the potential efficiency of converting solar radiation into phytoenergy in annual crops: from leaf biochemistry to canopy physiology and crop ecology.

A new simple framework was proposed to quantify the efficiency of converting incoming solar radiation into phytoenergy in annual crops. It emphasizes the need to account for (i) efficiency gain when scaling up from the leaf level to the canopy level, and (ii) efficiency loss due to incomplete canopy closure during early and late phases of the crop cycle. Equations are given to estimate losses due to the constraints in various biochemical or physiological steps. For a given amount of daily radiation, a longer daytime was shown to increase energy use efficiency, because of the convex shape of the photosynthetic light response. Due to the higher cyclic electron transport, C4 leaves were found to have a lower energy loss via non-photochemical quenching, compared with C3 leaves. This contributes to the more linear light response in C4 than in C3 photosynthesis. Because of this difference in the curvature of the light response, canopy-to-leaf photosynthesis ratio, benefit from the optimum acclimation of the leaf nitrogen profile in the canopy, and productivity gain from future improvements in leaf photosynthetic parameters and canopy architecture were all shown to be higher in C3 than in C4 species. The indicative efficiency of converting incoming solar radiation into phytoenergy is ~2.2 and 3.0% in present C3 and C4 crops, respectively, when grown under well-managed conditions. An achievable efficiency via future genetic improvement was estimated to be as high as 3.6 and 4.1% for C3 and C4 crops, respectively.

[1]  R. Loomis,et al.  The Prediction of Canopy Assimilation , 2015 .

[2]  K. Hikosaka,et al.  Optimal nitrogen distribution within a leaf canopy under direct and diffuse light. , 2014, Plant, cell & environment.

[3]  Xinyou Yin,et al.  Accounting for the decrease of photosystem photochemical efficiency with increasing irradiance to estimate quantum yield of leaf photosynthesis , 2014, Photosynthesis Research.

[4]  Donald R Ort,et al.  The theoretical limit to plant productivity. , 2014, Environmental science & technology.

[5]  Barbara George-Jaeggli,et al.  Stay-green alleles individually enhance grain yield in sorghum under drought by modifying canopy development and water uptake patterns. , 2014, The New phytologist.

[6]  P. J. Andralojc,et al.  Natural variation in photosynthetic capacity, growth, and yield in 64 field-grown wheat genotypes , 2014, Journal of experimental botany.

[7]  M. Badger,et al.  Transplastomic integration of a cyanobacterial bicarbonate transporter into tobacco chloroplasts , 2014, Journal of experimental botany.

[8]  H. Griffiths,et al.  Acclimation of C4 metabolism to low light in mature maize leaves could limit energetic losses during progressive shading in a crop canopy , 2014, Journal of experimental botany.

[9]  J. McGrath,et al.  Can the Cyanobacterial Carbon-Concentrating Mechanism Increase Photosynthesis in Crop Species? A Theoretical Analysis1[W][OPEN] , 2014, Plant Physiology.

[10]  E H Murchie,et al.  Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. , 2013, Journal of experimental botany.

[11]  Alessandro Cescatti,et al.  What does optimization theory actually predict about crown profiles of photosynthetic capacity when models incorporate greater realism? , 2013, Plant, cell & environment.

[12]  Xin-Guang Zhu,et al.  Opinion: prospects for improving photosynthesis by altering leaf anatomy. , 2012, Plant science : an international journal of experimental plant biology.

[13]  V. Allard,et al.  Acclimation of Leaf Nitrogen to Vertical Light Gradient at Anthesis in Wheat Is a Whole-Plant Process That Scales with the Size of the Canopy1[W][OA] , 2012, Plant Physiology.

[14]  Xinyou Yin,et al.  Physiological basis of genetic variation in leaf photosynthesis among rice (Oryza sativa L.) introgression lines under drought and well-watered conditions , 2012, Journal of experimental botany.

[15]  Xinyou Yin,et al.  Mathematical review of the energy transduction stoichiometries of C(4) leaf photosynthesis under limiting light. , 2012, Plant, cell & environment.

[16]  Susanne von Caemmerer,et al.  The Development of C4 Rice: Current Progress and Future Challenges , 2012, Science.

[17]  F. Rappaport,et al.  Back‐reactions, short‐circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O2 , 2012, FEBS letters.

[18]  Xinyou Yin,et al.  Using a biochemical C4 photosynthesis model and combined gas exchange and chlorophyll fluorescence measurements to estimate bundle-sheath conductance of maize leaves differing in age and nitrogen content. , 2011, Plant, cell & environment.

[19]  P. C. Struik,et al.  Leaf photosynthesis and respiration of three bioenergy crops in relation to temperature and leaf nitrogen: how conserved are biochemical model parameters among crop species? , 2011, Journal of experimental botany.

[20]  Paul C. Struik,et al.  Temporal dynamics of light and nitrogen vertical distributions in canopies of sunflower, kenaf and cynara , 2011 .

[21]  Wei Sun,et al.  The efficiency of C(4) photosynthesis under low light conditions: assumptions and calculations with CO(2) isotope discrimination. , 2011, Journal of experimental botany.

[22]  N. Baker,et al.  The water-water cycle in leaves is not a major alternative electron sink for dissipation of excess excitation energy when CO(2) assimilation is restricted. , 2011, Plant, cell & environment.

[23]  G. Johnson,et al.  Physiology of PSI cyclic electron transport in higher plants. , 2011, Biochimica et biophysica acta.

[24]  J. Amthor From sunlight to phytomass: on the potential efficiency of converting solar radiation to phyto-energy. , 2010, The New phytologist.

[25]  D. Ort,et al.  Optimizing Antenna Size to Maximize Photosynthetic Efficiency[W] , 2010, Plant Physiology.

[26]  H. Griffiths,et al.  Can the progressive increase of C₄ bundle sheath leakiness at low PFD be explained by incomplete suppression of photorespiration? , 2010, Plant, cell & environment.

[27]  F. Dohleman,et al.  Does greater leaf-level photosynthesis explain the larger solar energy conversion efficiency of Miscanthus relative to switchgrass? , 2009, Plant, cell & environment.

[28]  F. Dohleman,et al.  More Productive Than Maize in the Midwest: How Does Miscanthus Do It?1[W][OA] , 2009, Plant Physiology.

[29]  H.J.M. de Groot,et al.  Harnessing Solar Energy for the Production of Clean Fuel , 2008 .

[30]  Joshua S Yuan,et al.  Plants to power: bioenergy to fuel the future. , 2008, Trends in plant science.

[31]  N. Carpita,et al.  Maize and sorghum: genetic resources for bioenergy grasses. , 2008, Trends in plant science.

[32]  D. S. Kubien,et al.  The biochemistry of Rubisco in Flaveria. , 2008, Journal of experimental botany.

[33]  S. Long,et al.  What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? , 2008, Current opinion in biotechnology.

[34]  David M Kramer,et al.  Determining the limitations and regulation of photosynthetic energy transduction in leaves. , 2007, Plant, cell & environment.

[35]  Xin-Guang Zhu,et al.  Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm1[W][OA] , 2007, Plant Physiology.

[36]  R. Rosenkranz,et al.  Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana , 2007, Nature Biotechnology.

[37]  Xinyou Yin,et al.  Mathematical review of literature to assess alternative electron transports and interphotosystem excitation partitioning of steady-state C3 photosynthesis under limiting light. , 2006, Plant, cell & environment.

[38]  S. Long,et al.  Can improvement in photosynthesis increase crop yields? , 2006, Plant, cell & environment.

[39]  Xinyou Yin,et al.  Crop Systems Dynamics: An Ecophysiological Simulation Model for Genotype-By-Environment Interactions , 2005 .

[40]  Xinyou Yin,et al.  Extension of a biochemical model for the generalized stoichiometry of electron transport limited C3 photosynthesis , 2004 .

[41]  Carl J. Bernacchi,et al.  In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis , 2003 .

[42]  Göran Berndes,et al.  The contribution of biomass in the future global energy supply: a review of 17 studies , 2003 .

[43]  Roger M. Gifford,et al.  Plant respiration in productivity models: conceptualisation, representation and issues for global terrestrial carbon-cycle research. , 2003, Functional plant biology : FPB.

[44]  Jan Vos,et al.  A flexible sigmoid function of determinate growth. , 2003, Annals of botany.

[45]  L. Fuchigami,et al.  159 The Relationship between Actual Photosystem II Efficiency and Quantum Yield for CO2 Assimilation is Not Affected by Nitrogen Content in Apple Leaves , 2000 .

[46]  S. Ruuska,et al.  Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. , 2000, Journal of experimental botany.

[47]  S. V. Caemmerer,et al.  Biochemical models of leaf photosynthesis. , 2000 .

[48]  R. Loomis,et al.  Yield Potential, Plant Assimilatory Capacity, and Metabolic Efficiencies , 1999 .

[49]  K. Asada,et al.  THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons. , 1999, Annual review of plant physiology and plant molecular biology.

[50]  E. Titarenko,et al.  Jasmonic Acid-Dependent and -Independent Signaling Pathways Control Wound-Induced Gene Activation in Arabidopsis thaliana , 1997, Plant physiology.

[51]  D. Pury,et al.  Simple scaling of photosynthesis from leaves to canopies without the errors of big‐leaf models , 1997 .

[52]  W. W. Adams,et al.  Enhanced Employment of the Xanthophyll Cycle and Thermal Energy Dissipation in Spinach Exposed to High Light and N Stress , 1997, Plant physiology.

[53]  Stephen P. Long,et al.  Leaf photosynthesis in the C4-grass Miscanthus x giganteus, growing in the cool temperate climate of southern England , 1996 .

[54]  Roger M. Gifford,et al.  Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long‐term vs. short‐term distinctions for modelling , 1995 .

[55]  Stephen P. Long,et al.  Can perennial C4 grasses attain high efficiencies of radiant energy conversion in cool climates , 1995 .

[56]  M. Werger,et al.  Patterns of light and nitrogen distribution in relation to whole canopy carbon gain in C3 and C4 mono- and dicotyledonous species , 1995, Oecologia.

[57]  John R. Evans,et al.  The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco , 1994, Planta.

[58]  W. Junk,et al.  Leaf and canopy photosynthetic CO2 uptake of a stand of Echinochloa polystachya on the Central Amazon floodplain , 1994, Oecologia.

[59]  E. Ögren Convexity of the Photosynthetic Light-Response Curve in Relation to Intensity and Direction of Light during Growth. , 1993 .

[60]  S. Long,et al.  Quantum yields for uptake of carbon dioxide in C3 vascular plants of contrasting habitats and taxonomic groupings , 1993, Planta.

[61]  James F. Reynolds,et al.  Modelling photosynthesis of cotton grown in elevated CO2 , 1992 .

[62]  Stephen P. Long,et al.  The Productivity of the C_4 Grass Echinochloa Polystachya on the Amazon Floodplain , 1991 .

[63]  H. Berge,et al.  Simulation of Ecophysiological Processes of Growth in Several Annual Crops , 1989 .

[64]  Graham D. Farquhar,et al.  Models of Integrated Photosynthesis of Cells and Leaves , 1989 .

[65]  O. Björkman,et al.  Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins , 1987, Planta.

[66]  J. Ehleringer,et al.  Variation in Quantum Yield for CO(2) Uptake among C(3) and C(4) Plants. , 1983, Plant physiology.

[67]  D. Wilson,et al.  Effect of Selection for Dark Respiration Rate of Mature Leaves on Crop Yields of Lolium perenne cv. S23 , 1982 .

[68]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[69]  J. Monteith Climate and the efficiency of crop production in Britain , 1977 .

[70]  C. E. Murphy,et al.  Development and Evaluation of Simplified Models for Simulating Canopy Photosynthesis and Transpiration , 1976 .

[71]  J. Monteith SOLAR RADIATION AND PRODUCTIVITY IN TROPICAL ECOSYSTEMS , 1972 .

[72]  R. Emerson The Quantum Yield of Photosynthesis , 1958 .

[73]  Xinyou Yin,et al.  Can exploiting natural genetic variation in leaf photosynthesis contribute to increasing rice productivity? A simulation analysis. , 2014, Plant, cell & environment.

[74]  G. Garab,et al.  Chlorophyll a fluorescence: beyond the limits of the QA model , 2013, Photosynthesis Research.

[75]  Florian A. Busch,et al.  C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. , 2013, Plant, cell & environment.

[76]  J. Allen Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. , 2003, Trends in plant science.

[77]  A. Condon,et al.  Evaluating the Impact of a Trait for Increased Specific Leaf Area on Wheat Yields Using a Crop Simulation Model , 2003 .

[78]  J. H. M. Thornley,et al.  Modelling the Components of Plant Respiration: Some Guiding Principles , 2000 .

[79]  R. C. Muchow,et al.  Radiation Use Efficiency , 1999 .

[80]  P. Sands Modelling Canopy Production. I. Optimal Distribution of Photosynthetic Resources , 1995 .

[81]  U. Schreiber,et al.  Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis , 1995 .

[82]  J. Goudriaan,et al.  Modelling Potential Crop Growth Processes , 1994, Current Issues in Production Ecology.

[83]  Graeme L. Hammer,et al.  A theoretical analysis of nitrogen and radiation effects on radiation use efficiency in peanut , 1994 .

[84]  M. J. Kropff,et al.  Mogelijkheden en beperkingen van biomassa als energiebron. , 1991 .

[85]  I. Terashima,et al.  Effects of Light and Nitrogen Nutrition on the Organization of the Photosynthetic Apparatus in Spinach , 1988 .

[86]  Jhanel Wilson,et al.  A comparison of barley cultivars with different leaf inclinations , 1972 .

[87]  R. Loomis,et al.  Maximum Crop Productivity: An Extimate 1 , 1963 .

[88]  Alfred Ursprung,et al.  Plant Physiology , 1949, Nature.