Quantifying impacts of enhancing photosynthesis on crop yield

Enhancing photosynthesis is widely accepted as critical to advancing crop yield. However, yield consequences of photosynthetic manipulation are confounded by feedback effects arising from interactions with crop growth, development dynamics and the prevailing environment. Here, we developed a cross-scale modelling capability that connects leaf photosynthesis to crop yield in a manner that addresses the confounding factors. The model was validated using data on crop biomass and yield for wheat and sorghum from diverse field experiments. Consequences for yield were simulated for major photosynthetic enhancement targets related to leaf CO2 and light energy capture efficiencies, and for combinations of these targets. Predicted impacts showed marked variation and were dependent on the photosynthetic enhancement, crop type and environment, especially the degree of water limitation. The importance of interdependencies operating across scales of biological organization was highlighted, as was the need to increase understanding and modelling of the photosynthesis–stomatal conductance link to better quantify impacts of enhancing photosynthesis.Cross-scale models connecting leaf photosynthesis to crop yield—with feedback between plant growth and the environment—can predict yield following enhancement of photosynthesis. Impacts range markedly depending on factors such as water limitation.

[1]  Chris Murphy,et al.  APSIM - Evolution towards a new generation of agricultural systems simulation , 2014, Environ. Model. Softw..

[2]  Susanne von Caemmerer,et al.  Temperature responses of mesophyll conductance differ greatly between species. , 2015, Plant, cell & environment.

[3]  R. Sage,et al.  C4 Photosynthesis and Related CO2 Concentrating Mechanisms , 2011 .

[4]  Graeme L. Hammer,et al.  Water extraction by grain sorghum in a sub-humid environment. I. Analysis of the water extraction pattern , 1993 .

[5]  A. Rogers,et al.  Photosynthesis, Productivity, and Yield of Maize Are Not Affected by Open-Air Elevation of CO2 Concentration in the Absence of Drought1[OA] , 2006, Plant Physiology.

[6]  G. Hammer,et al.  Functional dynamics of the nitrogen balance of sorghum. II. Grain filling period. , 2010 .

[7]  G. Hammer,et al.  Functional dynamics of the nitrogen balance of sorghum: I. N demand of vegetative plant parts , 2010 .

[8]  R. Furbank,et al.  Strategies for improving C4 photosynthesis. , 2016, Current opinion in plant biology.

[9]  G. Fitzgerald,et al.  'I. , 2019, Australian journal of primary health.

[10]  P. J. Andralojc,et al.  Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. , 2011, Journal of experimental botany.

[11]  William A. Williams,et al.  A model for simulating photosynthesis in plant communities , 1967 .

[12]  S. Long,et al.  Meeting the Global Food Demand of the Future by Engineering Crop Photosynthesis and Yield Potential , 2015, Cell.

[13]  G. Hammer,et al.  Simulating daily field crop canopy photosynthesis: an integrated software package. , 2017, Functional plant biology : FPB.

[14]  O. Ghannoum,et al.  C4 photosynthesis and water stress. , 2008, Annals of botany.

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

[16]  Joe T. Ritchie,et al.  Model for predicting evaporation from a row crop with incomplete cover , 1972 .

[17]  Dean P. Holzworth,et al.  Plant Modelling Framework: Software for building and running crop models on the APSIM platform , 2014, Environ. Model. Softw..

[18]  J. R. Evans Improving Photosynthesis , 2013, Plant Physiology.

[19]  I. R. Cowan,et al.  Stomatal conductance correlates with photosynthetic capacity , 1979, Nature.

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

[21]  J. Flexas,et al.  Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. , 2016, Plant, cell & environment.

[22]  R. Slatyer,et al.  Mechanisms Regulating Photosynthesis in Pennisetum Typhoides , 1973 .

[23]  I. R. Cowan,et al.  Leaf Conductance in Relation to Assimilation in Eucalyptus pauciflora Sieb. ex Spreng: Influence of Irradiance and Partial Pressure of Carbon Dioxide. , 1978, Plant physiology.

[24]  A. Cousins,et al.  Temperature response of mesophyll conductance in three C4 species calculated with two methods: 18 O discrimination and in vitro Vpmax. , 2017, The New phytologist.

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

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

[27]  W. Diepenbrock,et al.  Integrating effects of leaf nitrogen, age, rank, and growth temperature into the photosynthesis-stomatal conductance model LEAFC3-N parameterised for barley (Hordeum vulgare L.) , 2009 .

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

[29]  J. Amir,et al.  A model of water limitation on spring wheat growth and yield , 1991 .

[30]  Martin A. J. Parry,et al.  A faster Rubisco with potential to increase photosynthesis in crops , 2014, Nature.

[31]  N. McDowell,et al.  Tobacco aquaporin NtAQP 1 is involved in mesophyll conductance to CO 2 in vivo , 2006 .

[32]  Graeme L. Hammer,et al.  Can Changes in Canopy and/or Root System Architecture Explain Historical Maize Yield Trends in the U.S. Corn Belt? , 2009 .

[33]  T. Sinclair,et al.  Crop transformation and the challenge to increase yield potential. , 2004, Trends in plant science.

[34]  J. Flexas,et al.  Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. , 2012, Plant science : an international journal of experimental plant biology.

[35]  J. R. Evans,et al.  Nitrogen and Photosynthesis in the Flag Leaf of Wheat (Triticum aestivum L.). , 1983, Plant physiology.

[36]  Graeme L. Hammer,et al.  Connecting Biochemical Photosynthesis Models with Crop Models to Support Crop Improvement , 2016, Front. Plant Sci..

[37]  Susanne von Caemmerer,et al.  Enhancing C3 Photosynthesis , 2010, Plant Physiology.

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

[39]  Richard Trethowan,et al.  Variation in mesophyll conductance among Australian wheat genotypes. , 2014, Functional plant biology : FPB.

[40]  Greg McLean,et al.  Adapting APSIM to model the physiology and genetics of complex adaptive traits in field crops. , 2010, Journal of experimental botany.

[41]  K. Mott,et al.  Effects of the mesophyll on stomatal responses in amphistomatous leaves. , 2018, Plant, cell & environment.

[42]  Takeshi Horie,et al.  Leaf Nitrogen, Photosynthesis, and Crop Radiation Use Efficiency: A Review , 1989 .

[43]  Josep Cifre,et al.  Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. , 2006, The Plant journal : for cell and molecular biology.

[44]  T. Sinclair Is transpiration efficiency a viable plant trait in breeding for crop improvement? , 2012, Functional plant biology : FPB.

[45]  Diversity in stomatal function is integral to modelling plant carbon and water fluxes , 2017, Nature Ecology & Evolution.

[46]  Mark E. Cooper,et al.  Modelling Crop Improvement in a G×E×M Framework via Gene–Trait–Phenotype Relationships , 2009 .

[47]  Tracy Lawson,et al.  Overexpression of the RieskeFeS Protein Increases Electron Transport Rates and Biomass Yield1[CC-BY] , 2017, Plant Physiology.

[48]  R. Dalal,et al.  APSIM's water and nitrogen modules and simulation of the dynamics of water and nitrogen in fallow systems , 1998 .

[49]  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.

[50]  Wataru Yamori,et al.  The rate-limiting step for CO(2) assimilation at different temperatures is influenced by the leaf nitrogen content in several C(3) crop species. , 2011, Plant, cell & environment.

[51]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[52]  T. Lawson,et al.  Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. , 2004, Journal of experimental botany.

[53]  R. Furbank,et al.  Functional Analysis of Corn Husk Photosynthesis[W][OA] , 2011, Plant Physiology.

[54]  K. Noguchi,et al.  Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. , 2013, The New phytologist.

[55]  Paul C. Struik,et al.  Can increased leaf photosynthesis be converted into higher crop mass production? A simulation study for rice using the crop model GECROS , 2017, Journal of experimental botany.

[56]  J. Foley,et al.  Yield Trends Are Insufficient to Double Global Crop Production by 2050 , 2013, PloS one.

[57]  E. M. Larson,et al.  Simulation of canopy photosynthesis in maize and soybean , 1989 .

[58]  Albert Olioso,et al.  Simulation of diurnal transpiration and photosynthesis of a water stressed soybean crop , 1996 .

[59]  J. R. Evans,et al.  Chapter 8 Nitrogen and Water Use Efficiency of C 4 Plants , 2010 .