1932

Abstract

Photorespiration is essential for C plants but operates at the massive expense of fixed carbon dioxide and energy. Photorespiration is initiated when the initial enzyme of photosynthesis, ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), reacts with oxygen instead of carbon dioxide and produces a toxic compound that is then recycled by photorespiration. Photorespiration can be modeled at the canopy and regional scales to determine its cost under current and future atmospheres. A regional-scale model reveals that photorespiration currently decreases US soybean and wheat yields by 36% and 20%, respectively, and a 5% decrease in the losses due to photorespiration would be worth approximately $500 million annually in the United States. Furthermore, photorespiration will continue to impact yield under future climates despite increases in carbon dioxide, with models suggesting a 12–55% improvement in gross photosynthesis in the absence of photorespiration, even under climate change scenarios predicting the largest increases in atmospheric carbon dioxide concentration. Although photorespiration is tied to other important metabolic functions, the benefit of improving its efficiency appears to outweigh any potential secondary disadvantages.

[Erratum, Closure]

An erratum has been published for this article:
The Costs of Photorespiration to Food Production Now and in the Future
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043015-111709
2016-04-29
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/arplant/67/1/annurev-arplant-043015-111709.html?itemId=/content/journals/10.1146/annurev-arplant-043015-111709&mimeType=html&fmt=ahah

Literature Cited

  1. Ainsworth EA, Long SP. 1.  2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol. 165:351–72 [Google Scholar]
  2. Ainsworth EA, Rogers A. 2.  2007. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ. 30:258–70 [Google Scholar]
  3. Alexandratos N, Bruinsma J. 3.  2012. World agriculture towards 2030/2050: the 2012 revision ESA Work. Pap. 12-03, Agric. Dev. Econ. Div., Food Agric. Organ. UN, Rome
  4. Badger MR, Collatz GJ. 4.  1978. Studies on the kinetic mechanism of ribulose-1,5-bisphosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Inst. Wash. Yearb. 76:355–61 [Google Scholar]
  5. Bagley J, Rosenthal DM, Ruiz-Vera UM, Siebers MH, Kumar P. 5.  et al. 2015. The influence of photosynthetic acclimation to rising CO2 and warmer temperatures on leaf and canopy photosynthesis models. Glob. Biogeochem. Cycles 29:194–206 [Google Scholar]
  6. Ball JT, Woodrow I, Berry J. 6.  1987. A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. Progress in Photosynthesis Research, Vol. 4: Proceedings of the VIIth International Congress on Photosynthesis Providence, Rhode Island, USA, August 10–15, 1986 J Biggins 221–24 Dordrecht, Neth: Springer [Google Scholar]
  7. Bernacchi CJ, Bagley JE, Serbin SP, Ruiz-Vera UM, Rosenthal DM, VanLoocke A. 7.  2013. Modelling C3 photosynthesis from the chloroplast to the ecosystem. Plant Cell Environ. 36:1641–57 [Google Scholar]
  8. Bernacchi CJ, Morgan PB, Ort DR, Long SP. 8.  2005. The growth of soybean under free air CO2 enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220:434–46 [Google Scholar]
  9. Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP. 9.  2002. Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol. 130:1992–98 [Google Scholar]
  10. Berner RA. 10.  1999. Atmospheric oxygen over Phanerozoic time. PNAS 96:10955–57 [Google Scholar]
  11. Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G. 11.  et al. 2011. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–9 [Google Scholar]
  12. Bloom AJ, Asensio JSR, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA. 12.  2011. CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93:355–67 [Google Scholar]
  13. Bloom AJ, Burger M, Asensio JSR, Cousins AB. 13.  2010. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903 [Google Scholar]
  14. Bloom AJ, Burger M, Kimball BA, Pinter PJ Jr. 14.  2014. Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat. Clim. Change 4:477–80 [Google Scholar]
  15. Buckley TN, Mott KA, Farquhar GD. 15.  2003. A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ. 26:1767–85 [Google Scholar]
  16. Bunce JA. 16.  1988. Effects of boundary layer conductance on substomatal pressures of carbon dioxide. Plant Cell Environ. 11:205–8 [Google Scholar]
  17. Busch FA, Sage TL, Cousins AB, Sage RF. 17.  2013. C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ. 36:200–12 [Google Scholar]
  18. Campbell G, Norman J. 18.  1998. Introduction to Environmental Biophysics New York: Springer
  19. Cen Y-P, Sage RF. 19.  2005. The regulation of Rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol. 139:979–90 [Google Scholar]
  20. Collatz GJ, Ball JT, Grivet C, Berry JA. 20.  1991. Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer. Agric. For. Meteorol. 54:107–36 [Google Scholar]
  21. Cousins A, Bloom A. 21.  2003. Influence of elevated CO2 and nitrogen nutrition on photosynthesis and nitrate photo-assimilation in maize (Zea mays L.). Plant Cell Environ. 26:1525–30 [Google Scholar]
  22. Donner SD, Kucharik CJ. 22.  2003. Evaluating the impacts of land management and climate variability on crop production and nitrate export across the Upper Mississippi Basin. Glob. Biogeochem. Cycles 17:1085 [Google Scholar]
  23. Drake BG, Gonzàlez-Meler MA, Long SP. 23.  1997. More efficient plants: a consequence of rising atmospheric CO2?. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:609–39 [Google Scholar]
  24. Drewry DT, Kumar P, Long S, Bernacchi CJ, Liang XZ, Sivapalan M. 24.  2010. Ecohydrological responses of dense canopies to environmental variability: 1. Interplay between vertical structure and photosynthetic pathway. J. Geophys. Res. Biogeosci. 115:G04022 [Google Scholar]
  25. Drewry DT, Kumar P, Long S, Bernacchi CJ, Liang XZ, Sivapalan M. 25.  2010. Ecohydrological responses of dense canopies to environmental variability: 2. Role of acclimation under elevated CO2. J. Geophys. Res. Biogeosci. 115:G001341 [Google Scholar]
  26. Edwards GE, Walker DA. 26.  1983. C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis Oxford, UK: Blackwell Sci.
  27. 27. FAO (Food Agric. Organ. UN), IFAD (Int. Fund Agric. Dev.), WFP (World Food Programme) 2015. The state of food insecurity in the world 2015: strengthening the enabling environment for food security and nutrition. Rep., FAO, Rome
  28. Farquhar GD, von Caemmerer S, Berry JA. 28.  1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90 [Google Scholar]
  29. Fischer RA, Rees D, Sayre KD, Lu Z-M, Condon AG, Saavedra AL. 29.  1998. Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci. 38:1467–75 [Google Scholar]
  30. Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H. 30.  2008. Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ. 31:602–21 [Google Scholar]
  31. Foley JA, Prentice IC, Ramankutty N, Levis S, Pollard D. 31.  et al. 1996. An integrated biosphere model of land surface processes, terrestrial carbon balance, and vegetation dynamics. Glob. Biogeochem. Cycles 10:603–28 [Google Scholar]
  32. Foyer CH, Bloom AJ, Queval G, Noctor G. 32.  2009. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu. Rev. Plant Biol. 60:455–84 [Google Scholar]
  33. Green MA, Emery K, Hishikawa Y, Warta W, Dunlop ED. 33.  2015. Solar cell efficiency tables (version 45). Prog. Photovolt. Res. Appl. 23:1–9 [Google Scholar]
  34. Hanning I, Heldt HW. 34.  1993. On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves: partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products. Plant Physiol. 103:1147–54 [Google Scholar]
  35. Hanson A, Roje S. 35.  2001. One-carbon metabolism in higher plants. Annu. Rev. Plant Biol. 52:119–37 [Google Scholar]
  36. Hibberd JM, Sheehy JE, Langdale JA. 36.  2008. Using C4 photosynthesis to increase the yield of rice—rationale and feasibility. Curr. Opin. Plant Biol. 11:228–31 [Google Scholar]
  37. 37. IPCC (Intergov. Panel Clim. Change) 2013. Principles governing IPCC work https://www.ipcc.ch/pdf/ipcc-principles/ipcc-principles.pdf
  38. 38. IPCC (Intergov. Panel Clim. Change) 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, Switz: IPCC
  39. Jones HG. 39.  2013. Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology Cambridge, UK: Cambridge Univ. Press
  40. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J. 40.  et al. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol. 25:593–99 [Google Scholar]
  41. Kramer DM, Evans JR. 41.  2011. The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155:70–78 [Google Scholar]
  42. Kucharik CJ. 42.  2003. Evaluation of a process-based agro-ecosystem model (Agro-IBIS) across the U.S. Corn Belt: simulations of the interannual variability in maize yield. Earth Interact. 7:1–33 [Google Scholar]
  43. Kucharik CJ, Brye KR. 43.  2003. Integrated BIosphere Simulator (IBIS) yield and nitrate loss predictions for Wisconsin maize receiving varied amounts of nitrogen fertilizer. J. Environ. Qual. 32:247–68 [Google Scholar]
  44. Kucharik CJ, Foley JA, Delire C, Fisher VA, Coe MT. 44.  et al. 2000. Testing the performance of a dynamic global ecosystem model: water balance, carbon balance, and vegetation structure. Glob. Biogeochem. Cycles 14:795–825 [Google Scholar]
  45. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR. 45.  2009. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60:2859–76 [Google Scholar]
  46. Lobell DB, Asner GP. 46.  2003. Climate and management contributions to recent trends in U.S. agricultural yields. Science 299:1032 [Google Scholar]
  47. Lobell DB, Burke MB. 47.  2008. Why are agricultural impacts of climate change so uncertain? The importance of temperature relative to precipitation. Environ. Res. Lett. 3:034007 [Google Scholar]
  48. Lobell DB, Field CB. 48.  2007. Global scale climate–crop yield relationships and the impacts of recent warming. Environ. Res. Lett. 2:014002 [Google Scholar]
  49. Long SP, Ainsworth EA, Leakey ADB, Nösberger J, Ort DR. 49.  2006. Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312:1918–21 [Google Scholar]
  50. Maier A, Fahnenstich H, von Caemmerer S, Engqvist MK, Weber APM. 50.  et al. 2012. Glycolate oxidation in A. thaliana chloroplasts improves biomass production. Front. Plant Sci. 3:38 [Google Scholar]
  51. Maurino VG, Peterhansel C. 51.  2010. Photorespiration: current status and approaches for metabolic engineering. Curr. Opin. Plant Biol. 13:248–55 [Google Scholar]
  52. Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC. 52.  et al. 2011. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob. Change Biol. 17:2134–44 [Google Scholar]
  53. Michael JR, Wolfram S. 53.  2013. Identifying supply and demand elasticities of agricultural commodities: implications for the US ethanol mandate. Am. Econ. Rev. 103:2265–95 [Google Scholar]
  54. Moore BD, Cheng SH, Rice J, Seemann JR. 54.  1998. Sucrose cycling, Rubisco expression, and prediction of photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ. 21:905–15 [Google Scholar]
  55. Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey ADB. 55.  et al. 2014. Increasing CO2 threatens human nutrition. Nature 510:139–42 [Google Scholar]
  56. Ogren WL. 56.  1984. Photorespiration: pathways, regulation, and modification. Annu. Rev. Plant Physiol. 35:415–42 [Google Scholar]
  57. Ort DR, Baker NR. 57.  2002. A photoprotective role for O2 as an alternative electron sink in photosynthesis?. Curr. Opin. Plant Biol. 5:193–98 [Google Scholar]
  58. Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE. 58.  et al. 2015. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. PNAS 112:8529–36 [Google Scholar]
  59. Peltier G, Aro E-M, Shikanai T. 59.  2016. NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu. Rev. Plant Biol. 67:55–80 [Google Scholar]
  60. Peterhansel C, Blume C, Offermann S. 60.  2013. Photorespiratory bypasses: How can they work?. J. Exp. Bot. 64:709–15 [Google Scholar]
  61. Rachmilevitch S, Cousins AB, Bloom AJ. 61.  2004. Nitrate assimilation in plant shoots depends on photorespiration. PNAS 101:11506–10 [Google Scholar]
  62. Ray DK, Mueller ND, West PC, Foley JA. 62.  2013. Yield trends are insufficient to double global crop production by 2050. PLOS ONE 8:e66428 [Google Scholar]
  63. Rogers A, Humphries SW. 63.  2000. A mechanistic evaluation of photosynthetic acclimation at elevated CO2. Glob. Change Biol. 6:1005–11 [Google Scholar]
  64. Ruiz-Vera UM, Siebers M, Gray SB, Drag DW, Rosenthal DM. 64.  et al. 2013. Global warming can negate the expected CO2 stimulation in photosynthesis and productivity for soybean grown in the midwestern United States. Plant Physiol. 162:410–23 [Google Scholar]
  65. Sage RF, Way DA, Kubien DS. 65.  2008. Rubisco, Rubisco activase, and global climate change. J. Exp. Bot. 59:1581–95 [Google Scholar]
  66. Salvucci ME, Crafts-Brandner SJ. 66.  2004. Mechanism for deactivation of Rubisco under moderate heat stress. Physiol. Plant. 122:513–19 [Google Scholar]
  67. Sharkey TD. 67.  1988. Estimating the rate of photorespiration in leaves. Physiol. Plant. 73:147–52 [Google Scholar]
  68. Somerville C. 68.  1986. Analysis of photosynthesis with mutants of higher plants and algae. Annu. Rev. Plant Physiol. 37:467–506 [Google Scholar]
  69. Sun Y, Gu L, Dickinson RE, Norby RJ, Pallardy SG, Hoffman FM. 69.  2014. Impact of mesophyll diffusion on estimated global land CO2 fertilization. PNAS 111:15774–79 [Google Scholar]
  70. Tans P. 70.  2015. Trends in atmospheric carbon dioxide Glob. Monit. Div., Earth Syst. Res. Lab., Natl. Ocean. Atmos. Adm., Boulder, CO. http://www.esrl.noaa.gov/gmd/ccgg/trends
  71. Tholen D, Ethier G, Genty B, Pepin S, Zhu X-G. 71.  2012. Variable mesophyll conductance revisited: theoretical background and experimental implications. Plant Cell Environ. 35:2087–103 [Google Scholar]
  72. Tholen D, Zhu X-G. 72.  2011. The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol. 156:90–105 [Google Scholar]
  73. Thompson SL, Pollard D. 73.  1995. A global climate model (GENESIS) with a land-surface transfer scheme (LSX). Part I: present climate simulation. J. Clim. 8:732–61 [Google Scholar]
  74. Thompson SL, Pollard D. 74.  1995. A global climate model (GENESIS) with a land-surface transfer scheme (LSX). Part II: CO2 sensitivity. J. Clim. 8:1104–21 [Google Scholar]
  75. Tilman D, Balzer C, Hill J, Befort BL. 75.  2011. Global food demand and the sustainable intensification of agriculture. PNAS 108:20260–64 [Google Scholar]
  76. von Caemmerer S. 76.  2000. Biochemical Models of Leaf Photosynthesis Collingwood, Aust: CSIRO
  77. von Caemmerer S. 77.  2013. Steady-state models of photosynthesis. Plant Cell Environ. 36:1617–30 [Google Scholar]
  78. von Caemmerer S, Evans JR. 78.  2015. Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ. 38:629–37 [Google Scholar]
  79. von Caemmerer S, Farquhar GD. 79.  1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–87 [Google Scholar]
  80. Walker BJ, Ariza LS, Kaines S, Badger MR, Cousins AB. 80.  2013. Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant Cell Environ. 36:2108–19 [Google Scholar]
  81. Walker BJ, Ort DR. 81.  2015. Improved method for measuring the apparent CO2 photocompensation point resolves the impact of multiple internal conductances to CO2 to net gas exchange. Plant Cell Environ. 38:2462–74 [Google Scholar]
  82. Walker BJ, Strand DD, Kramer DM, Cousins AB. 82.  2014. The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation. Plant Physiol. 165:453–62 [Google Scholar]
  83. Whitney SM, Houtz RL, Alonso H. 83.  2011. Advancing our understanding and capacity to engineer nature's CO2-sequestering enzyme, Rubisco. Plant Physiol. 155:27–35 [Google Scholar]
  84. Wingler A, Lea PJ, Quick WP, Leegood RC. 84.  2000. Photorespiration: metabolic pathways and their role in stress protection. Philos. Trans. R. Soc. Lond. B 355:1517–29 [Google Scholar]
  85. 85. Wolfram Res 2015. Mathematica Wolfram Res., Champaign, IL. http://www.wolfram.com/mathematica
  86. Xin C, Tholen D, Zhu X-G. 86.  2014. The benefits of photorespiratory bypasses: How can they work?. Plant Physiol. 167:574–85 [Google Scholar]
  87. Yamori W, Shikanai T. 87.  2016. Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu. Rev. Plant Biol. 67:81–106 [Google Scholar]
  88. Zhu X-G, Long SP, Ort DR. 88.  2008. What is the maximum efficiency with which photosynthesis can convert solar energy into biomass?. Curr. Opin. Biotechnol. 19:153–59 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043015-111709
Loading
/content/journals/10.1146/annurev-arplant-043015-111709
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error