The Costs of Photorespiration to Food Production Now and in the Future

Annual Review of Plant Biology

Volumn 67, Issue , 2016, Pages 107-129

  Walker, Berkley J ^a,b   Vanloocke, Andy ^c   Bernacchi, Carl J ^a,b   Ort, Donald R ^a,b  

^a US Department of Agriculture Agricultural Research Service   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Climate change; Food security; Modeling

Indexed keywords

CARBON DIOXIDE; OXYGEN; RIBULOSEBISPHOSPHATE CARBOXYLASE;

AGRICULTURE; BIOMASS; CLIMATE CHANGE; CROP; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DEVELOPMENT; PLANT PHYSIOLOGY;

AGRICULTURE; BIOMASS; CARBON DIOXIDE; CLIMATE CHANGE; CROPS, AGRICULTURAL; OXYGEN; PHOTOSYNTHESIS; PLANT DEVELOPMENT; PLANT PHYSIOLOGICAL PHENOMENA; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84968735652     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-043015-111709     Document Type: Review

References (88)

1. Ainsworth EA, Long SP. 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
2. Ainsworth EA, Rogers A. 2007. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ. 30:258-70
3. Alexandratos N, Bruinsma J. 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. 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
5. Bagley J, Rosenthal DM, Ruiz-Vera UM, Siebers MH, Kumar P, 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
6. Ball JT, Woodrow I, Berry J. 1987. A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In Progress in Photosynthesis Research, Vol. 4: Proceedings of the VIIth International Congress on Photosynthesis Providence, Rhode Island, USA, August 10-15, 1986, ed. J Biggins, pp. 221-24. Dordrecht, Neth.: Springer
7. Bernacchi CJ, Bagley JE, Serbin SP, Ruiz-Vera UM, Rosenthal DM, VanLoocke A. 2013. Modelling C3 photosynthesis from the chloroplast to the ecosystem. Plant Cell Environ. 36:1641-57
8. Bernacchi CJ, Morgan PB, Ort DR, Long SP. 2005. The growth of soybean under free airCO2 enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220:434-46
9. Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP. 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
10. Berner RA. 1999. Atmospheric oxygen over Phanerozoic time. PNAS 96:10955-57
11. Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, et al. 2011. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805-9
12. Bloom AJ, Asensio JSR, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA. 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
13. Bloom AJ, Burger M, Asensio JSR, Cousins AB. 2010. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899-903
14. Bloom AJ, Burger M, Kimball BA, Pinter PJ Jr. 2014. Nitrate assimilation is inhibited by elevated CO2 in field-grown wheat. Nat. Clim. Change 4:477-80
15. Buckley TN, Mott KA, Farquhar GD. 2003. A hydromechanical and biochemical model of stomatal conductance. Plant Cell Environ. 26:1767-85
16. Bunce JA. 1988. Effects of boundary layer conductance on substomatal pressures of carbon dioxide. Plant Cell Environ. 11:205-8
17. Busch FA, Sage TL, Cousins AB, Sage RF. 2013. C3 plants enhance rates of photosynthesis by reassimilating photorespired and respired CO2. Plant Cell Environ. 36:200-12
18. Campbell G, Norman J. 1998. Introduction to Environmental Biophysics. New York: Springer
19. Cen Y-P, Sage RF. 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
20. Collatz GJ, Ball JT, Grivet C, Berry JA. 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
21. Cousins A, Bloom A. 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
22. Donner SD, Kucharik CJ. 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
23. Drake BG, Gonzàlez-Meler MA, Long SP. 1997. More efficient plants: a consequence of rising atmospheric CO2 Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:609-39
24. Drewry DT, Kumar P, Long S, Bernacchi CJ, Liang XZ, Sivapalan M. 2010. Ecohydrological responses of dense canopies to environmental variability: 1. Interplay between vertical structure and photosynthetic pathway. J. Geophys. Res. Biogeosci. 115:G04022
25. Drewry DT, Kumar P, Long S, Bernacchi CJ, Liang XZ, Sivapalan M. 2010. Ecohydrological responses of dense canopies to environmental variability: 2. Role of acclimation under elevated CO2. J. Geophys. Res. Biogeosci. 115:G001341
26. Edwards GE, Walker DA. 1983. C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis. Oxford, UK: Blackwell Sci.
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. FarquharGD,von Caemmerer S, Berry JA. 1980.Abiochemical model of photosyntheticCO2 assimilation in leaves of C3 species. Planta 149:78-90
29. FischerRA, Rees D, Sayre KD, Lu Z-M, Condon AG, Saavedra AL. 1998. Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Sci. 38:1467-75
30. Flexas J, Ribas-Carb ó M, Diaz-Espejo A, Galmés J, Medrano H. 2008. Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ. 31:602-21
31. Foley JA, Prentice IC, Ramankutty N, Levis S, Pollard D, et al. 1996. An integrated biosphere model of land surface processes, terrestrial carbon balance, and vegetation dynamics. Glob. Biogeochem. Cycles 10:603-28
32. Foyer CH, Bloom AJ, Queval G, Noctor G. 2009. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu. Rev. Plant Biol. 60:455-84
33. Green MA, Emery K, Hishikawa Y, Warta W, Dunlop ED. 2015. Solar cell efficiency tables (version 45). Prog. Photovolt. Res. Appl. 23:1-9
34. Hanning I, Heldt HW. 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
35. Hanson A, Roje S. 2001. One-carbon metabolism in higher plants. Annu. Rev. Plant Biol. 52:119-37
36. Hibberd JM, Sheehy JE, Langdale JA. 2008. Using C4 photosynthesis to increase the yield of rice- rationale and feasibility. Curr. Opin. Plant Biol. 11:228-31
37. IPCC (Intergov. Panel Clim. Change). 2013. Principles governing IPCC work. https://www.ipcc.ch/pdf/ ipcc-principles/ipcc-principles.pdf
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. 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, et al. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol. 25:593-99
41. KramerDM,Evans JR. 2011. The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155:70-78
42. Kucharik CJ. 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
43. Kucharik CJ, Brye KR. 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
44. Kucharik CJ, Foley JA, Delire C, Fisher VA, Coe MT, 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
45. Leakey 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. J. Exp. Bot. 60:2859-76
46. Lobell DB, Asner GP. 2003. Climate and management contributions to recent trends in U.S. agricultural yields. Science 299:1032
47. Lobell DB, BurkeMB.2008.Whyare agricultural impacts of climate change so uncertain The importance of temperature relative to precipitation. Environ. Res. Lett. 3:034007
48. Lobell DB, Field CB. 2007. Global scale climate-crop yield relationships and the impacts of recent warming. Environ. Res. Lett. 2:014002
49. Long SP, Ainsworth EA, LeakeyADB,Nösberger J, Ort DR. 2006. Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentrations. Science 312:1918-21
50. Maier A, Fahnenstich H, von Caemmerer S, Engqvist MK, Weber APM, et al. 2012. Glycolate oxidation in A. thaliana chloroplasts improves biomass production. Front. Plant Sci. 3:38
51. Maurino VG, Peterhansel C. 2010. Photorespiration: current status and approaches for metabolic engineering. Curr. Opin. Plant Biol. 13:248-55
52. Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, et al. 2011. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob. Change Biol. 17:2134-44
53. Michael JR, Wolfram S. 2013. Identifying supply and demand elasticities of agricultural commodities: implications for the US ethanol mandate. Am. Econ. Rev. 103:2265-95
54. Moore BD, Cheng SH, Rice J, Seemann JR. 1998. Sucrose cycling, Rubisco expression, and prediction of photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ. 21:905-15
55. Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey ADB, et al. 2014. Increasing CO2 threatens human nutrition. Nature 510:139-42
56. Ogren WL. 1984. Photorespiration: pathways, regulation, and modification. Annu. Rev. Plant Physiol. 35:415-42
57. Ort DR, Baker NR. 2002. A photoprotective role for O2 as an alternative electron sink in photosynthesis Curr. Opin. Plant Biol. 5:193-98
58. Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, et al. 2015. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. PNAS 112:8529-36
59. Peltier G, Aro E-M, Shikanai T. 2016. NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu. Rev. Plant Biol. 67:55-80
60. Peterhansel C, Blume C, Offermann S. 2013. Photorespiratory bypasses: How can they work J. Exp. Bot. 64:709-15
61. Rachmilevitch S, Cousins AB, Bloom AJ. 2004. Nitrate assimilation in plant shoots depends on photorespiration. PNAS 101:11506-10
62. Ray DK, Mueller ND, West PC, Foley JA. 2013. Yield trends are insufficient to double global crop production by 2050. PLOS ONE 8:e66428
63. Rogers A, Humphries SW. 2000. A mechanistic evaluation of photosynthetic acclimation at elevatedCO2. Glob. Change Biol. 6:1005-11
64. Ruiz-Vera UM, Siebers M, Gray SB, Drag DW, Rosenthal DM, 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
65. Sage RF, Way DA, Kubien DS. 2008. Rubisco, Rubisco activase, and global climate change. J. Exp. Bot. 59:1581-95
66. Salvucci ME, Crafts-Brandner SJ. 2004. Mechanism for deactivation of Rubisco under moderate heat stress. Physiol. Plant. 122:513-19
67. Sharkey TD. 1988. Estimating the rate of photorespiration in leaves. Physiol. Plant. 73:147-52
68. Somerville C. 1986. Analysis of photosynthesis with mutants of higher plants and algae. Annu. Rev. Plant Physiol. 37:467-506
69. Sun Y, Gu L, Dickinson RE, Norby RJ, Pallardy SG, Hoffman FM. 2014. Impact of mesophyll diffusion on estimated global land CO2 fertilization. PNAS 111:15774-79
70. Tans P. 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. 2012. Variable mesophyll conductance revisited: Theoretical background and experimental implications. Plant Cell Environ. 35:2087-103
72. Tholen D, Zhu X-G. 2011. The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion. Plant Physiol. 156:90-105
73. Thompson SL, Pollard D. 1995. A global climate model (GENESIS) with a land-surface transfer scheme (LSX). Part I: present climate simulation. J. Clim. 8:732-61
74. Thompson SL, Pollard D. 1995. A global climate model (GENESIS) with a land-surface transfer scheme (LSX). Part II: CO2 sensitivity. J. Clim. 8:1104-21
75. Tilman D, Balzer C, Hill J, Befort BL. 2011. Global food demand and the sustainable intensification of agriculture. PNAS 108:20260-64
76. von Caemmerer S. 2000. Biochemical Models of Leaf Photosynthesis. Collingwood, Aust.: CSIRO
77. von Caemmerer S. 2013. Steady-state models of photosynthesis. Plant Cell Environ. 36:1617-30
78. von Caemmerer S, Evans JR. 2015. Temperature responses of mesophyll conductance differ greatly between species. Plant Cell Environ. 38:629-37
79. von Caemmerer S, Farquhar GD. 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376-87
80. Walker BJ, Ariza LS, Kaines S, Badger MR, Cousins AB. 2013. Temperature response of in vivo Rubisco kinetics and mesophyll conductance in Arabidopsis thaliana: comparisons to Nicotiana tabacum. Plant Cell Environ. 36:2108-19
81. Walker BJ, Ort DR. 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
82. Walker BJ, Strand DD, Kramer DM, Cousins AB. 2014. The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation. Plant Physiol. 165:453-62
83. Whitney SM, Houtz RL, Alonso H. 2011. Advancing our understanding and capacity to engineer nature's CO2-sequestering enzyme, Rubisco. Plant Physiol. 155:27-35
84. Wingler A, Lea PJ, Quick WP, Leegood RC. 2000. Photorespiration: metabolic pathways and their role in stress protection. Philos. Trans. R. Soc. Lond. B 355:1517-29
85. Wolfram Res. 2015. Mathematica. Wolfram Res., Champaign, IL. http://www.wolfram.com/ mathematica
86. Xin C, Tholen D, Zhu X-G. 2014. The benefits of photorespiratory bypasses: How can they work Plant Physiol. 167:574-85
87. Yamori W, Shikanai T. 2016. Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu. Rev. Plant Biol. 67:81-106
88. Zhu X-G, Long SP, Ort DR. 2008. What is the maximum efficiency with which photosynthesis can convert solar energy into biomassCurr. Opin. Biotechnol. 19:153-59