Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions

Köhler, Iris H.; Ruiz-Vera, Ursula M.; VanLoocke, Andy; Thomey, Michell L.; Clemente, Tom; Long, Stephen P.; Ort, Donald R.; Bernacchi, Carl J.

doi:10.1093/jxb/erw435

Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions

Journal Article · Mon Dec 12 00:00:00 EST 2016 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/erw435· OSTI ID:1625388

Köhler, Iris H. ^[1]; Ruiz-Vera, Ursula M. ^[2]; ^[3]; Thomey, Michell L. ^[4]; Clemente, Tom ^[5]; ^[6]; Ort, Donald R. ^[7]; ^[7]

United States Department of Agriculture, Urbana, IL (United States). Global Change and Photosynthesis Research Unit, Agricultural Research Service; University of Illinois at Urbana-Champaign, Urbana, IL (United States). Carl R. Woese Institute for Genomic Biology; DOE/OSTI
University of Illinois at Urbana-Champaign, Urbana, IL (United States). Carl R. Woese Institute for Genomic Biology
Iowa State University, Ames, IA (United States). Department of Agronomy
United States Department of Agriculture, Urbana, IL (United States). Global Change and Photosynthesis Research Unit, Agricultural Research Service; University of Illinois at Urbana-Champaign, Urbana, IL (United States). Carl R. Woese Institute for Genomic Biology
University of Nebraska-Lincoln, Lincoln, NE (United States). Center for Plant Science Innovation
United States Department of Agriculture, Urbana, IL (United States). Global Change and Photosynthesis Research Unit, Agricultural Research Service; University of Illinois at Urbana-Champaign, Urbana, IL (United States). Carl R. Woese Institute for Genomic Biology; University of Lancaster, Lancaster (United Kingdom). Lancaster Environment Centre
United States Department of Agriculture, Urbana, IL (United States). Global Change and Photosynthesis Research Unit, Agricultural Research Service; University of Illinois at Urbana-Champaign, Urbana, IL (United States). Carl R. Woese Institute for Genomic Biology; University of Illinois at Urbana-Champaign, Urbana, IL (United States). Departments of Plant Biology and Crop Sciences

Predictions suggest that current crop production needs to double by 2050 to meet global food and energy demands. Based on theory and experimental studies, overexpression of the photosynthetic enzyme sedoheptulose-1,7-bisphosphatase (SBPase) is expected to enhance C3 crop photosynthesis and yields. Here we test how expression of the cyanobacterial, bifunctional fructose-1,6/sedoheptulose-1,7-bisphosphatase (FBP/SBPase) affects carbon assimilation and seed yield (SY) in a major crop (soybean, Glycine max). For three growing seasons, wild-type (WT) and FBP/SBPase-expressing (FS) plants were grown in the field under ambient (400 μmol mol-1) and elevated (600 μmol mol-1) CO2 concentrations [CO2] and under ambient and elevated temperatures (+2.7 °C during daytime, +3.4 °C at night) at the SoyFACE research site. Across treatments, FS plants had significantly higher carbon assimilation (4–14%), Vc,max (5–8%), and Jmax (4–8%). Under ambient [CO2], elevated temperature led to significant reductions of SY of both genotypes by 19–31%. However, under elevated [CO2] and elevated temperature, FS plants maintained SY levels, while the WT showed significant reductions between 11% and 22% compared with plants under elevated [CO2] alone. These results show that the manipulation of the photosynthetic carbon reduction cycle can mitigate the effects of future high CO2 and high temperature environments on soybean yield.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Associated Univ., Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-06OR23100

OSTI ID:: 1625388

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 3 Vol. 68; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (34)

A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species Farquhar, G. D.; von Caemmerer, S.; Berry, J. A. Planta, Vol. 149, Issue 1 https://doi.org/10.1007/bf00386231	journal	June 1980
Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants Feng, Lingling; Wang, Kun; Li, Yang Plant Cell Reports, Vol. 26, Issue 9 https://doi.org/10.1007/s00299-006-0299-y	journal	April 2007
The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity Bernacchi, Carl J.; Morgan, Patrick B.; Ort, Donald R. Planta, Vol. 220, Issue 3 https://doi.org/10.1007/s00425-004-1320-8	journal	July 2004
Investigating the role of the thiol-regulated enzyme sedoheptulose-1,7-bisphosphatase in the control of photosynthesis Raines, Christine A.; Harrison, Elizabeth P.; Olcer, Hulya Physiologia Plantarum, Vol. 110, Issue 3 https://doi.org/10.1034/j.1399-3054.2000.1100303.x	journal	November 2000
Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1, 7-bisphosphatase in tobacco enhances photosynthesis and growth Miyagawa, Yoshiko; Tamoi, Masahiro; Shigeoka, Shigeru Nature Biotechnology, Vol. 19, Issue 10 https://doi.org/10.1038/nbt1001-965	journal	October 2001
Free-air CO2 enrichment (FACE) of a poplar plantation: the POPFACE fumigation system Miglietta, Franco; Peressotti, Alessandro; Vaccari, Francesco Primo New Phytologist, Vol. 150, Issue 2 https://doi.org/10.1046/j.1469-8137.2001.00115.x	journal	May 2001
Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco Simkin, Andrew J.; McAusland, Lorna; Headland, Lauren R. Journal of Experimental Botany, Vol. 66, Issue 13 https://doi.org/10.1093/jxb/erv204	journal	May 2015
Increased Sedoheptulose-1,7-Bisphosphatase Activity in Transgenic Tobacco Plants Stimulates Photosynthesis and Growth from an Early Stage in Development Lefebvre, Stephane; Lawson, Tracy; Fryer, Mike Plant Physiology, Vol. 138, Issue 1 https://doi.org/10.1104/pp.104.055046	journal	April 2005
Increasing Photosynthetic Carbon Assimilation in C ₃ Plants to Improve Crop Yield: Current and Future Strategies Raines, Christine A. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.168559	journal	November 2010
Global Warming Can Negate the Expected CO ₂ Stimulation in Photosynthesis and Productivity for Soybean Grown in the Midwestern United States Ruiz-Vera, Ursula M.; Siebers, Matthew; Gray, Sharon B. Plant Physiology, Vol. 162, Issue 1 https://doi.org/10.1104/pp.112.211938	journal	March 2013
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement Blankenship, R. E.; Tiede, D. M.; Barber, J. Science, Vol. 332, Issue 6031, p. 805-809 https://doi.org/10.1126/science.1200165	journal	May 2011
Over-expressing the C3 photosynthesis cycle enzyme Sedoheptulose-1-7 Bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE) Rosenthal, David M.; Locke, Anna M.; Khozaei, Mahdi BMC Plant Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2229-11-123	journal	January 2011
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves von Caemmerer, S.; Farquhar, G. D. Planta, Vol. 153, Issue 4 https://doi.org/10.1007/BF00384257	journal	December 1981
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species Farquhar, G. D.; von Caemmerer, S.; Berry, J. A. Planta, Vol. 149, Issue 1 https://doi.org/10.1007/BF00386231	journal	June 1980
Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation Harrison, Elizabeth P.; Willingham, Nicola M.; Lloyd, Julie C. Planta, Vol. 204, Issue 1 https://doi.org/10.1007/s004250050226	journal	December 1997
The Calvin cycle revisited Raines, Christine A. Photosynthesis Research, Vol. 75, Issue 1, p. 1-10 https://doi.org/10.1023/A:1022421515027	journal	January 2003
Production of Transgenic Soybean Plants Using Agrobacterium-Mediated DNA Transfer Hinchee, Maud A. W.; Connor-Ward, Dannette V.; Newell, Christine A. Nature Biotechnology, Vol. 6, Issue 8 https://doi.org/10.1038/nbt0888-915	journal	August 1988
Broad range of 2050 warming from an observationally constrained large climate model ensemble Rowlands, Daniel J.; Frame, David J.; Ackerley, Duncan Nature Geoscience, Vol. 5, Issue 4 https://doi.org/10.1038/ngeo1430	journal	March 2012
Rubisco activase: an enzyme with a temperature-dependent dual function?: Temperature-dependent function of Rubisco activase Rokka, Anne; Zhang, Lixin; Aro, Eva-Mari The Plant Journal, Vol. 25, Issue 4 https://doi.org/10.1046/j.1365-313x.2001.00981.x	journal	February 2001
Biochemical Models of Leaf Photosynthesis von Caemmerer, S. https://doi.org/10.1071/9780643103405	book	January 2000
Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants Feng, Lingling; Han, Yujun; Liu, Gai Functional Plant Biology, Vol. 34, Issue 9 https://doi.org/10.1071/FP07074	journal	January 2007
Global food demand and the sustainable intensification of agriculture Tilman, D.; Balzer, C.; Hill, J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 50 https://doi.org/10.1073/pnas.1116437108	journal	November 2011
Redesigning photosynthesis to sustainably meet global food and bioenergy demand Ort, Donald R.; Merchant, Sabeeha S.; Alric, Jean Proceedings of the National Academy of Sciences, Vol. 112, Issue 28 https://doi.org/10.1073/pnas.1424031112	journal	June 2015
Expression of the gus A gene in embryogenic cell lines of Sitka spruce following Agrobacterium -mediated transformation Drake, P. M. W.; John, A.; Power, J. B. Journal of Experimental Botany, Vol. 48, Issue 1 https://doi.org/10.1093/jxb/48.1.151	journal	January 1997
Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error Long, S. P. Journal of Experimental Botany, Vol. 54, Issue 392 https://doi.org/10.1093/jxb/erg262	journal	September 2003
Optimizing the Distribution of Resources between Enzymes of Carbon Metabolism Can Dramatically Increase Photosynthetic Rate: A Numerical Simulation Using an Evolutionary Algorithm Zhu, Xin-Guang; de Sturler, Eric; Long, Stephen P. Plant Physiology, Vol. 145, Issue 2 https://doi.org/10.1104/pp.107.103713	journal	August 2007
A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism Henkes, Stefan; Sonnewald, Uwe; Badur, Ralf The Plant Cell, Vol. 13, Issue 3 https://doi.org/10.1105/tpc.13.3.535	journal	March 2001
Canopy warming caused photosynthetic acclimation and reduced seed yield in maize grown at ambient and elevated [CO ₂ ] Ruiz-Vera, Ursula M.; Siebers, Matthew H.; Drag, David W. Global Change Biology, Vol. 21, Issue 11 https://doi.org/10.1111/gcb.13013	journal	September 2015
Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle Raines, Christine A. Plant, Cell and Environment, Vol. 29, Issue 3 https://doi.org/10.1111/j.1365-3040.2005.01488.x	journal	March 2006
Accelerating yield potential in soybean: potential targets for biotechnological improvement: Targets to improve soybean yields Ainsworth, Elizabeth A.; Yendrek, Craig R.; Skoneczka, Jeffrey A. Plant, Cell & Environment, Vol. 35, Issue 1 https://doi.org/10.1111/j.1365-3040.2011.02378.x	journal	July 2011
Food for Thought: Lower-Than-Expected Crop Yield Stimulation with Rising CO2 Concentrations Long, S. P. Science, Vol. 312, Issue 5782 https://doi.org/10.1126/science.1114722	journal	June 2006
Improving Photosynthetic Efficiency for Greater Yield Zhu, Xin-Guang; Long, Stephen P.; Ort, Donald R. Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev-arplant-042809-112206	journal	June 2010
RISING ATMOSPHERIC CARBON DIOXIDE: Plants FACE the Future Long, Stephen P.; Ainsworth, Elizabeth A.; Rogers, Alistair Annual Review of Plant Biology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.arplant.55.031903.141610	journal	June 2004
OECD-FAO Agricultural Outlook 2012 No authors listed OECD-FAO Agricultural Outlook https://doi.org/10.1787/agr_outlook-2012-en	book	July 2012

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