Accelerating the development of a sustainable bioenergy portfolio through stable isotopes

Blanc‐Betes, Elena; Gomez‐Casanovas, Nuria; Yang, Wendy H.; Chandrasoma, Janith; Clark, Teresa J.; De Lucia, Evan H.; Hyde, Charles A.; Kent, Angela D.; Pett‐Ridge, Jennifer; Rabinowitz, Joshua; Raglin, Sierra S.; Schwender, Jorg; Shen, Yihui; Van Allen, Rachel; von Haden, Adam C.

doi:10.1111/gcbb.13056

Title: Accelerating the development of a sustainable bioenergy portfolio through stable isotopes

Journal Article · 27 April 2023 · Global Change Biology. Bioenergy

DOI: https://doi.org/10.1111/gcbb.13056 · OSTI ID:1968827

^[1];

^[2];

^[3];

^[4]; Clark, Teresa J. ^[5];

^[1]; Hyde, Charles A. ^[3];

^[3]; Pett‐Ridge, Jennifer ^[6]; Rabinowitz, Joshua ^[7];

^[3]; Schwender, Jorg ^[5]; Shen, Yihui ^[7]; Van Allen, Rachel ^[3];

^[8]

Univ. of Illinois at Urbana-Champaign, IL (United States); Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Texas A & M Univ., College Station, TX (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Univ. of Illinois at Urbana-Champaign, IL (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States; Princeton Univ., NJ (United States)
Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States); Univ. of Wisconsin, Madison, WI (United States)

Bioenergy could help limit global warming to 2°C above pre-industrial levels while supplying almost a fourth of the world's renewable energy needs by 2050. However, the deployment of bioenergy raises concerns that adoption at meaningful scales may lead to unintended negative environmental consequences. Meanwhile, the full consolidation of a bioenergy industry is currently challenged by a sufficient, resilient, and resource-efficient biomass supply and an effective conversion process. Here, we provide a comprehensive analysis of how stable isotope approaches have accelerated the development of a robust bioeconomy by advancing knowledge about environmental sustainability, feedstock development, and biological conversion. We show that advances in stable isotope research have generated crucial information to (1) gain mechanistic insight into the potential of bioenergy crops to mitigate climate change as well as their impact on water and nutrient cycling; (2) develop high-yielding, resilient feedstocks that produce high-value bioproducts in planta; and (3) engineer microbes to enhance feedstock conversion to bioenergy products. Further, we highlight knowledge gaps that could benefit from future research facilitated by stable isotope approaches. We conclude that advances in mechanistic knowledge and innovations within the field of stable isotopes in cross-disciplinary research actions will greatly contribute to breaking down the barriers to establishing a robust bioeconomy.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344; SC0018420; SC0012704

OSTI ID:: 1968827

Alternate ID(s):: OSTI ID: 2449719

Report Number(s):: LLNL-JRNL-854330; BNL-224198-2023-JAAM; 1082195

Journal Information:: Global Change Biology. Bioenergy, Vol. 15, Issue 7; ISSN 1757-1693

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (143)

Partitioning of evapotranspiration using a stable isotope technique in an arid and high temperature agricultural production system Lu, Xuefei; Liang, Liyin L.; Wang, Lixin Agricultural Water Management, Vol. 179 https://doi.org/10.1016/j.agwat.2016.08.012	journal	January 2017
Nitrous oxide emissions during establishment of eight alternative cellulosic bioenergy cropping systems in the North Central United States Oates, Lawrence G.; Duncan, David S.; Gelfand, Ilya GCB Bioenergy, Vol. 8, Issue 3 https://doi.org/10.1111/gcbb.12268	journal	May 2015
Long‐term yields in annual and perennial bioenergy crops in the Midwestern United States Kantola, Ilsa B.; Masters, Michael D.; Blanc‐Betes, Elena GCB Bioenergy https://doi.org/10.1111/gcbb.12940	journal	April 2022
Comparative Biogeochemical Cycles of Bioenergy Crops Reveal Nitrogen-Fixation and Low Greenhouse Gas Emissions in a Miscanthus × giganteus Agro-Ecosystem Davis, Sarah C.; Parton, William J.; Dohleman, Frank G. Ecosystems, Vol. 13, Issue 1 https://doi.org/10.1007/s10021-009-9306-9	journal	December 2009
Is switchgrass good for carbon savings? Long‐term results in marginal land Zegada‐Lizarazu, Walter; Zanetti, Federica; Di Virgilio, Nicola GCB Bioenergy, Vol. 14, Issue 7 https://doi.org/10.1111/gcbb.12944	journal	April 2022
Land use change to bioenergy: A meta-analysis of soil carbon and GHG emissions Harris, Z. M.; Spake, R.; Taylor, G. Biomass and Bioenergy, Vol. 82 https://doi.org/10.1016/j.biombioe.2015.05.008	journal	November 2015
Beyond denitrification: The role of microbial diversity in controlling nitrous oxide reduction and soil nitrous oxide emissions Shan, Jun; Sanford, Robert A.; Chee‐Sanford, Joanne Global Change Biology, Vol. 27, Issue 12 https://doi.org/10.1111/gcb.15545	journal	March 2021
Winter precipitation and snow accumulation drive the methane sink or source strength of Arctic tussock tundra Blanc-Betes, Elena; Welker, Jeffrey M.; Sturchio, Neil C. Global Change Biology, Vol. 22, Issue 8 https://doi.org/10.1111/gcb.13242	journal	May 2016
Microbial extracellular polysaccharide production and aggregate stability controlled by switchgrass (Panicum virgatum) root biomass and soil water potential Sher, Yonatan; Baker, Nameer R.; Herman, Don Soil Biology and Biochemistry, Vol. 143 https://doi.org/10.1016/j.soilbio.2020.107742	journal	April 2020
Nutrient management and bioaugmentation interactively shape plant–microbe interactions in Miscanthus × giganteus Kane, Jennifer L.; Robinson, Marshall C.; Schartiger, Ronald G. GCB Bioenergy, Vol. 14, Issue 11 https://doi.org/10.1111/gcbb.13000	journal	September 2022
Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects Blagodatskaya, E.; Yuyukina, T.; Blagodatsky, S. Soil Biology and Biochemistry, Vol. 43, Issue 4 https://doi.org/10.1016/j.soilbio.2010.12.011	journal	April 2011
Looking back to look ahead: a vision for soil denitrification research Almaraz, Maya; Wong, Michelle Y.; Yang, Wendy H. Ecology, Vol. 101, Issue 1 https://doi.org/10.1002/ecy.2917	journal	November 2019
The influence of drought and heat stress on long-term carbon fluxes of bioenergy crops grown in the Midwestern USA: Drought effect on carbon fluxes Joo, Eva; Hussain, Mir Zaman; Zeri, Marcelo Plant, Cell & Environment, Vol. 39, Issue 9 https://doi.org/10.1111/pce.12751	journal	June 2016
Strain improvement by metabolic engineering: lysine production as a case study for systems biology Koffas, Mattheos; Stephanopoulos, Gregory Current Opinion in Biotechnology, Vol. 16, Issue 3 https://doi.org/10.1016/j.copbio.2005.04.010	journal	June 2005
Water-Use Efficiency: Advances and Challenges in a Changing Climate Hatfield, Jerry L.; Dold, Christian Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00103	journal	February 2019
Enhanced biofuel production through coupled acetic acid and xylose consumption by engineered yeast Wei, Na; Quarterman, Josh; Kim, Soo Rin Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3580	journal	October 2013
BECCS capability of dedicated bioenergy crops under a future land‐use scenario targeting net negative carbon emissions Kato, Etsushi; Yamagata, Yoshiki Earth's Future, Vol. 2, Issue 9 https://doi.org/10.1002/2014EF000249	journal	September 2014
Stable Isotopes in Plant Ecology Dawson, Todd E.; Mambelli, Stefania; Plamboeck, Agneta H. Annual Review of Ecology and Systematics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.ecolsys.33.020602.095451	journal	November 2002
More Productive Than Maize in the Midwest: How Does Miscanthus Do It? Dohleman, Frank G.; Long, Stephen P. Plant Physiology, Vol. 150, Issue 4 https://doi.org/10.1104/pp.109.139162	journal	June 2009
Consensus, uncertainties and challenges for perennial bioenergy crops and land use Whitaker, Jeanette; Field, John L.; Bernacchi, Carl J. GCB Bioenergy, Vol. 10, Issue 3 https://doi.org/10.1111/gcbb.12488	journal	November 2017
Changes in soil carbon stocks under perennial and annual bioenergy crops Ferchaud, Fabien; Vitte, Guillaume; Mary, Bruno GCB Bioenergy, Vol. 8, Issue 2 https://doi.org/10.1111/gcbb.12249	journal	March 2015
Responsiveness of miscanthus and switchgrass yields to stand age and nitrogen fertilization: A meta‐regression analysis Sharma, Bijay P.; Zhang, Na; Lee, DoKyoung GCB Bioenergy, Vol. 14, Issue 5 https://doi.org/10.1111/gcbb.12929	journal	March 2022
Metabolite pools and carbon flow during C ₄ photosynthesis in maize: ¹³ CO ₂ labeling kinetics and cell type fractionation Arrivault, Stéphanie; Obata, Toshihiro; Szecówka, Marek Journal of Experimental Botany, Vol. 68, Issue 2 https://doi.org/10.1093/jxb/erw414	journal	November 2016
Estimation of Biological Nitrogen Fixation Associated with 11 Ecotypes of Panicum maximum Grown in Nitrogen‐15‐labeled Soil¹ Miranda, Cesar H. Behling; Boddey, Robert M. Agronomy Journal, Vol. 79, Issue 3 https://doi.org/10.2134/agronj1987.00021962007900030032x	journal	May 1987
Isotopically nonstationary ¹³ C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation Ma, Fangfang; Jazmin, Lara J.; Young, Jamey D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 47 https://doi.org/10.1073/pnas.1319485111	journal	November 2014
Seasonal Controls of CO ₂ and CH ₄ Dynamics in a Temporarily Flooded Subtropical Wetland Gomez‐Casanovas, Nuria; DeLucia, Nicholas J.; DeLucia, Evan H. Journal of Geophysical Research: Biogeosciences, Vol. 125, Issue 3 https://doi.org/10.1029/2019JG005257	journal	March 2020
Conversion of Escherichia coli to Generate All Biomass Carbon from CO2 Gleizer, Shmuel; Ben-Nissan, Roee; Bar-On, Yinon M. Cell, Vol. 179, Issue 6 https://doi.org/10.1016/j.cell.2019.11.009	journal	November 2019
Drying times: plant traits to improve crop water use efficiency and yield Condon, Anthony G. Journal of Experimental Botany, Vol. 71, Issue 7 https://doi.org/10.1093/jxb/eraa002	journal	January 2020
Impact of synthetic biology and metabolic engineering on industrial production of fine chemicals Jullesson, David; David, Florian; Pfleger, Brian Biotechnology Advances, Vol. 33, Issue 7 https://doi.org/10.1016/j.biotechadv.2015.02.011	journal	November 2015
isocalcR: An R package to streamline and standardize stable isotope calculations in ecological research Mathias, Justin M.; Hudiburg, Tara W. Global Change Biology, Vol. 28, Issue 24 https://doi.org/10.1111/gcb.16407	journal	September 2022
Global agriculture and nitrous oxide emissions Reay, Dave S.; Davidson, Eric A.; Smith, Keith A. Nature Climate Change, Vol. 2, Issue 6 https://doi.org/10.1038/nclimate1458	journal	May 2012
The global value of water in agriculture D’Odorico, Paolo; Chiarelli, Davide Danilo; Rosa, Lorenzo Proceedings of the National Academy of Sciences, Vol. 117, Issue 36, p. 21985-21993 https://doi.org/10.1073/pnas.2005835117	journal	August 2020
Functional differences in the microbial processing of recent assimilates under two contrasting perennial bioenergy plantations Elias, Dafydd M. O.; Rowe, Rebecca L.; Pereira, M. Glória Soil Biology and Biochemistry, Vol. 114 https://doi.org/10.1016/j.soilbio.2017.07.026	journal	November 2017
Nitrous oxide emissions from agricultural soils challenge climate sustainability in the US Corn Belt Lawrence, Nathaniel C.; Tenesaca, Carlos G.; VanLoocke, Andy Proceedings of the National Academy of Sciences, Vol. 118, Issue 46 https://doi.org/10.1073/pnas.2112108118	journal	November 2021
Using 15N tracers to estimate N2O and N2 emissions from nitrification and denitrification in coastal plain wetlands under contrasting land-uses Morse, Jennifer L.; Bernhardt, Emily S. Soil Biology and Biochemistry, Vol. 57 https://doi.org/10.1016/j.soilbio.2012.07.025	journal	February 2013
Accumulation of C4‐carbon from Miscanthus in organic‐matter‐rich soils Leifeld, Jens; Alewell, Christine; Paul, Sonja M. GCB Bioenergy, Vol. 13, Issue 8 https://doi.org/10.1111/gcbb.12861	journal	June 2021
Enlisting wild grass genes to combat nitrification in wheat farming: A nature-based solution Subbarao, Guntur V.; Kishii, Masahiro; Bozal-Leorri, Adrian Proceedings of the National Academy of Sciences, Vol. 118, Issue 35 https://doi.org/10.1073/pnas.2106595118	journal	August 2021
Bioenergy for climate change mitigation: Scale and sustainability Calvin, Katherine; Cowie, Annette; Berndes, Göran GCB Bioenergy, Vol. 13, Issue 9 https://doi.org/10.1111/gcbb.12863	journal	July 2021
Metabolic engineering for enhanced oil in biomass Vanhercke, Thomas; Dyer, John M.; Mullen, Robert T. Progress in Lipid Research, Vol. 74 https://doi.org/10.1016/j.plipres.2019.02.002	journal	April 2019
Associative nitrogen fixation linked with three perennial bioenergy grasses in field and greenhouse experiments Wewalwela, Jayani J.; Tian, Yuan; Donaldson, Janet R. GCB Bioenergy, Vol. 12, Issue 12 https://doi.org/10.1111/gcbb.12744	journal	October 2020
Emissions of methane and nitrous oxide from Australian sugarcane soils Denmead, O. T.; Macdonald, B. C. T.; Bryant, G. Agricultural and Forest Meteorology, Vol. 150, Issue 6 https://doi.org/10.1016/j.agrformet.2009.06.018	journal	June 2010
Metabolic flux elucidation for large-scale models using 13C labeled isotopes Suthers, Patrick F.; Burgard, Anthony P.; Dasika, Madhukar S. Metabolic Engineering, Vol. 9, Issue 5-6 https://doi.org/10.1016/j.ymben.2007.05.005	journal	September 2007
Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways Li, Hui; Bölscher, Tobias; Winnick, Matthew Environmental Science & Technology, Vol. 55, Issue 5 https://doi.org/10.1021/acs.est.0c04592	journal	February 2021
Dynamics of Nitrogen Uptake and Mobilization in Field-grown Winter Oilseed Rape (Brassica napus) From Stem Extension to Harvest. II. An 15N-labelling-based Simulation Model of N Partitioning Between Vegetative and Reproductive Tissues Malagoli, P.; Laine, P.; Rossato, L. Annals of Botany, Vol. 95, Issue 7 https://doi.org/10.1093/aob/mci131	journal	March 2005
A review of approaches for evapotranspiration partitioning Kool, D.; Agam, N.; Lazarovitch, N. Agricultural and Forest Meteorology, Vol. 184 https://doi.org/10.1016/j.agrformet.2013.09.003	journal	January 2014
Marginal land conversion to perennial energy crops with biomass removal enhances soil carbon sequestration Xu, Yi; Zhou, Jie; Feng, Wenhao GCB Bioenergy, Vol. 14, Issue 10 https://doi.org/10.1111/gcbb.12990	journal	August 2022
Soil carbon debt of 12,000 years of human land use Sanderman, Jonathan; Hengl, Tomislav; Fiske, Gregory J. Proceedings of the National Academy of Sciences, Vol. 114, Issue 36 https://doi.org/10.1073/pnas.1706103114	journal	August 2017
Effects of switchgrass cultivars and intraspecific differences in root structure on soil carbon inputs and accumulation Adkins, Jaron; Jastrow, Julie D.; Morris, Geoffrey P. Geoderma, Vol. 262 https://doi.org/10.1016/j.geoderma.2015.08.019	journal	January 2016
In silico assessment of the potential of basalt amendments to reduce N ₂ O emissions from bioenergy crops Blanc‐Betes, Elena; Kantola, Ilsa B.; Gomez‐Casanovas, Nuria GCB Bioenergy, Vol. 13, Issue 1 https://doi.org/10.1111/gcbb.12757	journal	November 2020
Differential priming of soil carbon driven by soil depth and root impacts on carbon availability de Graaff, Marie-Anne; Jastrow, Julie D.; Gillette, Shay Soil Biology and Biochemistry, Vol. 69 https://doi.org/10.1016/j.soilbio.2013.10.047	journal	February 2014
What can we learn from N₂O isotope data? – Analytics, processes and modelling Yu, Longfei; Harris, Eliza; Lewicka‐Szczebak, Dominika Rapid Communications in Mass Spectrometry, Vol. 34, Issue 20 https://doi.org/10.1002/rcm.8858	journal	August 2020
Fertilizer placement to improve crop nutrient acquisition and yield: A review and meta-analysis Nkebiwe, Peteh Mehdi; Weinmann, Markus; Bar-Tal, Asher Field Crops Research, Vol. 196 https://doi.org/10.1016/j.fcr.2016.07.018	journal	September 2016
Plant identity control on soil food web structure and C transfers under perennial bioenergy plantations Briones, M. J. I.; Elias, D. M. O.; Grant, H. K. Soil Biology and Biochemistry, Vol. 138 https://doi.org/10.1016/j.soilbio.2019.107603	journal	November 2019
The glucose 6-phosphate shunt around the Calvin–Benson cycle Sharkey, Thomas D.; Weise, Sean E. Journal of Experimental Botany, Vol. 67, Issue 14 https://doi.org/10.1093/jxb/erv484	journal	November 2015
Sugar Synthesis from CO2 in Escherichia coli Antonovsky, Niv; Gleizer, Shmuel; Noor, Elad Cell, Vol. 166, Issue 1 https://doi.org/10.1016/j.cell.2016.05.064	journal	June 2016
Quantifying the effects of switchgrass ( Panicum virgatum ) on deep organic C stocks using natural abundance ¹⁴ C in three marginal soils Slessarev, Eric W.; Nuccio, Erin E.; McFarlane, Karis J. GCB Bioenergy, Vol. 12, Issue 10 https://doi.org/10.1111/gcbb.12729	journal	August 2020
Nitrogen deposition and greenhouse gas emissions from grasslands: uncertainties and future directions Gomez-Casanovas, Nuria; Hudiburg, Tara W.; Bernacchi, Carl J. Global Change Biology, Vol. 22, Issue 4 https://doi.org/10.1111/gcb.13187	journal	February 2016
Rewiring the microbial metabolic network for efficient utilization of mixed carbon sources An, Ning; Chen, Xin; Sheng, Huakang Journal of Industrial Microbiology and Biotechnology, Vol. 48, Issue 9-10 https://doi.org/10.1093/jimb/kuab040	journal	July 2021
Overcoming the metabolic burden of protein secretion in Schizosaccharomyces pombe – A quantitative approach using 13C-based metabolic flux analysis Klein, Tobias; Lange, Sabrina; Wilhelm, Nadine Metabolic Engineering, Vol. 21 https://doi.org/10.1016/j.ymben.2013.11.001	journal	January 2014
Changes in soil organic carbon under perennial crops Ledo, Alicia; Smith, Pete; Zerihun, Ayalsew Global Change Biology, Vol. 26, Issue 7 https://doi.org/10.1111/gcb.15120	journal	May 2020
Biophysical and economic limits to negative CO2 emissions Smith, Pete; Davis, Steven J.; Creutzig, Felix Nature Climate Change, Vol. 6, Issue 1 https://doi.org/10.1038/nclimate2870	journal	December 2015
13C metabolic flux analysis at a genome-scale Gopalakrishnan, Saratram; Maranas, Costas D. Metabolic Engineering, Vol. 32 https://doi.org/10.1016/j.ymben.2015.08.006	journal	November 2015
A Method to Constrain Genome-Scale Models with 13C Labeling Data García Martín, Héctor; Kumar, Vinay Satish; Weaver, Daniel PLOS Computational Biology, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pcbi.1004363	journal	September 2015
Land use change from C3 grassland to C4 Miscanthus : effects on soil carbon content and estimated mitigation benefit after six years Zatta, Alessandro; Clifton-Brown, John; Robson, Paul GCB Bioenergy, Vol. 6, Issue 4 https://doi.org/10.1111/gcbb.12054	journal	April 2013
A review of transformative strategies for climate mitigation by grasslands Gomez-Casanovas, Nuria; Blanc-Betes, Elena; Moore, Caitlin E. Science of The Total Environment, Vol. 799 https://doi.org/10.1016/j.scitotenv.2021.149466	journal	December 2021
The Global Distribution of Biological Nitrogen Fixation in Terrestrial Natural Ecosystems Davies‐Barnard, T.; Friedlingstein, P. Global Biogeochemical Cycles, Vol. 34, Issue 3 https://doi.org/10.1029/2019GB006387	journal	March 2020
Using alternative forage species to reduce emissions of the greenhouse gas nitrous oxide from cattle urine deposited onto soil Luo, J.; Balvert, S. F.; Wise, B. Science of The Total Environment, Vol. 610-611 https://doi.org/10.1016/j.scitotenv.2017.08.186	journal	January 2018
Transpiration efficiency: new insights into an old story Vadez, Vincent; Kholova, Jana; Medina, Susan Journal of Experimental Botany, Vol. 65, Issue 21 https://doi.org/10.1093/jxb/eru040	journal	March 2014
Application of Stable Isotope Tracing to Elucidate Metabolic Dynamics During Yarrowia lipolytica α-Ionone Fermentation Czajka, Jeffrey J.; Kambhampati, Shrikaar; Tang, Yinjie J. iScience, Vol. 23, Issue 2 https://doi.org/10.1016/j.isci.2020.100854	journal	February 2020
Soil Organic Carbon Isotope Tracing in Sorghum under Ambient CO2 and Free-Air CO2 Enrichment (FACE) Leavitt, Steven; Cheng, Li; Williams, David Land, Vol. 11, Issue 2 https://doi.org/10.3390/land11020309	journal	February 2022
The metabolic origins of non-photorespiratory CO2 release during photosynthesis: a metabolic flux analysis Xu, Yuan; Fu, Xinyu; Sharkey, Thomas D. Plant Physiology, Vol. 186, Issue 1 https://doi.org/10.1093/plphys/kiab076	journal	February 2021
Robust paths to net greenhouse gas mitigation and negative emissions via advanced biofuels Field, John L.; Richard, Tom L.; Smithwick, Erica A. H. Proceedings of the National Academy of Sciences, Vol. 117, Issue 36 https://doi.org/10.1073/pnas.1920877117	journal	August 2020
Measuring techniques for concentration and stable isotopologues of CO2 in a terrestrial ecosystem: A review Voglar, Grega E.; Zavadlav, Saša; Levanič, Tom Earth-Science Reviews, Vol. 199 https://doi.org/10.1016/j.earscirev.2019.102978	journal	December 2019
Cover crop root contributions to soil carbon in a no-till corn bioenergy cropping system Austin, Emily E.; Wickings, Kyle; McDaniel, Marshall D. GCB Bioenergy, Vol. 9, Issue 7 https://doi.org/10.1111/gcbb.12428	journal	January 2017
Carbon isotopes and water use efficiency in C4 plants Ellsworth, Patrick Z.; Cousins, Asaph B. Current Opinion in Plant Biology, Vol. 31 https://doi.org/10.1016/j.pbi.2016.04.006	journal	June 2016
Short‐term effects of bioenergy cropping on soil carbon and nitrogen dynamics in a Florida Ultisol Silveira, M. L.; Brandani, C. B.; Kohmann, M. M. Soil Science Society of America Journal, Vol. 84, Issue 4 https://doi.org/10.1002/saj2.20081	journal	July 2020
Phosphoketolase pathway contributes to carbon metabolism in cyanobacteria Xiong, Wei; Lee, Tai-Chi; Rommelfanger, Sarah Nature Plants, Vol. 2, Issue 1, Article No. 15187 https://doi.org/10.1038/nplants.2015.187	journal	December 2015
Kinetic flux profiling for quantitation of cellular metabolic fluxes Yuan, Jie; Bennett, Bryson D.; Rabinowitz, Joshua D. Nature Protocols, Vol. 3, Issue 8 https://doi.org/10.1038/nprot.2008.131	journal	July 2008
Analyzing Mass Spectrometry Imaging Data of 13C-Labeled Phospholipids in Camelina sativa and Thlaspi arvense (Pennycress) Embryos Romsdahl, Trevor B.; Kambhampati, Shrikaar; Koley, Somnath Metabolites, Vol. 11, Issue 3 https://doi.org/10.3390/metabo11030148	journal	March 2021
Separating Soil Respiration into Plant and Soil Components Using Analyses of the Natural Abundance of Carbon-13 Rochette, P.; Flanagan, L. B.; Gregorich, E. G. Soil Science Society of America Journal, Vol. 63, Issue 5 https://doi.org/10.2136/sssaj1999.6351207x	journal	January 1999
Physiological and agronomic approaches for improving water-use efficiency in crop plants Farooq, Muhammad; Hussain, Mubshar; Ul-Allah, Sami Agricultural Water Management, Vol. 219 https://doi.org/10.1016/j.agwat.2019.04.010	journal	June 2019
The oxidative pentose phosphate pathway is the primary source of NADPH for lipid overproduction from glucose in Yarrowia lipolytica Wasylenko, Thomas M.; Ahn, Woo Suk; Stephanopoulos, Gregory Metabolic Engineering, Vol. 30 https://doi.org/10.1016/j.ymben.2015.02.007	journal	July 2015
Reduced Nitrogen Losses after Conversion of Row Crop Agriculture to Perennial Biofuel Crops Smith, Candice M.; David, Mark B.; Mitchell, Corey A. Journal of Environment Quality, Vol. 42, Issue 1 https://doi.org/10.2134/jeq2012.0210	journal	January 2013
The seeds of green energy: Expanding the contribution of plant oils as biofuels Ohlrogge, John; Chapman, Kent The Biochemist, Vol. 33, Issue 2 https://doi.org/10.1042/BIO03302034	journal	April 2011
The future of bioenergy Reid, Walter V.; Ali, Mariam K.; Field, Christopher B. Global Change Biology, Vol. 26, Issue 1 https://doi.org/10.1111/gcb.14883	journal	December 2019
Challenges and opportunities for mitigating nitrous oxide emissions from fertilized cropping systems Venterea, Rodney T.; Halvorson, Ardell D.; Kitchen, Newell Frontiers in Ecology and the Environment, Vol. 10, Issue 10 https://doi.org/10.1890/120062	journal	December 2012
15N Natural Abundance Evidences a Better Use of N Sources by Late Nitrogen Application in Bread Wheat Fuertes-Mendizábal, Teresa; Estavillo, José M.; Duñabeitia, Miren K. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00853	journal	June 2018
Stable isotopes Ehleringer, James R.; Osmond, C. Barry Plant Physiological Ecology https://doi.org/10.1007/978-94-010-9013-1_13	book	January 2000
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
Conversion of grazed pastures to energy cane as a biofuel feedstock alters the emission of GHGs from soils in Southeastern United States Gomez-Casanovas, Nuria; DeLucia, Nicholas J.; Hudiburg, Tara W. Biomass and Bioenergy, Vol. 108 https://doi.org/10.1016/j.biombioe.2017.11.020	journal	January 2018
Greater microbial carbon use efficiency and carbon sequestration in soils: Amendment of biochar versus crop straws Liu, Zhiwei; Wu, Xiulan; Liu, Wei GCB Bioenergy, Vol. 12, Issue 12 https://doi.org/10.1111/gcbb.12763	journal	October 2020
Evaluation of carbon isotope flux partitioning theory under simplified and controlled environmental conditions Fassbinder, Joel J.; Griffis, Timothy J.; Baker, John M. Agricultural and Forest Meteorology, Vol. 153 https://doi.org/10.1016/j.agrformet.2011.09.020	journal	February 2012
Nutrient Imbalances in Agricultural Development Vitousek, P. M.; Naylor, R.; Crews, T. Science, Vol. 324, Issue 5934 https://doi.org/10.1126/science.1170261	journal	June 2009
Associative nitrogen fixation (ANF) in switchgrass (Panicum virgatum) across a nitrogen input gradient Roley, Sarah S.; Duncan, David S.; Liang, Di PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0197320	journal	June 2018
A quantitative review comparing the yields of two candidate C4 perennial biomass crops in relation to nitrogen, temperature and water Heaton, E. Biomass and Bioenergy, Vol. 27, Issue 1 https://doi.org/10.1016/j.biombioe.2003.10.005	journal	July 2004
Micro-scale resolution of carbon turnover in soil - Insights from laser ablation isotope ratio mass spectrometry on water-glass embedded aggregates Vergara Sosa, Manuel; Lehndorff, Eva; Rodionov, Andrei Soil Biology and Biochemistry, Vol. 159 https://doi.org/10.1016/j.soilbio.2021.108279	journal	August 2021
2H and 13C metabolic flux analysis elucidates in vivo thermodynamics of the ED pathway in Zymomonas mobilis Jacobson, Tyler B.; Adamczyk, Paul A.; Stevenson, David M. Metabolic Engineering, Vol. 54 https://doi.org/10.1016/j.ymben.2019.05.006	journal	July 2019
Understanding Plant Nitrogen Metabolism through Metabolomics and Computational Approaches Beatty, Perrin; Klein, Matthias; Fischer, Jeffrey Plants, Vol. 5, Issue 4 https://doi.org/10.3390/plants5040039	journal	October 2016
Contribution of nitrogen fixation to first year Miscanthus × giganteus Keymer, Daniel P.; Kent, Angela D. GCB Bioenergy, Vol. 6, Issue 5 https://doi.org/10.1111/gcbb.12095	journal	July 2013
Betting on negative emissions Fuss, Sabine; Canadell, Josep G.; Peters, Glen P. Nature Climate Change, Vol. 4, Issue 10 https://doi.org/10.1038/nclimate2392	journal	September 2014
Mechanisms underlying limited soil carbon gains in perennial and cover‐cropped bioenergy systems revealed by stable isotopes Ye, Chenglong; Hall, Steven J. GCB Bioenergy, Vol. 12, Issue 1 https://doi.org/10.1111/gcbb.12657	journal	October 2019
Engineered Assimilation of Exogenous and Endogenous Formate in Escherichia coli Yishai, Oren; Goldbach, Leander; Tenenboim, Hezi ACS Synthetic Biology, Vol. 6, Issue 9 https://doi.org/10.1021/acssynbio.7b00086	journal	June 2017
Metabolic Fluxes in an Illuminated Arabidopsis Rosette Szecowka, Marek; Heise, Robert; Tohge, Takayuki The Plant Cell, Vol. 25, Issue 2 https://doi.org/10.1105/tpc.112.106989	journal	February 2013
In Situ Quantification of Biological N ₂ Production Using Naturally Occurring ¹⁵ N ¹⁵ N Yeung, Laurence Y.; Haslun, Joshua A.; Ostrom, Nathaniel E. Environmental Science & Technology, Vol. 53, Issue 9 https://doi.org/10.1021/acs.est.9b00812	journal	April 2019
INCA: a computational platform for isotopically non-stationary metabolic flux analysis Young, J. D. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu015	journal	January 2014
Priming of soil organic carbon induced by sugarcane residues and its biochar control the source of nitrogen for plant uptake: A dual 13C and 15N isotope three-source-partitioning study Weng, Zhe (Han); Liu, Xihui; Eldridge, Simon Soil Biology and Biochemistry, Vol. 146 https://doi.org/10.1016/j.soilbio.2020.107792	journal	July 2020
Climate-smart soils Paustian, Keith; Lehmann, Johannes; Ogle, Stephen Nature, Vol. 532, Issue 7597 https://doi.org/10.1038/nature17174	journal	April 2016
Elucidation of Triacylglycerol Overproduction in the C4 Bioenergy Crop Sorghum bicolor by Constraint-Based Analysis Clark, Teresa J.; Schwender, Jorg Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.787265	journal	February 2022
Greenhouse gas emissions from soils—A review Oertel, Cornelius; Matschullat, Jörg; Zurba, Kamal Geochemistry, Vol. 76, Issue 3 https://doi.org/10.1016/j.chemer.2016.04.002	journal	October 2016
Evapotranspiration partitioning at the ecosystem scale using the stable isotope method—A review Xiao, Wei; Wei, Zhongwang; Wen, Xuefa Agricultural and Forest Meteorology, Vol. 263 https://doi.org/10.1016/j.agrformet.2018.09.005	journal	December 2018
New high precision approach for measuring 15N–N2 gas fluxes from terrestrial ecosystems Yang, Wendy H.; McDowell, Andrew C.; Brooks, Paul D. Soil Biology and Biochemistry, Vol. 69 https://doi.org/10.1016/j.soilbio.2013.11.009	journal	February 2014
Application of isotope labeling experiments and 13C flux analysis to enable rational pathway engineering McAtee, Allison G.; Jazmin, Lara J.; Young, Jamey D. Current Opinion in Biotechnology, Vol. 36 https://doi.org/10.1016/j.copbio.2015.08.004	journal	December 2015
Optknock: A bilevel programming framework for identifying gene knockout strategies for microbial strain optimization Burgard, Anthony P.; Pharkya, Priti; Maranas, Costas D. Biotechnology and Bioengineering, Vol. 84, Issue 6 https://doi.org/10.1002/bit.10803	journal	October 2003
Metabolic flux analysis of the non-transitory starch tradeoff for lipid production in mature tobacco leaves Chu, Kevin L.; Koley, Somnath; Jenkins, Lauren M. Metabolic Engineering, Vol. 69 https://doi.org/10.1016/j.ymben.2021.12.003	journal	January 2022
Methane production and oxidation potentials along a fen‐bog gradient from southern boreal to subarctic peatlands in Finland Zhang, Hui; Tuittila, Eeva‐Stiina; Korrensalo, Aino Global Change Biology, Vol. 27, Issue 18 https://doi.org/10.1111/gcb.15740	journal	June 2021
Emerging approaches to measure photosynthesis from the leaf to the ecosystem Siebers, Matthew H.; Gomez-Casanovas, Nuria; Fu, Peng Emerging Topics in Life Sciences, Vol. 5, Issue 2 https://doi.org/10.1042/ETLS20200292	journal	February 2021
An improved isotopic method for partitioning net ecosystem–atmosphere CO2 exchange Wehr, R.; Saleska, S. R. Agricultural and Forest Meteorology, Vol. 214-215 https://doi.org/10.1016/j.agrformet.2015.09.009	journal	December 2015
Changes in Respiratory Mitochondrial Machinery and Cytochrome and Alternative Pathway Activities in Response to Energy Demand Underlie the Acclimation of Respiration to Elevated CO₂ in the Invasive Opuntia ficus-indica Gomez-Casanovas, Nuria; Blanc-Betes, Elena; Gonzalez-Meler, Miquel A. Plant Physiology, Vol. 145, Issue 1 https://doi.org/10.1104/pp.107.103911	journal	July 2007
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
Commentary: Why don’t plant leaves get fat? Chapman, Kent D.; Dyer, John M.; Mullen, Robert T. Plant Science, Vol. 207 https://doi.org/10.1016/j.plantsci.2013.03.003	journal	June 2013
Pathways of soil organic matter formation from above and belowground inputs in a Sorghum bicolor bioenergy crop Fulton-Smith, Sarah; Cotrufo, M. Francesca GCB Bioenergy, Vol. 11, Issue 8 https://doi.org/10.1111/gcbb.12598	journal	February 2019
13C Metabolic Flux Analysis Wiechert, Wolfgang Metabolic Engineering, Vol. 3, Issue 3 https://doi.org/10.1006/mben.2001.0187	journal	July 2001
Nitrogen Fixation in Wheat Provided by Klebsiella pneumoniae 342 Iniguez, A. Leonardo; Dong, Yuemei; Triplett, Eric W. Molecular Plant-Microbe Interactions, Vol. 17, Issue 10 https://doi.org/10.1094/MPMI.2004.17.10.1078	journal	October 2004
Tracing the flow of carbon dioxide and water vapor between the biosphere and atmosphere: A review of optical isotope techniques and their application Griffis, Timothy J. Agricultural and Forest Meteorology, Vol. 174-175 https://doi.org/10.1016/j.agrformet.2013.02.009	journal	June 2013
OptForce: An Optimization Procedure for Identifying All Genetic Manipulations Leading to Targeted Overproductions Ranganathan, Sridhar; Suthers, Patrick F.; Maranas, Costas D. PLoS Computational Biology, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pcbi.1000744	journal	April 2010
A new bioenergy model that simulates the impacts of plant‐microbial interactions, soil carbon protection, and mechanistic tillage on soil carbon cycling Juice, Stephanie M.; Walter, Christopher A.; Allen, Kara E. GCB Bioenergy, Vol. 14, Issue 3 https://doi.org/10.1111/gcbb.12914	journal	January 2022
Bioenergy Underground: Challenges and opportunities for phenotyping roots and the microbiome for sustainable bioenergy crop production York, Larry M.; Cumming, Jonathan R.; Trusiak, Adrianna The Plant Phenome Journal, Vol. 5, Issue 1 https://doi.org/10.1002/ppj2.20028	journal	January 2022
Elementary metabolite units (EMU): A novel framework for modeling isotopic distributions Antoniewicz, Maciek R.; Kelleher, Joanne K.; Stephanopoulos, Gregory Metabolic Engineering, Vol. 9, Issue 1 https://doi.org/10.1016/j.ymben.2006.09.001	journal	January 2007
Non-Targeted Metabolomics Reveals Sorghum Rhizosphere-Associated Exudates are Influenced by the Belowground Interaction of Substrate and Sorghum Genotype Miller, Sarah B.; Heuberger, Adam L.; Broeckling, Corey D. International Journal of Molecular Sciences, Vol. 20, Issue 2 https://doi.org/10.3390/ijms20020431	journal	January 2019
Carbon Sequestration under Irrigated Switchgrass ( L.) Production Collins, H. P.; Smith, J. L.; Fransen, S. Soil Science Society of America Journal, Vol. 74, Issue 6 https://doi.org/10.2136/sssaj2010.0020	journal	January 2010
Challenges in Engineering Microbes for Biofuels Production Stephanopoulos, Gregory Science, Vol. 315, Issue 5813, p. 801-804 https://doi.org/10.1126/science.1139612	journal	February 2007
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K. Global Change Biology, Vol. 19, Issue 5 https://doi.org/10.1111/gcb.12131	journal	February 2013
Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis Young, Jamey D.; Shastri, Avantika A.; Stephanopoulos, Gregory Metabolic Engineering, Vol. 13, Issue 6 https://doi.org/10.1016/j.ymben.2011.08.002	journal	November 2011
Recent advances in domesticating non‐model microorganisms Fatma, Zia; Schultz, J. Carl; Zhao, Huimin Biotechnology Progress, Vol. 36, Issue 5 https://doi.org/10.1002/btpr.3008	journal	May 2020
Quantitative flux analysis reveals folate-dependent NADPH production Fan, Jing; Ye, Jiangbin; Kamphorst, Jurre J. Nature, Vol. 510, Issue 7504 https://doi.org/10.1038/nature13236	journal	May 2014
Tracing metabolic flux through time and space with isotope labeling experiments Allen, Doug K.; Young, Jamey D. Current Opinion in Biotechnology, Vol. 64 https://doi.org/10.1016/j.copbio.2019.11.003	journal	August 2020
Quantifying global agricultural water appropriation with data derived from earth observations Wu, Bingfang; Tian, Fuyou; Zhang, Miao Journal of Cleaner Production, Vol. 358 https://doi.org/10.1016/j.jclepro.2022.131891	journal	July 2022
Isotopic evidence for episodic nitrogen fixation in switchgrass (Panicum virgatum L.) Roley, Sarah S.; Xue, Chao; Hamilton, Stephen K. Soil Biology and Biochemistry, Vol. 129 https://doi.org/10.1016/j.soilbio.2018.11.006	journal	February 2019
CO2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion Jones, Shawn W.; Fast, Alan G.; Carlson, Ellinor D. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12800	journal	September 2016
Soil water vapour isotopes identify missing water source for streamside trees Oerter, Erik J.; Siebert, Griffin; Bowling, David R. Ecohydrology, Vol. 12, Issue 4 https://doi.org/10.1002/eco.2083	journal	February 2019
A guide to metabolic flux analysis in metabolic engineering: Methods, tools and applications Antoniewicz, Maciek R. Metabolic Engineering, Vol. 63 https://doi.org/10.1016/j.ymben.2020.11.002	journal	January 2021
Engineering Strategies to Boost Crop Productivity by Cutting Respiratory Carbon Loss Amthor, Jeffrey S.; Bar-Even, Arren; Hanson, Andrew D. The Plant Cell, Vol. 31, Issue 2 https://doi.org/10.1105/tpc.18.00743	journal	January 2019
Novel Approach for High-Throughput Metabolic Screening of Whole Plants by Stable Isotopes Dersch, Lisa Maria; Beckers, Veronique; Rasch, Detlev Plant Physiology, Vol. 171, Issue 1 https://doi.org/10.1104/pp.15.01217	journal	March 2016