Why cutting respiratory CO 2 loss from crops is possible, practicable, and prudential

Joshi, Jaya; Amthor, Jeffrey S.; McCarty, Donald R.; Messina, Carlos D.; Wilson, Mark A.; Millar, A. Harvey; Hanson, Andrew D.

doi:10.1002/moda.1

Title: Why cutting respiratory CO ₂ loss from crops is possible, practicable, and prudential

Journal Article · Fri Jan 20 00:00:00 UTC 2023 · Modern Agriculture

DOI: https://doi.org/10.1002/moda.1 · OSTI ID:1914360

^[1]; Amthor, Jeffrey S. ^[2]; McCarty, Donald R. ^[3]; Messina, Carlos D. ^[3]; Wilson, Mark A. ^[4]; Millar, A. Harvey ^[5];

^[3]

Department of Biology Centre for Applied Synthetic Biology Concordia University Montréal Quebec Canada
Northern Arizona University Center for Ecosystem Science and Society Flagstaff Arizona USA
Horticultural Sciences Department University of Florida Gainesville Florida USA
Department of Biochemistry and Redox Biology Center University of Nebraska Lincoln Nebraska USA
Australian Research Council Centre of Excellence in Plant Energy Biology School of Molecular Sciences University of Western Australia Crawley Western Australia Australia

Abstract Plants release back to the atmosphere about half of the CO ₂ they capture by photosynthesis. Decreasing the rate of crop respiration could therefore potentially increase yields, store more carbon in the soil and draw down atmospheric CO ₂ . However, decreasing respiration rate has had very little research effort compared to increasing photosynthesis, the historically dominant metabolic paradigm for crop improvement. Conceptual and technical advances, particularly in protein turnover and directed enzyme evolution, have now opened ways to trim the large fraction of respiration that fuels proteome maintenance by lowering the breakdown and resynthesis rates of enzymes and other proteins. In addition to being theoretically possible and practicable, exploring the reduction of respiration is prudential, given that it (i) has barely yet been tried and (ii) could help meet the challenges of sustaining crop productivity and managing atmospheric carbon.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0020153

OSTI ID:: 1914360

Journal Information:: Modern Agriculture, Journal Name: Modern Agriculture Journal Issue: 1 Vol. 1; ISSN 2751-4102

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: Country unknown/Code not available

Language:: English

References (77)

Directed evolution of an industrial biocatalyst: 2-deoxy-D-ribose 5-phosphate aldolase Jennewein, Stefan; Schürmann, Martin; Wolberg, Michael Biotechnology Journal, Vol. 1, Issue 5 https://doi.org/10.1002/biot.200600020	journal	May 2006
Engineering protonation conformation of l ‐aspartate‐α‐decarboxylase to relieve mechanism‐based inactivation Qian, Yuanyuan; Lu, Cui; Liu, Jia Biotechnology and Bioengineering, Vol. 117, Issue 6 https://doi.org/10.1002/bit.27316	journal	March 2020
The McCree–de Wit–Penning de Vries–Thornley Respiration Paradigms: 30 Years Later Amthor, J. Annals of Botany, Vol. 86, Issue 1 https://doi.org/10.1006/anbo.2000.1175	journal	July 2000
Comparative Biochemistry of Ribulose Bisphosphate Carboxylase in Higher Plants Ogren, William L.; Hunt, Larry D. Photosynthetic Carbon Assimilation https://doi.org/10.1007/978-1-4684-8106-8_9	book	January 1978
Maintenance energy: a general model for energy-limited and energy-sufficient growth Pirt, S. J. Archives of Microbiology, Vol. 133, Issue 4 https://doi.org/10.1007/bf00521294	journal	January 1982
Codon usage bias Parvathy, Sujatha Thankeswaran; Udayasuriyan, Varatharajalu; Bhadana, Vijaipal Molecular Biology Reports, Vol. 49, Issue 1 https://doi.org/10.1007/s11033-021-06749-4	journal	November 2021
Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation Yamori, Wataru; Hikosaka, Kouki; Way, Danielle A. Photosynthesis Research, Vol. 119, Issue 1-2 https://doi.org/10.1007/s11120-013-9874-6	journal	June 2013
Biochemical and synthetic biology approaches to improve photosynthetic CO2-fixation Erb, Tobias J.; Zarzycki, Jan Current Opinion in Chemical Biology, Vol. 34 https://doi.org/10.1016/j.cbpa.2016.06.026	journal	October 2016
Systems for in vivo hypermutation: a quest for scale and depth in directed evolution Rix, Gordon; Liu, Chang C. Current Opinion in Chemical Biology, Vol. 64 https://doi.org/10.1016/j.cbpa.2021.02.008	journal	October 2021
Scalable, Continuous Evolution of Genes at Mutation Rates above Genomic Error Thresholds Ravikumar, Arjun; Arzumanyan, Garri A.; Obadi, Muaeen K. A. Cell, Vol. 175, Issue 7 https://doi.org/10.1016/j.cell.2018.10.021	journal	December 2018
The evolution of metabolism: How to test evolutionary hypotheses at the genomic level Scossa, Federico; Fernie, Alisdair R. Computational and Structural Biotechnology Journal, Vol. 18 https://doi.org/10.1016/j.csbj.2020.02.009	journal	January 2020
Photosynthetic limits on carbon sequestration in croplands Janzen, H. Henry; van Groenigen, Kees Jan; Powlson, David S. Geoderma, Vol. 416 https://doi.org/10.1016/j.geoderma.2022.115810	journal	June 2022
Paradigm shift in plant growth control Körner, Christian Current Opinion in Plant Biology, Vol. 25 https://doi.org/10.1016/j.pbi.2015.05.003	journal	June 2015
Next-generation strategies for understanding and influencing source–sink relations in crop plants Sonnewald, Uwe; Fernie, Alisdair R. Current Opinion in Plant Biology, Vol. 43 https://doi.org/10.1016/j.pbi.2018.01.004	journal	June 2018
Redesigning thiamin synthesis: Prospects and potential payoffs Hanson, Andrew D.; Amthor, Jeffrey S.; Sun, Jiayi Plant Science, Vol. 273 https://doi.org/10.1016/j.plantsci.2018.01.019	journal	August 2018
Increasing Photosynthesis: Unlikely Solution For World Food Problem Sinclair, Thomas R.; Rufty, Thomas W.; Lewis, Ramsey S. Trends in Plant Science, Vol. 24, Issue 11 https://doi.org/10.1016/j.tplants.2019.07.008	journal	November 2019
Directed Evolution of Plant Processes: Towards a Green (r)Evolution? Gionfriddo, Matteo; De Gara, Laura; Loreto, Francesco Trends in Plant Science, Vol. 24, Issue 11 https://doi.org/10.1016/j.tplants.2019.08.004	journal	November 2019
Enzymes as Parts in Need of Replacement – and How to Extend Their Working Life Tivendale, Nathan D.; Hanson, Andrew D.; Henry, Christopher S. Trends in Plant Science, Vol. 25, Issue 7 https://doi.org/10.1016/j.tplants.2020.02.006	journal	July 2020
Addressing Research Bottlenecks to Crop Productivity Reynolds, Matthew; Atkin, Owen K.; Bennett, Malcolm Trends in Plant Science, Vol. 26, Issue 6 https://doi.org/10.1016/j.tplants.2021.03.011	journal	June 2021
Surplus Carbon Drives Allocation and Plant–Soil Interactions Prescott, Cindy E.; Grayston, Sue J.; Helmisaari, Heljä-Sisko Trends in Ecology & Evolution, Vol. 35, Issue 12 https://doi.org/10.1016/j.tree.2020.08.007	journal	December 2020
Differences among commercial maize (Zea mays L.) hybrids in respiration rates of mature leaves Earl, H. J.; Tollenaar, M. Field Crops Research, Vol. 59, Issue 1 https://doi.org/10.1016/s0378-4290(98)00098-7	journal	October 1998
Survival of the cheapest: how proteome cost minimization drives evolution Kepp, Kasper P. Quarterly Reviews of Biophysics, Vol. 53 https://doi.org/10.1017/s0033583520000037	journal	January 2020
The Moderately (D)efficient Enzyme: Catalysis-Related Damage In Vivo and Its Repair Bathe, Ulschan; Leong, Bryan J.; McCarty, Donald R. Biochemistry, Vol. 60, Issue 47 https://doi.org/10.1021/acs.biochem.1c00613	journal	November 2021
Proteome Scale-Protein Turnover Analysis Using High Resolution Mass Spectrometric Data from Stable-Isotope Labeled Plants Fan, Kai-Ting; Rendahl, Aaron K.; Chen, Wen-Ping Journal of Proteome Research, Vol. 15, Issue 3 https://doi.org/10.1021/acs.jproteome.5b00772	journal	January 2016
Cheating the Cheater: Suppressing False-Positive Enrichment during Biosensor-Guided Biocatalyst Engineering Trivedi, Vikas D.; Mohan, Karishma; Chappell, Todd C. ACS Synthetic Biology, Vol. 11, Issue 1 https://doi.org/10.1021/acssynbio.1c00506	journal	December 2021
The Moderately Efficient Enzyme: Evolutionary and Physicochemical Trends Shaping Enzyme Parameters Bar-Even, Arren; Noor, Elad; Savir, Yonatan Biochemistry, Vol. 50, Issue 21 https://doi.org/10.1021/bi2002289	journal	May 2011
From Suicide Enzyme to Catalyst: The Iron-Dependent Sulfide Transfer in Methanococcus jannaschii Thiamin Thiazole Biosynthesis Eser, Bekir E.; Zhang, Xuan; Chanani, Prem K. Journal of the American Chemical Society, Vol. 138, Issue 11 https://doi.org/10.1021/jacs.6b00445	journal	March 2016
Diminishing returns and tradeoffs constrain the laboratory optimization of an enzyme Tokuriki, Nobuhiko; Jackson, Colin J.; Afriat-Jurnou, Livnat Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms2246	journal	January 2012
Distinguishing between yield advances and yield plateaus in historical crop production trends Grassini, Patricio; Eskridge, Kent M.; Cassman, Kenneth G. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3918	journal	December 2013
Protein turnover in plant biology Nelson, Clark J.; Millar, A. Harvey Nature Plants, Vol. 1, Issue 3 https://doi.org/10.1038/nplants.2015.17	journal	March 2015
In vivo hypermutation and continuous evolution Molina, Rosana S.; Rix, Gordon; Mengiste, Amanuella A. Nature Reviews Methods Primers, Vol. 2, Issue 1 https://doi.org/10.1038/s43586-022-00119-5	journal	May 2022
Bioinformatic and experimental evidence for suicidal and catalytic plant THI4s Joshi, Jaya; Beaudoin, Guillaume A. W.; Patterson, Jenelle A. Biochemical Journal, Vol. 477, Issue 11 https://doi.org/10.1042/bcj20200297	journal	June 2020
The greenest revolution – harnessing the power of plants to help combat climate change Busch, Wolfgang; Miller, Charlotte The Biochemist, Vol. 44, Issue 3 https://doi.org/10.1042/bio_2022_113	journal	June 2022
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
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
The timescale of early land plant evolution Morris, Jennifer L.; Puttick, Mark N.; Clark, James W. Proceedings of the National Academy of Sciences, Vol. 115, Issue 10 https://doi.org/10.1073/pnas.1719588115	journal	February 2018
The number of catalytic cycles in an enzyme’s lifetime and why it matters to metabolic engineering Hanson, Andrew D.; McCarty, Donald R.; Henry, Christopher S. Proceedings of the National Academy of Sciences, Vol. 118, Issue 13 https://doi.org/10.1073/pnas.2023348118	journal	March 2021
Directed evolution of a thermostable esterase Giver, L.; Gershenson, A.; Freskgard, P.-O. Proceedings of the National Academy of Sciences, Vol. 95, Issue 22, p. 12809-12813 https://doi.org/10.1073/pnas.95.22.12809	journal	October 1998
Interspecies Differences in Proteome Turnover Kinetics Are Correlated With Life Spans and Energetic Demands Swovick, Kyle; Firsanov, Denis; Welle, Kevin A. Molecular & Cellular Proteomics, Vol. 20 https://doi.org/10.1074/mcp.ra120.002301	journal	January 2021
Organic acid excretion from roots: a plant mechanism for enhancing phosphorus acquisition, enhancing aluminum tolerance, and recruiting beneficial rhizobacteria Wu, Liujie; Kobayashi, Yuriko; Wasaki, Jun Soil Science and Plant Nutrition, Vol. 64, Issue 6 https://doi.org/10.1080/00380768.2018.1537093	journal	October 2018
Effects of Synonymous Mutations beyond Codon Bias: The Evidence for Adaptive Synonymous Substitutions from Microbial Evolution Experiments Bailey, Susan F.; Alonso Morales, Luz Angela; Kassen, Rees Genome Biology and Evolution, Vol. 13, Issue 9 https://doi.org/10.1093/gbe/evab141	journal	June 2021
The uncoupling of respiration in plant mitochondria: keeping reactive oxygen and nitrogen species under control Popov, Vasily N.; Syromyatnikov, Mikhail Y.; Fernie, Alisdair R. Journal of Experimental Botany, Vol. 72, Issue 3 https://doi.org/10.1093/jxb/eraa510	journal	November 2020
Radiation use efficiency increased over a century of maize (Zea mays L.) breeding in the US corn belt Messina, Carlos D.; Rotundo, Jose; Hammer, Graeme L. Journal of Experimental Botany, Vol. 73, Issue 16 https://doi.org/10.1093/jxb/erac212	journal	May 2022
Frontiers in metabolic reconstruction and modeling of plant genomes Seaver, S. M. D.; Henry, C. S.; Hanson, A. D. Journal of Experimental Botany, Vol. 63, Issue 6 https://doi.org/10.1093/jxb/err371	journal	January 2012
Synthetic biology approaches for improving photosynthesis Kubis, Armin; Bar-Even, Arren Journal of Experimental Botany, Vol. 70, Issue 5 https://doi.org/10.1093/jxb/erz029	journal	January 2019
Signatures of Ecological Resource Availability in the Animal and Plant Proteomes Elser, James J.; Fagan, William F.; Subramanian, Sankar Molecular Biology and Evolution, Vol. 23, Issue 10 https://doi.org/10.1093/molbev/msl068	journal	July 2006
Respiration and Dry Matter Accumulation Around the Time of Anthesis in Field Stands of Winter Wheat (Triticum aestivum) Mccullough, D. E.; Hunt, L. A. Annals of Botany, Vol. 63, Issue 3 https://doi.org/10.1093/oxfordjournals.aob.a087748	journal	March 1989
Stromal NADH supplied by PHOSPHOGLYCERATE DEHYDROGENASE3 is crucial for photosynthetic performance Höhner, Ricarda; Day, Philip M.; Zimmermann, Sandra E. Plant Physiology, Vol. 186, Issue 1 https://doi.org/10.1093/plphys/kiaa117	journal	January 2021
Using continuous directed evolution to improve enzymes for plant applications García-García, Jorge D.; Van Gelder, Kristen; Joshi, Jaya Plant Physiology, Vol. 188, Issue 2 https://doi.org/10.1093/plphys/kiab500	journal	October 2021
Respiratory energy demands and scope for demand expansion and destruction Bathe, Ulschan; Leong, Bryan J.; Van Gelder, Kristen Plant Physiology https://doi.org/10.1093/plphys/kiac493	journal	October 2022
The global nitrogen cycle in the twenty-first century Fowler, David; Coyle, Mhairi; Skiba, Ute Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621 https://doi.org/10.1098/rstb.2013.0164	journal	July 2013
Proteins with High Turnover Rate in Barley Leaves Estimated by Proteome Analysis Combined with in Planta Isotope Labeling Nelson, Clark J.; Alexova, Ralitza; Jacoby, Richard P. Plant Physiology, Vol. 166, Issue 1 https://doi.org/10.1104/pp.114.243014	journal	July 2014
Inference and prediction of metabolic network fluxes Nikoloski, Zoran; Perez-Storey, Richard; Sweetlove, Lee J. Plant Physiology https://doi.org/10.1104/pp.15.01082	journal	September 2015
Parts-Prospecting for a High-Efficiency Thiamin Thiazole Biosynthesis Pathway Sun, Jiayi; Sigler, Cindy L.; Beaudoin, Guillaume A. W. Plant Physiology, Vol. 179, Issue 3 https://doi.org/10.1104/pp.18.01085	journal	October 2018
Protein Degradation Rate in Arabidopsis thaliana Leaf Growth and Development Li, Lei; Nelson, Clark J.; Trösch, Josua The Plant Cell, Vol. 29, Issue 2 https://doi.org/10.1105/tpc.16.00768	journal	January 2017
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
Soil carbon sequestration to mitigate climate change: a critical re-examination to identify the true and the false Powlson, D. S.; Whitmore, A. P.; Goulding, K. W. T. European Journal of Soil Science, Vol. 62, Issue 1 https://doi.org/10.1111/j.1365-2389.2010.01342.x	journal	January 2011
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: Tansley review Ainsworth, Elizabeth A.; Long, Stephen P. New Phytologist, Vol. 165, Issue 2 https://doi.org/10.1111/j.1469-8137.2004.01224.x	journal	November 2004
Plant carbon metabolism and climate change: elevated CO ₂ and temperature impacts on photosynthesis, photorespiration and respiration Dusenge, Mirindi Eric; Duarte, André Galvao; Way, Danielle A. New Phytologist, Vol. 221, Issue 1 https://doi.org/10.1111/nph.15283	journal	July 2018
Core principles which explain variation in respiration across biological scales O'Leary, Brendan M.; Asao, Shinichi; Millar, A. Harvey New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15576	journal	December 2018
Growth rate correlates negatively with protein turnover in Arabidopsis accessions Ishihara, Hirofumi; Moraes, Thiago Alexandre; Pyl, Eva-Theresa The Plant Journal, Vol. 91, Issue 3 https://doi.org/10.1111/tpj.13576	journal	June 2017
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components Field, C. B. Science, Vol. 281, Issue 5374 https://doi.org/10.1126/science.281.5374.237	journal	July 1998
Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection De Souza, Amanda P.; Burgess, Steven J.; Doran, Lynn Science, Vol. 377, Issue 6608, p. 851-854 https://doi.org/10.1126/science.adc9831	journal	August 2022
The Steady-State Internal Redox State (NADH/NAD) Reflects the External Redox State and Is Correlated with Catabolic Adaptation in Escherichia coli de Graef, Mark R.; Alexeeva, Svetlana; Snoep, Jacky L. Journal of Bacteriology, Vol. 181, Issue 8 https://doi.org/10.1128/jb.181.8.2351-2357.1999	journal	April 1999
The Protein Cost of Metabolic Fluxes: Prediction from Enzymatic Rate Laws and Cost Minimization Noor, Elad; Flamholz, Avi; Bar-Even, Arren PLOS Computational Biology, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pcbi.1005167	journal	November 2016
Yield Trends Are Insufficient to Double Global Crop Production by 2050 Ray, Deepak K.; Mueller, Nathaniel D.; West, Paul C. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066428	journal	June 2013
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed LeBauer, David S.; Treseder, Kathleen K. Ecology, Vol. 89, Issue 2 https://doi.org/10.1890/06-2057.1	journal	February 2008
Yield Potential, Plant Assimilatory Capacity, and Metabolic Efficiencies Loomis, R. S.; Amthor, J. S. Crop Science, Vol. 39, Issue 6 https://doi.org/10.2135/cropsci1999.3961584x	journal	November 1999
Post-Green Revolution Trends in Yield Potential of Temperate Maize in the North-Central United States Duvick, D. N.; Cassman, K. G. Crop Science, Vol. 39, Issue 6 https://doi.org/10.2135/cropsci1999.3961622x	journal	November 1999
‘Breathing Out’ under Heat Stress—Respiratory Control of Crop Yield under High Temperature Sharma, Nitin; Thakur, Meenakshi; Suryakumar, Pavithra Agronomy, Vol. 12, Issue 4 https://doi.org/10.3390/agronomy12040806	journal	March 2022
Extremely Low Leakage Expression Systems Using Dual Transcriptional-Translational Control for Toxic Protein Production Kato, Yusuke International Journal of Molecular Sciences, Vol. 21, Issue 3 https://doi.org/10.3390/ijms21030705	journal	January 2020
Application of CRISPR/Cas9 in Crop Quality Improvement Liu, Qier; Yang, Fan; Zhang, Jingjuan International Journal of Molecular Sciences, Vol. 22, Issue 8 https://doi.org/10.3390/ijms22084206	journal	April 2021
Potential for Applying Continuous Directed Evolution to Plant Enzymes: An Exploratory Study García-García, Jorge D.; Joshi, Jaya; Patterson, Jenelle A. Life, Vol. 10, Issue 9 https://doi.org/10.3390/life10090179	journal	September 2020
Parameter Reliability and Understanding Enzyme Function McDonald, Andrew G.; Tipton, Keith F. Molecules, Vol. 27, Issue 1 https://doi.org/10.3390/molecules27010263	journal	January 2022
The Role of Synthetic Biology in Atmospheric Greenhouse Gas Reduction: Prospects and Challenges DeLisi, Charles; Patrinos, Aristides; MacCracken, Michael BioDesign Research, Vol. 2020 https://doi.org/10.34133/2020/1016207	journal	July 2020
Excess carbon in aquatic organisms and ecosystems: Physiological, ecological, and evolutionary implications Hessen, Dag O.; Anderson, Thomas R. Limnology and Oceanography, Vol. 53, Issue 4 https://doi.org/10.4319/lo.2008.53.4.1685	journal	July 2008
Global Carbon Budget 2021 Friedlingstein, Pierre; Jones, Matthew W.; O'Sullivan, Michael Earth System Science Data, Vol. 14, Issue 4 https://doi.org/10.5194/essd-14-1917-2022	journal	April 2022

Similar Records

Towards a dynamic photosynthesis model to guide yield improvement in C4 crops

Journal Article · Fri Aug 06 00:00:00 UTC 2021 · The Plant Journal · OSTI ID:1812252

Wang, Yu; Chan, Kher Xing; Long, Stephen P.

Adapting enzymes to improve their functionality in plants: why and how

Journal Article · Tue Oct 03 00:00:00 UTC 2023 · Biochemical Society Transactions · OSTI ID:2578355

Oliveira-Filho, Edmar; Voiniciuc, Cătălin; Hanson, Andrew

Fundamental cosmology from ANDES precision spectroscopy

Journal Article · Fri May 05 00:00:00 UTC 2023 · Monthly Notices of the Royal Astronomical Society · OSTI ID:1974254

Marques, C. M. J.; Martins, C. J. A. P.; Alves, C. S.

Title: Why cutting respiratory CO 2 loss from crops is possible, practicable, and prudential

Citation Formats

References (77)

Similar Records

Related Subjects

Title: Why cutting respiratory CO ₂ loss from crops is possible, practicable, and prudential