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Focus on respiration

Focus on respiration Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 1* 2* 3,4* 5,6,7* Andrew D. Hanson, A. Harvey Millar, Zoran Nikoloski, and Danielle A. Way Horticultural Sciences Department, University of Florida, Gainesville, Florida 32611, USA ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, University of Western Australia, Crawley 6009 WA, Australia Bioinformatics, Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany Systems Biology and Mathematical Modeling, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia Department of Biology, Western University, London, ON, N6A 5B7, Canada Nicholas School of the Environment, Duke University, Durham, North Carolina 27708, USA *To whom correspondence should be addressed. Email: adha@ufl.edu, harvey.millar@uwa.edu.au, Nikoloski@mpimp-golm.mpg.de, or Danielle.Way@anu.edu.au Respiration is as central to plant metabolism as photosynthesis; it is the main source of ATP, reducing equivalents, and biosynthetic intermediates in non-green tissues, and in green tissues during the night. Further, respiration returns to the atmosphere roughly half the carbon fixed by photosynthesis at both the individual plant level (Amthor et al., 2019) and on a global scale (Raich et al., 2014) and so is a major item in the global carbon budget. In fact, terrestrial plant respiration releases about six-fold more CO to the atmosphere than the anthropogenic total from fossil fuel consumption, cement production, and land use change (~60 versus ~10 gigatonnes CO per year) (NASEM, 2019). Crop respiration can be reckoned to contribute around 8 gigatonnes of CO to the terrestrial total annually (Field et al., 1998; Joshi et al., 2023), making crop CO2 emissions alone almost as great as anthropogenic emissions. Despite the cardinal metabolic and biogeochemical significance of plant respiration and the potential to increase crop yields by cutting respiratory CO loss (Amthor et al 2019, Garcia et al., 2023; Joshi et al., 2023), plant respiration has long had far less research attention than photosynthesis – a situation that has been justly called an ‘asymmetry in crop-focused academic research’ (Reynolds et al., 2021). This asymmetry is readily apparent from a search of plant science journals for articles relating to photo- synthesis or respiration over the past 70 years (Figure 1). The bias in favor of photosynthesis is curr- ently about three-fold in the major journals that cover both ‘basic plant biology’ (Figure 1A) and ‘crop science’ (Figure 1B) (a somewhat arbitrary but still useful division). This bias has apparently increased © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 over time, more markedly in basic science journals (which emphasize molecular mechanisms) (Figure 1A, inset) than in crop science journals (which focus on physiology, environmental responses and breeding) (Figure 1B, inset). It would thus seem that our grandparents – particularly reductionist ones – were more interested in understanding respiration than we have been in recent decades. This situation is ultimately unreasonable and a more symmetrical research investment in respiration will benefit plant science as a whole. This Focus Issue was inspired by the need to take stock of the progress now being made and to encourage further progress. It adds to recent reviews overviewing the progress in research on respiration rates (Dusenge et al., 2019; O’Leary et al., 2019), plant mitochondrial composition and activity (Møller et al., 2021), and assembly and function of the plant respiratory oxidative phosphorylation system (Meyer et al., 2019; 2022). It also complements the seminal review of Cannel and Thornley (2000) on guiding principles for modeling plant respiration. To these ends, the issue includes a set of Update Reviews that span the range of respiration research from the plant community level to subcellular and enzyme levels, as well as Research Articles. Arranged roughly in order of descending organizational level, the Updates are as follows. Bulut et al. (2023) survey the (still scant) literature on natural variation in plant respiration and the (more extensive) literature on variation in respiratory metabolites and other respiration-related traits. They end their review with a clarion call for more work on natural variation of respiration itself and on its mechanistic and evolutionary basis. Relatedly, O’Leary et al. (2023) review substantial advances in measuring plant respiration, particularly in high-throughput modes compatible with large-scale ecological surveys, gen- etic screens, crop breeding trials, and omics studies. They point to a future in which it will be possible to link respiratory variation to specific genes, benefitting basic knowledge as well as crop improvement. Wendering and Nikoloski (2023) cover advances in computational modeling of plant respiration, particularly the increasing use of mechanistic (i.e., biochemically based) models. They emphasize the potential value of such models to metabolic engineering of, and breeding for, a particular (average) respiration rate and their use in terrestrial biosphere models that simulate responses to climate change. Bridging between the crop level and biochemical processes, Bathe et al. (2023) revisit the principles of plant respiratory energy budgeting and estimating the costs of metabolic processes. They then apply these principles to assess how synthetic biology interventions that add new metabolic demands or cut existing ones could affect crop yield and carbon sequestration. Moving to the organelle level, Igamberd- iev and Bykova (2023) summarize advances in understanding the unique roles of mitochondrial meta- bolism in photosynthetic tissues in the light, including operation of tricarboxylic acid cycle enzymes in non-cyclic mode, and non-coupled electron transport. Overall, they present an emerging new view of how mitochondria in photosynthetic cells transition from powerhouses to thermodynamic buffering units ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 that regulate cellular redox and energy balance and furnish intermediates and reducing power to supp- ort biosynthesis. At the level of the whole respiratory chain, Ghifari et al. (2023) discuss advances in understanding the makeup, biogenesis, and turnover of plant oxidative phosphorylation complexes, and mechanisms that regulate their biogenesis and activity. At the individual enzyme level, McDonald (2023) covers advances in defining the distribution and physiological functions of the alternative oxid- ase of the plant mitochondrial electron transport chain, and anticipates the progress that genome edit- ing tools and new oxygen sensing technologies now make possible. Finally, at the metabolite level, Le and Millar (2023) cover the diverse respiratory substrates that mitochondria import and use in normal and stress conditions, highlighting evidence for metabolic channeling in supply of substrates to resp- iration. With this as a base, they then consider how synthetic biology could engineer bypasses to allow use of alternative respiratory substrates, with potential benefits for carbon use efficiency and growth. Reinforcing the disparity between the numbers of research publications on respiration and photo- synthesis in Figure 1, this issue’s Updates are shot through with phrases such as ‘neglected historic- ally’, ‘paucity of studies’, ‘relatively rare’, ‘poorly known’, ‘still elementary’, ‘always had far less attent- ion’, and ‘attracted considerably less…efforts in comparison to photosynthesis’. It is interesting to note that achievements in photosynthesis research have been greatly aided by community-wide adoption of grand challenges surrounding the wavelengths of light used by light-harvesting machinery, re-engin- eering Rubisco, building bypasses to photorespiration, and introducing C photosynthesis into C 4 3 crops. Plant respiration research has not yet rallied around such grand challenges and this may cont- inue to limit its further progress in a global era of science as an enabler of change, not just a tool of discovery. Another major reason for the advances in photosynthesis research is the accumulated knowledge about the few canonical pathways underlying photosynthesis, allowing development of des- criptive models (e.g., Farquhar et al., 1980) and guiding design of improvement strategies. In contrast, as the Updates remind us, measuring, characterizing, and engineering respiration requires a systems perspective, whose potential is not fully exploited despite advances in plant systems biology. These Updates seek to spark this process, in confident expectation of a bright future for knowledge of plant respiration and its application to agricultural productivity and climate change mitigation. REFERENCES Amthor JS, Bar-Even A, Hanson AD, Millar AH, Stitt M, Sweetlove LJ, Tyerman SD (2019) Engineering strategies to boost crop productivity by cutting respiratory carbon loss. Plant Cell 31: 297-314 Bathe U, Leong BJ, Van Gelder K, Barbier GG, Henry CS, Amthor JS, Hanson AD (2023) Resp- iratory energy demands and scope for demand expansion and destruction. Plant Physiol 2022 Oct 22:kiac493 ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 Bulut M, Alseekh S, Fernie AR (2023) Natural variation of respiration-related traits in plants. Plant Physiol 2022 Dec 22:kiac593 Cannel MGR, Thornley JHM (2000) Modeling of components of plant respiration: Some guiding principles. Ann Bot 85: 45–54 Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221: 32–49 Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO assimilation in leaves of C species. Planta 149: 78–90 Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237–240 Garcia A, Gaju O, Bowerman AF, Buck SA, Evans JR, Furbank RT, Gilliham M, Millar AH, Pogson BJ, Reynolds MP, et al. OK (2023) Enhancing crop yields through improvements in the efficiency of photosynthesis and respiration. New Phytol 237: 60–77 Ghifari AS, Saurabh Saha S, Murcha MW (2023) The biogenesis and regulation of the plant oxidative phosphorylation system. Plant Physiol 2023 Igamberdiev AU, Bykova NV (2023) Mitochondria in photosynthetic cells: Coordinating redox control and energy balance. Plant Physiol. 2022 Nov 28:kiac541 Joshi J, Amthor JS, McCarty DR, Messina CD, Wilson MA, Millar AH, Hanson AD (2023) Why cutting respiratory CO2 loss from crops is possible, practicable, and prudential. Modern Agriculture 2023: 1–11 Le XH, Millar AH (2023) The diversity of substrates for plant respiration and how to optimize their use. Plant Physiol. 2022 Dec 27:kiac599 McDonald AE (2023) Unique opportunities for future research on the alternative oxidase of plants. Plant Physiol. 2022 Dec 6:kiac555 Meyer EH, Letts JA, Maldonado M (2022) Structural insights into the assembly and the function of the plant oxidative phosphorylation system. New Phytol 235: 1315–1329 Meyer EH, Welchen E, Carrie C (2019) Assembly of the complexes of the oxidative phosphorylation system in land plant mitochondria. Annu Rev Plant Biol 70: 23–50 Møller IM, Rasmusson AG, Van Aken O (2021) Plant mitochondria – past, present and future. Plant J 108: 912–959 NASEM (National Academies of Sciences, Engineering and Medicine) (2019) Negative Emissions Technologies and Reliable Sequestration: A Research Agenda. https://doi.org/10.17226/25259 O'Leary BM, Asao S, Millar AH, Atkin OK (2019) Core principles which explain variation in respiration across biological scales. New Phytol 222: 670–686 ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 O’Leary BM, Scafaro AP, York LM (2023) High-throughput, dynamic, multi-dimensional: an expand- ing repertoire of plant respiration measurements. Plant Physiol 2023 Jan 13:kiac580 Raich JW, Lambers H, Oliver DJ (2014) 10.16 – Respiration in Terrestrial Ecosystems. In Holland HD, Turekian KK, eds, Treatise on Geochemistry (Second Edition). Elsevier, Amsterdam, pp 613– Reynolds M, Atkin OK, Bennett M, Cooper M, Dodd IC, Foulkes MJ, Frohberg C, Hammer G, Henderson IR, Huang B, et al. (2021) Addressing research bottlenecks to crop productivity. Trends Plant Sci 26: 607–630 Wendering P, Nikoloski Z (2023) Towards mechanistic modelling and rational engineering of plant respiration. Plant Physiol 2023 FIGURE LEGEND Figure 1. Cumulative numbers of publications on photosynthesis (P) and respiration (R) between 1950 and 2020. A, Publications in representative basic plant biology journals (i.e., Plant Physiology, Plant Cell, New Phytologist, Plant Journal, Plant Cell and Environment, Molecular Plant, Nature Plants, Plant Biology, Trends in Plant Science, Annual Review of Plant Biology, or Annual Review of Plant Physio- logy and Plant Molecular Biology, Annual Review of Plant Physiology). B, Publications in representative crop science journals (i.e., Field Crops Research, Advances in Agronomy, Agronomy Journal, Journal of Agricultural Science, European Journal of Agronomy, Crop Science, Canadian Journal of Plant Science, Australian Journal of Crop Science, Journal of the American Society for Horticultural Science, HortScience, Horticulture Research, Scientia Horticulturae). Insets in each plot show the ratio of respiration to photosynthesis publications (R/P). Data were extracted from the Web of Science database using either ‘photosynthesis’ or ‘respiration + plant’ as search terms along with the list of journal names. ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 ACCECPTED MANUSCRIPT http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png PLANT PHYSIOLOGY Oxford University Press

Focus on respiration

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Publisher
Oxford University Press
Copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.
ISSN
0032-0889
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1532-2548
DOI
10.1093/plphys/kiad041
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Abstract

Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 1* 2* 3,4* 5,6,7* Andrew D. Hanson, A. Harvey Millar, Zoran Nikoloski, and Danielle A. Way Horticultural Sciences Department, University of Florida, Gainesville, Florida 32611, USA ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, University of Western Australia, Crawley 6009 WA, Australia Bioinformatics, Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany Systems Biology and Mathematical Modeling, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia Department of Biology, Western University, London, ON, N6A 5B7, Canada Nicholas School of the Environment, Duke University, Durham, North Carolina 27708, USA *To whom correspondence should be addressed. Email: adha@ufl.edu, harvey.millar@uwa.edu.au, Nikoloski@mpimp-golm.mpg.de, or Danielle.Way@anu.edu.au Respiration is as central to plant metabolism as photosynthesis; it is the main source of ATP, reducing equivalents, and biosynthetic intermediates in non-green tissues, and in green tissues during the night. Further, respiration returns to the atmosphere roughly half the carbon fixed by photosynthesis at both the individual plant level (Amthor et al., 2019) and on a global scale (Raich et al., 2014) and so is a major item in the global carbon budget. In fact, terrestrial plant respiration releases about six-fold more CO to the atmosphere than the anthropogenic total from fossil fuel consumption, cement production, and land use change (~60 versus ~10 gigatonnes CO per year) (NASEM, 2019). Crop respiration can be reckoned to contribute around 8 gigatonnes of CO to the terrestrial total annually (Field et al., 1998; Joshi et al., 2023), making crop CO2 emissions alone almost as great as anthropogenic emissions. Despite the cardinal metabolic and biogeochemical significance of plant respiration and the potential to increase crop yields by cutting respiratory CO loss (Amthor et al 2019, Garcia et al., 2023; Joshi et al., 2023), plant respiration has long had far less research attention than photosynthesis – a situation that has been justly called an ‘asymmetry in crop-focused academic research’ (Reynolds et al., 2021). This asymmetry is readily apparent from a search of plant science journals for articles relating to photo- synthesis or respiration over the past 70 years (Figure 1). The bias in favor of photosynthesis is curr- ently about three-fold in the major journals that cover both ‘basic plant biology’ (Figure 1A) and ‘crop science’ (Figure 1B) (a somewhat arbitrary but still useful division). This bias has apparently increased © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 over time, more markedly in basic science journals (which emphasize molecular mechanisms) (Figure 1A, inset) than in crop science journals (which focus on physiology, environmental responses and breeding) (Figure 1B, inset). It would thus seem that our grandparents – particularly reductionist ones – were more interested in understanding respiration than we have been in recent decades. This situation is ultimately unreasonable and a more symmetrical research investment in respiration will benefit plant science as a whole. This Focus Issue was inspired by the need to take stock of the progress now being made and to encourage further progress. It adds to recent reviews overviewing the progress in research on respiration rates (Dusenge et al., 2019; O’Leary et al., 2019), plant mitochondrial composition and activity (Møller et al., 2021), and assembly and function of the plant respiratory oxidative phosphorylation system (Meyer et al., 2019; 2022). It also complements the seminal review of Cannel and Thornley (2000) on guiding principles for modeling plant respiration. To these ends, the issue includes a set of Update Reviews that span the range of respiration research from the plant community level to subcellular and enzyme levels, as well as Research Articles. Arranged roughly in order of descending organizational level, the Updates are as follows. Bulut et al. (2023) survey the (still scant) literature on natural variation in plant respiration and the (more extensive) literature on variation in respiratory metabolites and other respiration-related traits. They end their review with a clarion call for more work on natural variation of respiration itself and on its mechanistic and evolutionary basis. Relatedly, O’Leary et al. (2023) review substantial advances in measuring plant respiration, particularly in high-throughput modes compatible with large-scale ecological surveys, gen- etic screens, crop breeding trials, and omics studies. They point to a future in which it will be possible to link respiratory variation to specific genes, benefitting basic knowledge as well as crop improvement. Wendering and Nikoloski (2023) cover advances in computational modeling of plant respiration, particularly the increasing use of mechanistic (i.e., biochemically based) models. They emphasize the potential value of such models to metabolic engineering of, and breeding for, a particular (average) respiration rate and their use in terrestrial biosphere models that simulate responses to climate change. Bridging between the crop level and biochemical processes, Bathe et al. (2023) revisit the principles of plant respiratory energy budgeting and estimating the costs of metabolic processes. They then apply these principles to assess how synthetic biology interventions that add new metabolic demands or cut existing ones could affect crop yield and carbon sequestration. Moving to the organelle level, Igamberd- iev and Bykova (2023) summarize advances in understanding the unique roles of mitochondrial meta- bolism in photosynthetic tissues in the light, including operation of tricarboxylic acid cycle enzymes in non-cyclic mode, and non-coupled electron transport. Overall, they present an emerging new view of how mitochondria in photosynthetic cells transition from powerhouses to thermodynamic buffering units ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 that regulate cellular redox and energy balance and furnish intermediates and reducing power to supp- ort biosynthesis. At the level of the whole respiratory chain, Ghifari et al. (2023) discuss advances in understanding the makeup, biogenesis, and turnover of plant oxidative phosphorylation complexes, and mechanisms that regulate their biogenesis and activity. At the individual enzyme level, McDonald (2023) covers advances in defining the distribution and physiological functions of the alternative oxid- ase of the plant mitochondrial electron transport chain, and anticipates the progress that genome edit- ing tools and new oxygen sensing technologies now make possible. Finally, at the metabolite level, Le and Millar (2023) cover the diverse respiratory substrates that mitochondria import and use in normal and stress conditions, highlighting evidence for metabolic channeling in supply of substrates to resp- iration. With this as a base, they then consider how synthetic biology could engineer bypasses to allow use of alternative respiratory substrates, with potential benefits for carbon use efficiency and growth. Reinforcing the disparity between the numbers of research publications on respiration and photo- synthesis in Figure 1, this issue’s Updates are shot through with phrases such as ‘neglected historic- ally’, ‘paucity of studies’, ‘relatively rare’, ‘poorly known’, ‘still elementary’, ‘always had far less attent- ion’, and ‘attracted considerably less…efforts in comparison to photosynthesis’. It is interesting to note that achievements in photosynthesis research have been greatly aided by community-wide adoption of grand challenges surrounding the wavelengths of light used by light-harvesting machinery, re-engin- eering Rubisco, building bypasses to photorespiration, and introducing C photosynthesis into C 4 3 crops. Plant respiration research has not yet rallied around such grand challenges and this may cont- inue to limit its further progress in a global era of science as an enabler of change, not just a tool of discovery. Another major reason for the advances in photosynthesis research is the accumulated knowledge about the few canonical pathways underlying photosynthesis, allowing development of des- criptive models (e.g., Farquhar et al., 1980) and guiding design of improvement strategies. In contrast, as the Updates remind us, measuring, characterizing, and engineering respiration requires a systems perspective, whose potential is not fully exploited despite advances in plant systems biology. These Updates seek to spark this process, in confident expectation of a bright future for knowledge of plant respiration and its application to agricultural productivity and climate change mitigation. REFERENCES Amthor JS, Bar-Even A, Hanson AD, Millar AH, Stitt M, Sweetlove LJ, Tyerman SD (2019) Engineering strategies to boost crop productivity by cutting respiratory carbon loss. Plant Cell 31: 297-314 Bathe U, Leong BJ, Van Gelder K, Barbier GG, Henry CS, Amthor JS, Hanson AD (2023) Resp- iratory energy demands and scope for demand expansion and destruction. Plant Physiol 2022 Oct 22:kiac493 ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 Bulut M, Alseekh S, Fernie AR (2023) Natural variation of respiration-related traits in plants. Plant Physiol 2022 Dec 22:kiac593 Cannel MGR, Thornley JHM (2000) Modeling of components of plant respiration: Some guiding principles. Ann Bot 85: 45–54 Dusenge ME, Duarte AG, Way DA (2019) Plant carbon metabolism and climate change: elevated CO and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol 221: 32–49 Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO assimilation in leaves of C species. Planta 149: 78–90 Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237–240 Garcia A, Gaju O, Bowerman AF, Buck SA, Evans JR, Furbank RT, Gilliham M, Millar AH, Pogson BJ, Reynolds MP, et al. OK (2023) Enhancing crop yields through improvements in the efficiency of photosynthesis and respiration. New Phytol 237: 60–77 Ghifari AS, Saurabh Saha S, Murcha MW (2023) The biogenesis and regulation of the plant oxidative phosphorylation system. Plant Physiol 2023 Igamberdiev AU, Bykova NV (2023) Mitochondria in photosynthetic cells: Coordinating redox control and energy balance. Plant Physiol. 2022 Nov 28:kiac541 Joshi J, Amthor JS, McCarty DR, Messina CD, Wilson MA, Millar AH, Hanson AD (2023) Why cutting respiratory CO2 loss from crops is possible, practicable, and prudential. Modern Agriculture 2023: 1–11 Le XH, Millar AH (2023) The diversity of substrates for plant respiration and how to optimize their use. Plant Physiol. 2022 Dec 27:kiac599 McDonald AE (2023) Unique opportunities for future research on the alternative oxidase of plants. Plant Physiol. 2022 Dec 6:kiac555 Meyer EH, Letts JA, Maldonado M (2022) Structural insights into the assembly and the function of the plant oxidative phosphorylation system. New Phytol 235: 1315–1329 Meyer EH, Welchen E, Carrie C (2019) Assembly of the complexes of the oxidative phosphorylation system in land plant mitochondria. Annu Rev Plant Biol 70: 23–50 Møller IM, Rasmusson AG, Van Aken O (2021) Plant mitochondria – past, present and future. Plant J 108: 912–959 NASEM (National Academies of Sciences, Engineering and Medicine) (2019) Negative Emissions Technologies and Reliable Sequestration: A Research Agenda. https://doi.org/10.17226/25259 O'Leary BM, Asao S, Millar AH, Atkin OK (2019) Core principles which explain variation in respiration across biological scales. New Phytol 222: 670–686 ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 O’Leary BM, Scafaro AP, York LM (2023) High-throughput, dynamic, multi-dimensional: an expand- ing repertoire of plant respiration measurements. Plant Physiol 2023 Jan 13:kiac580 Raich JW, Lambers H, Oliver DJ (2014) 10.16 – Respiration in Terrestrial Ecosystems. In Holland HD, Turekian KK, eds, Treatise on Geochemistry (Second Edition). Elsevier, Amsterdam, pp 613– Reynolds M, Atkin OK, Bennett M, Cooper M, Dodd IC, Foulkes MJ, Frohberg C, Hammer G, Henderson IR, Huang B, et al. (2021) Addressing research bottlenecks to crop productivity. Trends Plant Sci 26: 607–630 Wendering P, Nikoloski Z (2023) Towards mechanistic modelling and rational engineering of plant respiration. Plant Physiol 2023 FIGURE LEGEND Figure 1. Cumulative numbers of publications on photosynthesis (P) and respiration (R) between 1950 and 2020. A, Publications in representative basic plant biology journals (i.e., Plant Physiology, Plant Cell, New Phytologist, Plant Journal, Plant Cell and Environment, Molecular Plant, Nature Plants, Plant Biology, Trends in Plant Science, Annual Review of Plant Biology, or Annual Review of Plant Physio- logy and Plant Molecular Biology, Annual Review of Plant Physiology). B, Publications in representative crop science journals (i.e., Field Crops Research, Advances in Agronomy, Agronomy Journal, Journal of Agricultural Science, European Journal of Agronomy, Crop Science, Canadian Journal of Plant Science, Australian Journal of Crop Science, Journal of the American Society for Horticultural Science, HortScience, Horticulture Research, Scientia Horticulturae). Insets in each plot show the ratio of respiration to photosynthesis publications (R/P). Data were extracted from the Web of Science database using either ‘photosynthesis’ or ‘respiration + plant’ as search terms along with the list of journal names. ACCECPTED MANUSCRIPT Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad041/7005674 by DeepDyve user on 29 January 2023 ACCECPTED MANUSCRIPT

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PLANT PHYSIOLOGY – Oxford University Press

Published: Jan 30, 2023

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