Elevated nocturnal respiratory rates in the mitochondria of CAM plants: current knowledge and unanswered questions

Leverett, Alistair; Borland, Anne M.

doi:10.1093/aob/mcad119

Title: Elevated nocturnal respiratory rates in the mitochondria of CAM plants: current knowledge and unanswered questions

Journal Article · 27 August 2023 · Annals of Botany

DOI: https://doi.org/10.1093/aob/mcad119 · OSTI ID:2282234

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Abstract Crassulacean acid metabolism (CAM) is a metabolic adaptation that has evolved convergently in 38 plant families to aid survival in water-limited niches. Whilst primarily considered a photosynthetic adaptation, CAM also has substantial consequences for nocturnal respiratory metabolism. Here, we outline the history, current state and future of nocturnal respiration research in CAM plants, with a particular focus on the energetics of nocturnal respiratory oxygen consumption. Throughout the 20th century, research interest in nocturnal respiration occurred alongside initial discoveries of CAM, although the energetic and mechanistic implications of nocturnal oxygen consumption and links to the operation of the CAM cycle were not fully understood. Recent flux balance analysis (FBA) models have provided new insights into the role that mitochondria play in the CAM cycle. Several FBA models have predicted that CAM requires elevated nocturnal respiratory rates, compared to C3 species, to power vacuolar malic acid accumulation. We provide physiological data, from the genus Clusia, to corroborate these modelling predictions, thereby reinforcing the importance of elevated nocturnal respiratory rates for CAM. Finally, we outline five unanswered questions pertaining to nocturnal respiration which must be addressed if we are to fully understand and utilize CAM plants in a hotter, drier world.

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Research Organization:: University of Nevada, Reno, NV (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0008834

OSTI ID:: 2282234

Journal Information:: Annals of Botany, Journal Name: Annals of Botany Journal Issue: 4 Vol. 132; ISSN 0305-7364

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Engineering of Crassulacean Acid Metabolism Schiller, Katharina; Bräutigam, Andrea Annual Review of Plant Biology, Vol. 72, Issue 1 https://doi.org/10.1146/annurev-arplant-071720-104814	journal	June 2021
Crassulacean Acid Metabolism Ranson, S. L.; Thomas, M. Annual Review of Plant Physiology, Vol. 11, Issue 1 https://doi.org/10.1146/annurev.pp.11.060160.000501	journal	June 1960
Crassulacean Acid Metabolism: A Curiosity in Context Osmond, C. B. Annual Review of Plant Physiology, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.pp.29.060178.002115	journal	June 1978
The Regulation of CAM and Respiratory Recycling by Water Supply and Light Regime in the C 3 -CAM Intermediate Sedum telephium Borland, A. M.; Griffiths, H. Functional Ecology, Vol. 4, Issue 1 https://doi.org/10.2307/2389649	journal	January 1990
Updating the occurrence of crassulacean acid metabolism (CAM) in the genus Clusia through carbon isotope analysis of species from Colombia Pachon, P.; Winter, K.; Lasso, E. Photosynthetica, Vol. 60, Issue 2 https://doi.org/10.32615/ps.2022.018	journal	May 2022
Altered Gene Regulatory Networks Are Associated With the Transition From C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae) Heyduk, Karolina; Hwang, Michelle; Albert, Victor Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.02000	journal	January 2019
Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis Lim, Sung Don; Lee, Sojeong; Choi, Won-Gyu Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00101	journal	February 2019
Metabolic Modeling of the C3-CAM Continuum Revealed the Establishment of a Starch/Sugar-Malate Cycle in CAM Evolution Tay, Ignacius Y. Y.; Odang, Kristoforus Bryant; Cheung, C. Y. Maurice Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.573197	journal	January 2021
CAM Models: Lessons and Implications for CAM Evolution Burgos, Asdrubal; Miranda, Enoc; Vilaprinyo, Ester Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.893095	journal	June 2022
Membrane Profiling by Free Flow Electrophoresis and SWATH-MS to Characterize Subcellular Compartment Proteomes in Mesembryanthemum crystallinum Guo, Qi; Liu, Lei; Yim, Won C. International Journal of Molecular Sciences, Vol. 22, Issue 9 https://doi.org/10.3390/ijms22095020	journal	May 2021

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