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Metabolic scaling theory in plant biology and the three oxygen paradoxa of aerobic life

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Abstract

Alfred Russell Wallace was a field naturalist with a strong interest in general physiology. In this vein, he wrote that oxygen (O2), produced by green plants, is “the food of protoplasm, without which it cannot continue to live”. Here we summarize current models relating body size to respiration rates (in the context of the metabolic scaling theory) and show that oxygen-uptake activities, measured at 21 vol.% O2, correlate closely with growth patterns at the level of specific organs within the same plant. Thus, whole plant respiration can change ontogenetically, corresponding to alterations in the volume fractions of different tissues. Then, we describe the evolution of cyanobacterial photosynthesis during the Paleoarchean, which changed the world forever. By slowly converting what was once a reducing atmosphere to an oxidizing one, microbes capable of O2-producing photosynthesis modified the chemical nature and distribution of the element iron (Fe), slowly drove some of the most ancient prokaryotes to extinction, created the ozone (O3) layer that subsequently shielded the first terrestrial plants and animals from harmful UV radiation, but also made it possible for Earth’s forest to burn, sometimes with catastrophic consequences. Yet another paradox is that the most abundant protein (i.e., the enzyme Rubisco, Ribulose-1,5-biphosphate carboxylase/oxygenase) has a greater affinity for oxygen than for carbon dioxide (CO2), even though its function is to bind with the latter rather than the former. We evaluate this second “oxygen paradox” within the context of photorespiratory carbon loss and crop yield reduction in C3 vs. C4 plants (rye vs. maize). Finally, we analyze the occurrence of reactive oxygen species (ROS) as destructive by-products of cellular metabolism, and discuss the three “O2-paradoxa” with reference to A. R. Wallace’s speculations on “design in nature”.

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Acknowledgments

This work was supported by the Alexander von Humboldt Foundation, Bonn, Germany (AvH Fellowships Stanford 2011/2012 to UK).

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Authors and Affiliations

  1. Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, 34132, Kassel, Germany

    Ulrich Kutschera

  2. Department of Plant Biology, Cornell University, Ithaca, NY, 14853, USA

    Karl J. Niklas

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  1. Ulrich Kutschera
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Correspondence to Ulrich Kutschera.

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This article is a contribution to the Special issue Alfred Russel Wallace (1823–1913): The man in the shadow of Charles Darwin—Guest Editors U. Kutschera, U. Hossfeld.

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Kutschera, U., Niklas, K.J. Metabolic scaling theory in plant biology and the three oxygen paradoxa of aerobic life. Theory Biosci. 132, 277–288 (2013). https://doi.org/10.1007/s12064-013-0194-3

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