title: Metabolic scaling theory in plant biology and the three oxygen paradoxa of aerobic life.
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".
authors: Institute of Biology, University of Kassel, Heinrich-Plett-Str. 40, 34132, Kassel, Germany, kut@uni-kassel.de.
authors: Ulrich
authors: U
authors: Kutschera
authors: Karl J
authors: KJ
authors: Niklas
mesh_terms: D000332:Aerobiosis; D000818:Animals; D005075:Biological Evolution; D001695:Biology / Q000266:history*; D001901:Botany / Q000266:history*; D049672:History, 19th Century; D049673:History, 20th Century; D008954:Models, Biological; D010100:Oxygen / Q000378:metabolism*; D010101:Oxygen Consumption; D010788:Photosynthesis / Q000502:physiology; D018521:Plant Physiological Phenomena; D010944:Plants / Q000378:metabolism; D017382:Reactive Oxygen Species
chemical_list: D017382:Reactive Oxygen Species; D010100:Oxygen
references: Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):869-85
references: 16754604
references: Science. 2009 Apr 24;324(5926):481-4
references: 19390038
references: Plant Sci. 2013 Jun;207:45-56
references: 23602098
references: J Exp Bot. 2012 Jun;63(10):3511-22
references: 22547659
references: Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11238-43
references: 23798417
references: Theory Biosci. 2005 Aug;124(1):1-24
references: 17046345
references: Am Nat. 2013 Mar;181(3):421-39
references: 23448890
references: New Phytol. 2011 Apr;190(2):431-41
references: 21118258
references: Theory Biosci. 2007 Apr;125(2):81-92
references: 17412289
references: New Phytol. 2010 Jan;185(1):27-41
references: 19863728
references: Biol Rev Camb Philos Soc. 2005 Nov;80(4):611-62
references: 16221332
references: J Physiol. 2008 Jan 1;586(1):83-95
references: 17947307
references: Biochem Soc Symp. 1995;61:1-31
references: 8660387
references: Science. 1993 Apr 30;260:640-6
references: 11539831
references: Plant Physiol. 2006 Jun;141(2):312-22
references: 16760481
references: Nature. 2003 Sep 18;425(6955):282-5
references: 13679913
references: J Exp Bot. 2013 Jan;64(3):717-30
references: 23162118
references: Naturwissenschaften. 2009 Nov;96(11):1339-54
references: 19763527
references: Science. 2013 Jun 14;340(6138):1287
references: 23766310
references: Nature. 2010 Oct 21;467(7318):929-34
references: 20962839
references: New Phytol. 2013 Apr;198(1):1-3
references: 23432200
references: Naturwissenschaften. 2004 Jun;91(6):255-76
references: 15241603
references: Ecol Lett. 2009 Jan;12(1):75-92
references: 19016828
references: Nucleic Acids Res. 2009 May;37(8):2539-48
references: 19264794
references: J Appl Physiol. 1953 Sep;6(3):189-93
references: 13096460
references: Theory Biosci. 2008 Aug;127(3):277-89
references: 18581157
references: J Exp Bot. 2011 May;62(9):2989-3000
references: 21652533
references: Theory Biosci. 2009 Aug;128(3):191-203
references: 19399544
references: Annu Rev Plant Biol. 2004;55:373-99
references: 15377225
references: Plant Signal Behav. 2010 May;5(5):509-17
references: 20234181
references: Science. 1954 May 7;119(3097):623-6
references: 13156638
references: Philos Trans R Soc Lond B Biol Sci. 2010 Jan 12;365(1537):111-32
references: 20008390
references: Plant Physiol Biochem. 2010 Dec;48(12):909-30
references: 20870416
references: Photosynth Res. 2004;80(1-3):373-86
references: 16328834
references: Biofactors. 2006;28(2):73-81
references: 17379938
references: New Phytol. 2010 Nov;188(3):696-710
references: 20819176
references: Science. 2010 May 7;328(5979):704-8
references: 20448176
references: Science. 2011 Aug 26;333(6046):1109-12
references: 21868666
references: Science. 2011 Oct 14;334(6053):184-5
references: 21998376
references: J Plant Physiol. 2007 Nov;164(11):1395-409
references: 17905474
references: Biol Rev Camb Philos Soc. 2004 Nov;79(4):871-89
references: 15682874
references: Photosynth Res. 2011 Jan;107(1):87-101
references: 20607406
references: Protoplasma. 2012 Jul;249(3):469-81
references: 21805384
references: Cell. 2012 Mar 16;148(6):1145-59
references: 22424226
references: Biol Direct. 2011 Jun 30;6:33
references: 21714937
references: Physiol Plant. 2010 Apr;138(4):414-29
references: 20002601
references: Planta. 2002 Nov;216(1):38-43
references: 12430012
references: Plant Signal Behav. 2011 Jan;6(1):72-6
references: 21301213
references: Autophagy. 2012 Mar;8(3):426-8
references: 22302001
references: Protoplasma. 2012 Oct;249(4):1049-57
references: 22016107
references: Plant Signal Behav. 2011 Nov;6(11):1700-5
references: 22057328
references: Proc Natl Acad Sci U S A. 2006 Jul 18;103(29):10861-5
references: 16832054