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In vivo phosphoenolpyruvate carboxylase activity is controlled by CO2 and O2 mole fractions and represents a major flux at high photorespiration rates

Abadie, Cyril, Tcherkez, Guillaume
Thenew phytologist 2019 v.221 no.4 pp. 1843-1852
C3 plants, Helianthus annuus, bicarbonates, carbon, carbon dioxide, enzyme activity, fumarate hydratase, gas exchange, leaves, malates, nuclear magnetic resonance spectroscopy, oxygen, phosphoenolpyruvate carboxylase, photorespiration, stable isotopes
Phosphenolpyruvate carboxylase (PEPC)‐catalysed fixation of bicarbonate to C₄ acids is commonly believed to represent a rather small flux in illuminated leaves. In addition, its potential variation with O₂ and CO₂ is not documented and thus is usually neglected in gas‐exchange studies. Here, we used quantitative NMR analysis of sunflower leaves labelled with ¹³CO₂ (99% ¹³C) under controlled conditions and measured the amount of ¹³C found in the four C‐atom positions in malate, the major product of PEPC activity. We found that amongst malate ¹³C‐isotopomers present after labelling, most molecules were labelled at both C‐1 and C‐4, showing the incorporation of ¹³C at C‐4 by PEPC fixation and subsequent redistribution to C‐1 by fumarase (malate–fumarate equilibrium). In addition, absolute quantification of ¹³C content showed that PEPC fixation increased at low CO₂ or high O₂, and represented up to 1.8 μmol m⁻² s⁻¹, that is, 40% of net assimilation measured by gas exchange under high O₂/CO₂ conditions. Our results show that PEPC fixation represents a quantitatively important CO₂‐fixing activity that varies with O₂ and/or CO₂ mole fraction and this challenges the common interpretation of net assimilation in C₃ plants, where PEPC activity is often disregarded or considered to be constant at a very low rate.