Acclimation to enhanced photorespiratory conditions increases the effectiveness of C2 photosynthesis in C3-C4 intermediates

Abstract

- C2 photosynthesis reduces photorespiratory carbon loss by shuttling glycine from mesophyll (M) to bundle sheath (BS) tissues, where glycine decarboxylase (GDC) releases CO2 that accumulates around rubisco. C2 photosynthesis has been considered a constitutive character, but as a metabolic trait, it may acclimate to the rate of photorespiratory glycine production. - We grew eleven species from two eudicot and two grass lineages spanning C3 to C2 phenotypes at 32 {degrees}C days and 200 or 800 {micro}mol mol-1 CO2. Acclimation was assessed using leaf gas exchange, GDC P-protein immunolocalization, M and BS ultrastructure, photosynthetic enzyme activity, and photosynthesis modelling. - Low relative to high growth CO2 enhanced C2-related phenotypes in sub-C2 and C2 species but not C3 or proto-Kranz species. Sub-C2 species positioned chloroplasts closer to mitochondria and had lower modelled BS conductance. C2 species increased rubisco capacity and GDC allocation to the BS. Aspartate aminotransferase activity increased in both sub-C2 and C2 species. - Acclimation to greater photorespiratory conditions strengthens C2 photosynthesis, but only in species whose BS has crossed a threshold of organelle and GDC investment. We hypothesize that acclimation could expose C2-related traits to selection and facilitate the origin of C4 photosynthesis.