Acclimation to enhanced photorespiratory conditions increases the effectiveness of C 2 photosynthesis in C 3 -C 4 intermediates

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Abstract

  • C 2 photosynthesis reduces photorespiratory carbon loss by shuttling glycine from mesophyll (M) to bundle sheath (BS) tissues, where glycine decarboxylase (GDC) releases CO 2 that accumulates around rubisco. C 2 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 C 3 to C 2 phenotypes at 32 °C days and 200 or 800 µmol mol -1 CO 2 . 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 CO 2 enhanced C 2 -related phenotypes in sub-C 2 and C 2 species but not C 3 or proto-Kranz species. Sub-C 2 species positioned chloroplasts closer to mitochondria and had lower modelled BS conductance. C 2 species increased rubisco capacity and GDC allocation to the BS. Aspartate aminotransferase activity increased in both sub-C 2 and C 2 species.

  • Acclimation to greater photorespiratory conditions strengthens C 2 photosynthesis, but only in species whose BS has crossed a threshold of organelle and GDC investment. We hypothesize that acclimation could expose C 2 -related traits to selection and facilitate the origin of C 4 photosynthesis.

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