On the contributions of photorespiration and compartmentation to the contrasting intramolecular ²H profiles of C₃ and C₄ plant sugars

Abstract

Compartmentation of C₄ photosynthetic biochemistry into bundle sheath (BS) and mesophyll (M) cells, and photorespiration in C₃ plants is predicted to have hydrogen isotopic consequences for metabolites at both molecular and site-specific levels. Molecular-level evidence was recently reported (Zhou et al., 2016), but evidence at the site-specific level is still lacking. We propose that such evidence exists in the contrasting ²H distribution profiles of glucose samples from naturally grown C₃, C₄ and CAM plants: photorespiration contributes to the relative ²H enrichment in H⁵ and relative ²H depletion in H¹ & H⁶ (the average of the two pro-chiral Hs and in particular H⁶, ^pro-R) in C₃ glucose, while ²H-enriched C₃ mesophyll cellular (chloroplastic) water most likely contributes to the enrichment at H₄; export of (transferable hydrogen atoms of) NADPH from C₄ mesophyll cells to bundle sheath cells (via the malate shuttle) and incorporation of ²H-relatively unenriched BS cellular water contribute to the relative depletion of H⁴ & H⁵ respectively; shuttling of triose-phosphates (PGA: phosphoglycerate dand DHAP: dihydroacetone phosphate) between C4 bundle sheath and mesophyll cells contributes to the relative enrichment in H¹ & H⁶ (in particular H⁶, ^pro-R) in C₄ glucose.

Keywords

Sugar biosynthesis, Intramolecular 2H distribution, Isotope effect, C3 photorespiration, C4 compartmentation

Citation

Zhou, Youping; Zhang, Benli; Stuart-Williams, Hilary; Grice, Kliti; Hocart, Charles H.; Gessler, Arthur; Kayler, Zachary E.; Farquhar, Graham D. 2018. On the contributions of photorespiration and compartmentation to the contrasting intramolecular ²H profiles of C₃ and C₄ plant sugars. Phytochemistry. 145: 197-206. https://doi.org/10.1016/j.phytochem.2017.11.004.