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

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.YZ was supported by a Shaanxi Provincial Talent 100 Fellowship, a Chinese Natural Science Foundation grant (NSFC 41773032) and a Shaanxi Department of Education grant (17JS013). KG was supported by the ARC Discovery Project series (DP130100577 and DP1096729). GDF & AG were supported by the Alexander-vonHumboldt foundation (Humboldt Research Award to GDF)

Hydrogen isotopic differences between C3 and C4 land plant lipids: consequences of compartmentation in C4 photosynthetic chemistry and C3 photorespiration

The 2H/1H ratio of carbon-bound H in biolipids holds potential for probing plant lipid biosynthesis and metabolism. The biochemical mechanism underlying the isotopic differences between lipids from C3 and C4 plants is still poorly understood. GC-pyrolysis-IRMS (gas chromatography-pyrolysis-isotope ratio mass spectrometry) measurement of the 2H/1H ratio of leaf lipids from controlled and field grown plants indicates that the biochemical isotopic fractionation (ε2Hlipid_biochem) differed between C3 and C4 plants in a pathway-dependent manner: ε2HC4 > ε2HC3 for the acetogenic pathway, ε2HC4 < ε2HC3 for the mevalonic acid pathway and the 1-deoxy-D-xylulose 5-phosphate pathway across all species examined. It is proposed that compartmentation of photosynthetic CO2 fixation into C4 mesophyll (M) and bundle sheath (BS) cells and suppression of photorespiration in C4 M and BS cells both result in C4 M chloroplastic pyruvate – the precursor for acetogenic pathway – being more depleted in 2H relative to pyruvate in C3 cells. In addition, compartmentation in C4 plants also results in (i) the transferable H of NADPH being enriched in 2H in C4 M chloroplasts compared with that in C3 chloroplasts for the 1-deoxy-D-xylulose 5-phosphate pathway pathway and (ii) pyruvate relatively 2H-enriched being used for the mevalonic acid pathway in the cytosol of BS cells in comparison with that in C3 cells