Roles for leakiness and O2 evolution in explaining lower-than-theoretical quantum yields of photosynthesis in the PEP-CK subtype of C4 plants

Abstract

Theoretically, the PEP-CK C₄ subtype has a higher quantum yield of CO₂ assimilation ( ${\Phi }_{{\mathrm{CO}}_2}$ ) than NADP-ME or NAD-ME subtypes because ATP required for operating the CO₂-concentrating mechanism is believed to mostly come from the mitochondrial electron transport chain (mETC). However, reported ${\Phi }_{{\mathrm{CO}}_2}$ is not higher in PEP-CK than in the other subtypes. We hypothesise, more photorespiration, associated with higher leakiness and O₂ evolution in bundle-sheath (BS) cells, cancels out energetic advantages in PEP-CK species. Nine species (two to four species per subtype) were evaluated by gas exchange, chlorophyll fluorescence, and two-photon microscopy to estimate the BS conductance (g_bs) and leakiness using a biochemical model. Average g_bs estimates were 2.9, 4.8, and 5.0 mmol m^-2 s^-1 bar^-1, and leakiness values were 0.129, 0.179, and 0.180, in NADP-ME, NAD-ME, and PEP-CK species, respectively. The BS CO₂ level was somewhat higher, O₂ level was marginally lower, and thus, photorespiratory loss was slightly lower, in NADP-ME than in NAD-ME and PEP-CK species. Differences in these parameters existed among species within a subtype, and g_bs was co-determined by biochemical decarboxylating sites and anatomical characteristics. Our hypothesis and results partially explain variations in observed ${\Phi }_{{\mathrm{CO}}_2}$ , but suggest that PEP-CK species probably use less ATP from mETC than classically defined PEP-CK mechanisms.

Keywords: C4 subtypes; fluorescence microscopy; light use efficiency; modelling; quantum efficiency.