In natural populations, plants with greater photosynthetic rates can accumulate more biomass and thus have greater fitness than plants with lower carbon uptake and assimilation rates. Photorespiration reduces the photosynthetic efficiency of C3 plants by almost half but has persisted in C3 plants for millennia. Recent evidence suggests that photorespiration, while diverting energy away from carbon assimilation, provides other metabolic benefits that might enhance fitness. Consistent with this notion, photosynthesis and photorespiration are thought to be co-regulated at a metabolic level. However, and despite a near complete description of the photorespiratory pathway and thorough understanding of the response of photorespiration to environmental stimuli, surprisingly little is known about genetic variation in photorespiration and its covariation with photosynthesis in natural populations. We hypothesized that the molecular coordination of photosynthesis and photorespiration would manifest as positive phenotypic and genetic correlations. We assessed natural variation and covariation for photosynthesis and photorespiration among 14 ecotypes Arabidopsis thaliana. The ecotypes were selected to represent physiological variation in photosynthetic capacity, life history (winter and spring annual) and habitat (mean annual precipitation, mean annual temperature). Photosynthesis and photorespiration were estimated by measuring the response of photosynthesis to intercellular [CO2] at ambient O2 and 1% O2 to simulate non-photorespiratory conditions. Photosynthesis and its associated parameters were estimated from the A vs Ci curves at ambient O2. Photorespiration was estimated as photorespiratory CO2 efflux by combining gas exchange and chlorophyll fluorescence data collected at ambient O2 and 1% O2.
Results/Conclusions
Phenotypic variation in photorespiratory CO2 efflux was highly correlated with photosynthetic rates and two metrics of photosynthetic capacity, maximum carboxylation capacity (Vc,max) and maximum linear electron flux through photosystem II (Jmax). However, genetic correlations were not detected between photosynthesis and photorespiration. We found standing genetic variation—as broad-sense heritability—for most photosynthetic traits, including photorespiration. Genetic correlation between photosynthetic electron transport and carboxylation capacities indicates that these traits are genetically constrained. Genetic correlations between traits supplying energy and carbon to the Calvin–Benson cycle are consistent with the biochemical model of photosynthesis, suggesting that selection on either of these traits would improve all of them. Interestingly, the lack of a genetic correlation between photosynthesis and photorespiration suggests that the positive scaling of these two traits can be broken.