Lessons from relatives: C4 photosynthesis enhances CO2 assimilation during the low-light phase of fluctuations

Abstract

Despite the global importance of species with C4 photosynthesis, there is a lack of consensus regarding C4 performance under fluctuating light. Contrasting hypotheses and experimental evidence suggest that C4 photosynthesis is either less or more efficient in fixing carbon under fluctuating light than the ancestral C3 form. Two main issues have been identified that may underly the lack of consensus: neglect of evolutionary distance between selected C3 and C4 species and use of contrasting fluctuating light treatments. To circumvent these issues, we measured photosynthetic responses to fluctuating light across three independent phylogenetically controlled comparisons between C3 and C4 species from Alloteropsis, Flaveria, and Cleome genera under 21% and 2% O2. Leaves were subjected to repetitive stepwise changes in light intensity (800 and 100 µmol m-2 s-1 PFD) with three contrasting durations: 6, 30 and 300 seconds. These experiments reconciled the opposing results found across previous studies and showed that 1) stimulation of CO2 assimilation in C4 species during the low light phase was both stronger and more sustained than in C3 species; 2) CO2 assimilation patterns during the high light phase could be attributable to species or C4 subtype differences rather than photosynthetic pathway; and 3) the duration of each light step in the fluctuation regime can strongly influence experimental outcomes.

Differential impact of decreasing relative humidity on photosynthesis under fluctuating light between maize and tomato

“…These results strongly supported that the loss in photosynthetic carbon gain in maize mainly occurred in the first 2 min after transition from low to high light (Lee et al 2022). However, under condition of FL–10 min at 60% relative humidity, no significant difference in the loss in photosynthetic carbon gain was observed between maize and tomato (Figure 3B), which was consistent with the scheme that photosynthetic efficiency during high‐light phase is attributable to species rather than photosynthetic pathway (Arce Cubas et al 2023). Therefore, the previous conclusion that C 4 plants utilize FL less efficiently than C 3 plants should be revised according to the changing frequency of FL.…”

“…Therefore, the changing frequency of FL is an important factor affecting sunfleck utilization efficiency in both maize and tomato. Consistently, a recent study found that photosynthetic efficiency under fluctuating light could be influenced by the fluctuation regime (Arce Cubas et al 2023).…”

“…Based on the characteristics of g s under FL (i.e., decrease of g s at low light and increase of g s at high light), the duration of low light significantly affects the absolute g s before transitioning to high light (Yamori et al 2020; Eyland et al 2021). Therefore, the changing frequency of FL can significantly influence the photosynthetic efficiency during shade‐sun transitions (Arce Cubas et al 2023). The effects of changing the frequency of FL on g s and CO 2 assimilation rate have been well clarified in the C 3 model plant Arabidopsis thaliana (Kimura et al 2020; Yamori et al 2020).…”

“…The effects of changing the frequency of FL on g s and CO 2 assimilation rate have been well clarified in the C 3 model plant Arabidopsis thaliana (Kimura et al 2020; Yamori et al 2020). Furthermore, the changing frequency of FL influences CO 2 assimilation rate during shade‐sun transitions in C 4 species, and C 4 species had stronger and more sustained CO 2 assimilation rate during the low‐light phase in FL compared with C 3 species (Arce Cubas et al 2023). However, it is unclear whether relative humidity interacts with the changing frequency of FL to influence photosynthetic efficiency under FL.…”