Why Are C3-C4 Intermediate Species Rare?

Abstract:

While C₃-C₄ intermediate photosynthesis is thought to represent the evolutionary bridge between C₃ and C₄ photosynthesis, C₃-C₄ intermediate species are ecologically rare in comparison to both C₃ and C₄ species. Here, we report results from a laboratory experiment, field observations, and model simulations that suggest a new explanation for the ecological rarity of C₃-C₄ intermediate species. In the laboratory experiment, we combined gas exchange and fluorescence to characterize the temperature response of photosynthesis in three closely-related species in the genus Flaveria that are representatives of the C₃, C₃-C₄ intermediate, and C₄ photosynthetic pathways. The leaf temperature that maximized the quantum yield for CO₂ assimilation (T_opt(Φ_CO2)) was 24.9 ± 0.7°C in Flaveria robusta (C₃), 29.8 ± 1.0°C in F. chloraefolia (C₃-C₄), and 35.7 ± 0.8°C in F. bidentis (C₄), and was linearly related to the temperature sensitivity of the coupling between CO₂ assimilation and electron transport (d(Φ_CO2/ Φ_PSII)/dT)). While F. chloraefolia does not simultaneously occur with F. robusta and F. bidentis in naturally-assembled communities, this C₃-C₄ intermediate species does occur with other C₃ and C₄ species. During the growing season in two of these mixed-photosynthetic-type communities, leaf temperatures for F. chloraefolia were similar to the T_opt(Φ_CO2) determined in the laboratory. A model of maximum potential carbon gain suggests that competitive coexistence of C₃, C₃-C₄ intermediate, and C₄ species could be dependent on a temperature regime that highlights the distinct relative advantages of the C₃-C₄ intermediate pathway. In combination, these results suggest that the relative temperature sensitivity of the C₃, C₃-C₄ intermediate, and C₄ photosynthetic pathways combined with environmental variation in temperature may help to explain why C₃-C₄ intermediate species are generally rare.