Drought constraints on C4 photosynthesis:: stomatal and metabolic limitations in C3 and C4 subspecies of Alloteropsis semialata

The C-4 photosynthetic pathway uses water more efficiently than the C-3 type, yet biogeographical analyses show a decline in C-4 species relative to C-3 species with decreasing rainfall. To investigate this paradox, the hypothesis that the C-4 advantage over C-3 photosynthesis is diminished by drought was tested, and the underlying stomatal and metabolic mechanisms of this response determined. The effects of drought and high evaporative demand on leaf gas exchange and photosynthetic electron sinks in C-3 and C-4 subspecies of the grass Alloteropsis semialata were examined. Plant responses to climatic variation and soil drought were investigated using a common garden experiment with well-watered and natural rainfall treatments, and underlying mechanisms analysed using controlled drying pot experiments. Photosynthetic rates were significantly higher in the C-4 than the C-3 subspecies in the garden experiment under well-watered conditions, but this advantage was completely lost during a rainless period when unwatered plants experienced severe drought. Controlled drying experiments showed that this loss was caused by a greater increase in metabolic, rather than stomatal, limitations in C-4 than in the C-3 leaves. Decreases in CO2 assimilation resulted in lower electron transport rates and decreased photochemical efficiency under drought conditions, rather than increased electron transport to alternative sinks. These findings suggest that the high metabolic sensitivity of photosynthesis to severe drought seen previously in several C-4 grass species may be an inherent characteristic of the C-4 pathway. The mechanism may explain the paradox of why C-4 species decline in arid environments despite high water-use efficiency.