Reduced plant water status under sub-ambient pCO₂ limits plant productivity in the wild progenitors of C₃ and C₄ cereals

Background and Aims The reduction of plant productivity by low atmospheric CO₂ partial pressure (pCO₂) during the last glacial period is proposed as a limiting factor for the establishment of agriculture. Supporting this hypothesis, previous work has shown that glacial pCO₂ limits biomass in the wild progenitors of C₃ and C₄ founder crops, in part due to the direct effects of glacial pCO₂ on photosynthesis. Here, we investigate the indirect role of pCO₂ mediated via water status, hypothesizing that faster soil water depletion at glacial (18 Pa) compared to post-glacial (27 Pa) pCO₂, due to greater stomatal conductance, feeds back to limit photosynthesis during drying cycles. Methods We grew four wild progenitors of C₃ and C₄ crops at glacial and post-glacial pCO₂ and investigated physiological changes in gas exchange, canopy transpiration, soil water content and water potential between regular watering events. Growth parameters including leaf area were measured. Key Results Initial transpiration rates were higher at glacial pCO₂ due to greater stomatal conductance. However, stomatal conductance declined more rapidly over the soil drying cycle in glacial pCO₂ and was associated with decreased intercellular pCO₂ and lower photosynthesis. Soil water content was similar between pCO₂ levels as larger leaf areas at post-glacial pCO₂ offset the slower depletion of water. Instead the feedback could be linked to reduced plant water status. Particularly in the C₄ plants, soil–leaf water potential gradients were greater at 18 Pa compared with 27 Pa pCO₂, suggesting an increased ratio of leaf evaporative demand to supply. Conclusions Reduced plant water status appeared to cause a negative feedback on stomatal aperture in plants at glacial pCO₂, thereby reducing photosynthesis. The effects were stronger in C₄ species, providing a mechanism for reduced biomass at 18 Pa. These results have added significance when set against the drier climate of the glacial period.