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.