Response of wild C4 crop progenitors to subambient CO2 highlights a possible role in the origin of agriculture

The synchronous origin of agriculture in at least four independent climatic regions at the end of the last glacial period (c10 kyr BP) points to a global limitation for crop domestication. One hypothesis proposes that a rapid carbon dioxide (CO(2)) increase from 18 Pa to similar to 27 Pa during deglaciation caused significant increases in the growth rates of wild crop progenitors, thereby removing a productivity barrier to their successful domestication. However, early C(4) crops present a challenge to this hypothesis, because they were among the first domesticates, but have a carbon-concentrating mechanism that offsets the limitation of photosynthesis by CO(2). We investigated the CO(2)-limitation hypothesis using the wild progenitors of five C(4) founder crops from four independent centres of domestication. Plants were grown in controlled environment chambers at glacial (18 Pa), postglacial (28 Pa) and current ambient (38 Pa) CO(2) levels, and photosynthesis, transpiration and biomass were measured. An increase in CO(2) from glacial to postglacial levels caused a significant gain in vegetative biomass of up to 40%, but the equivalent rise in CO(2) from postglacial to modern levels generally had no effect on biomass. Investigation into the underlying mechanisms showed C(4) photosynthesis to be limited more by glacial than postglacial CO(2) levels, matching theoretical expectations. Moreover, the increase in CO(2) from glacial to postglacial levels caused a reduction in the transpiration rate via decreases in stomatal conductance of similar to 35%. In combination, these physiological changes conferred a large improvement in water-use efficiency at the postglacial CO(2) partial pressure compared with the glacial level. Our data, therefore, provide experimental support for the CO(2)-limitation hypothesis, suggesting that these key physiological changes could have greatly enhanced the productivity of wild crop progenitors after deglaciation.