Increasing plant group productivity through latent genetic variation for cooperation

Technologies for crop breeding have become increasingly sophisticated, yet it remains unclear whether these advances are sufficient to meet future demands. A major challenge with current crop selection regimes is that they are often based on individual performance. This tends to select for plants with “selfish” traits, which leads to a yield loss when they compete in high-density stands. In traditional breeding, this well-known “tragedy of the commons” has been addressed by anticipating ideotypes with presumably preferential characteristics. However, this approach is limited to obvious architectural and physiological traits, and it depends on a mechanistic understanding of how these modulate growth and competition. Here, we developed a general and simple method for the discovery of alleles promoting cooperation of plants in stands; it is based on the game-theoretical premise that alleles increasing cooperation incur a cost to the individual but benefit the monoculture group. Testing the approach using the model plant Arabidopsis thaliana, we found a single major effect locus where the rarer allele was associated with increased levels of cooperation and superior monoculture productivity. We show that the allele likely affects a pleiotropic regulator of growth and defense, since it is also associated with reduced root competition but higher race-specific resistance against a specialized parasite. Even though cooperation is considered evolutionarily unstable, conflicting selective forces acting on a pleiotropic gene might thus maintain latent genetic variation for it in nature. Such variation, once identified in a crop, could be rapidly leveraged in modern breeding programs and provide efficient routes to increase yields.