Root Exudates Drive Interspecific Facilitation By Enhancing Nodulation and N2 Fixation.

Plant diversity in experimental systems often enhances ecosystem productivity, but the mechanisms causing this overyielding are only partly understood.  Intercropping faba beans (Vicia faba L.) and maize (Zea mays L.) results in overyielding, and also enhances nodulation by faba beans. By using permeable and impermeable root barriers in a two-year field experiment, we show that root-root interactions between faba bean and maize significantly increase both nodulation and symbiotic N₂ fixation in intercropped faba bean.  Furthermore, root exudates from maize promote faba bean nodulation, whereas root exudates from wheat and barley do not.  Thus a decline of soil nitrate concentrations caused by intercropped cereals is not the sole mechanism for maize promoting faba bean nodulation.  Intercropped maize also caused a two-fold increase in exudation of flavonoids (signaling compounds for rhizobia) in the systems.  Roots of faba bean treated with maize root exudates exhibited an immediate 11-fold increase in the expression of chalcone-flavanone isomerase (involved in flavonoid synthesis) gene, together with a significantly increased expression of genes mediating nodulation and auxin response.  After 35 days, faba beans treated with maize root exudate continued to demonstrate up-regulation of key nodulation genes such as ENOD93, and promoted nitrogen fixation.  Our results reveal a mechanism for how intercropped maize promotes nitrogen fixation of faba bean, where maize root exudates promote flavonoid synthesis in faba bean, increase nodulation, and stimulate nitrogen fixation following enhanced gene expression.  These results indicate facilitative root-root interactions and provide a mechanism for a positive relationship between species diversity and ecosystem productivity.