Pisum sativum Response to Nitrate as Affected by Rhizobium leguminosarum-Derived Signals

Legumes are suitable for the development of sustainable agroecosystems because of their ability to use atmospheric N₂ through symbiotic nitrogen fixation (SNF). However, a basic NO₃^- input is necessary before SNF takes place to ensure successful seedling establishment. Since Rhizobia not only induce nodulation but also affect root branching by stimulating the development of lateral roots, and NO₃^- as a signal also modulates root system architecture, we investigated whether Rhizobium-derived signals interfere in nitrate signaling. Here, we bring evidence that (i) Rhizobium-altered NO₃^--mediated processes in pea expressions of major players in NO₃^- transport, sensing, and signaling were affected, and (ii) the characteristic limitation of root foraging and branching in response to NO₃^- supply was abolished. The number of tertiary roots per secondary root was higher in infected compared to uninfected peas, thus indicating that the Rhizobium effect allows for favorable management of trade-offs between nodules growth for nitrogen capture and root foraging for water and other nutrient uptake in pea. The outcome of this basic research can be used to produce molecular tools for breeding pea genotypes able to develop deep-foraging and branched root systems, and more competitive architectures and molecular levels for soil NO₃^- absorption during seedling establishment without jeopardizing nodulation.