Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes

Abstract

Understanding how the cell uses a limited set of proteins to transduce very different signals into specific cellular responses is a central goal of cell biology and signal transduction disciplines. Although multifunctionality in signal transduction is widespread, the mechanisms that allow differential modes of signaling in multifunctional signaling pathways are not well defined. In legume plants, a common symbiosis signaling pathway composed of at least seven proteins mediates infection by both mycorrhizal fungi and rhizobial bacteria. Here we show that the symbiosis signaling pathway in legumes differentially transduces both bacterial and fungal signals (inputs) to generate alternative calcium responses (outputs). We show that these differential calcium responses are dependent on the same proteins, DMI1 and DMI2, for their activation, indicating an inherent flexibility in this signaling pathway. By using Lyapunov and other mathematical analyses, we discovered that both bacterial-induced and fungal-induced calcium responses are chaotic in nature. Chaotic systems require minimal energy to produce a wide spectrum of outputs in response to marginally different inputs. The flexibility provided by chaotic systems is consistent with the need to transduce two different signals, one from rhizobial bacteria and one from mycorrhizal fungi, by using common components of a single signaling pathway.