A tomato phloem-mobile protein regulates the shoot-to-root ratio by mediating the auxin response in distant organs

The plant vascular system serves as a conduit for delivery of both nutrients and signaling molecules to various distantly located organs. The anucleate sieve tube system of the angiosperm phloem delivers sugars and amino acids to developing organs, and has recently been shown to contain a unique population of RNA and proteins. Grafting studies have established that a number of these macromolecules are capable of moving long distances between tissues, thus providing support for operation of a phloem-mediated inter-organ communication network. Currently, our knowledge of the roles played by such phloem-borne macromolecules is in its infancy. Here, we show that, in tomato, translocation of a phloem-mobile cyclophilin, SlCyp1, from a wild-type scion into a mutant rootstock results in restoration of vascular development and lateral root initiation. This process occurs through reactivation of auxin response pathways and reprogramming of the root transcriptome. Moreover, we show that long-distance trafficking of SlCyp1 is associated with regulation of the shoot-to-root ratio in response to changing light intensities, by modulating root growth. We conclude that long-distance trafficking of SlCyp1 acts as a rheostat to control the shoot-to-root ratio, by mediating root development to integrate photosynthesis and light intensity with requirements for access to water and mineral nutrients. Significance Statement Plants must coordinate metabolism and growth of their organs to develop under changing environmental conditions. Here we show that a phloem cyclophilin, SlCyp1, accumulates in leaves as a function of light intensity and trafficks from shoot to root, resulting in major transcriptional changesrelated to auxin responses, and thus increased lateral root development. We propose that SlCyp1 acts as a rheostat that integrates leaf photosynthetic capacity with root growth under varying environmental conditions.