MicroRNA399s and strigolactones mediate systemic phosphate signaling between dodder-connected host plants and control association of host plants with rhizosphere microbes

A dodder (Cuscuta) often simultaneously parasitizes two or more adjacent hosts. Phosphate (Pi) deficiency is a common stress for plants, and plants often interact with soil microbes, including arbuscular mycorrhizal fungi (AMF), to cope with Pi stress. Little is known about whether dodder transmits Pi deficiency-induced systemic signals between different hosts. In this study, dodder-connected plant clusters, each composed of two tobacco (Nicotiana tabacum) plants connected by a dodder, were established, and in each cluster, one of the two tobacco plants was treated with Pi starvation. AMF colonization efficiency, rhizosphere bacterial community, and transcriptome were analyzed in the other dodder-connected Pi-replete tobacco plant to study the functions of interplant Pi signals. We found that dodder transfers Pi starvation-induced systemic signals between host plants, resulting in enhanced AMF colonization, changes of rhizosphere bacterial communities, and alteration of transcriptomes in the roots of Pi-replete plants. Importantly, genetic analyses indicated that microRNA399s (miR399s) and strigolactones suppress the systemic Pi signals and negatively affect AMF colonization in the Pi-replete plants. These findings provide new insight into the ecological role of dodder in mediating host-host and host-microbe interactions and highlight the importance of strigolactone and miR399 pathways in systemic Pi signaling.