Stem parasitic plant <i>Cuscuta australis</i> (dodder) transfers herbivory-induced signals among plants

Abstract

<i>Cuscuta</i> spp. (i.e., dodders) are stem parasites that naturally graft to their host plants to extract water and nutrients; multiple adjacent hosts are often parasitized by one or more <i>Cuscuta</i> plants simultaneously, forming connected plant clusters. Metabolites, proteins, and mRNAs are known to be transferred from hosts to <i>Cuscuta</i>, and <i>Cuscuta</i> bridges even facilitate host-to-host virus movement. Whether <i>Cuscuta</i> bridges transmit ecologically meaningful signals remains unknown. Here we show that, when host plants are connected by <i>Cuscuta</i> bridges, systemic herbivory signals are transmitted from attacked plants to unattacked plants, as revealed by the large transcriptomic changes in the attacked local leaves, undamaged systemic leaves of the attacked plants, and leaves of unattacked but connected hosts. The interplant signaling is largely dependent on the jasmonic acid pathway of the damaged local plants, and can be found among conspecific or heterospecific hosts of different families. Importantly, herbivore attack of one host plant elevates defensive metabolites in the other systemic <i>Cuscuta</i> bridge-connected hosts, resulting in enhanced resistance against insects even in several consecutively <i>Cuscuta</i>-connected host plants over long distances (> 100 cm). By facilitating plant-to-plant signaling, <i>Cuscuta</i> provides an information-based means of countering the resource-based fitness costs to their hosts.