Dodder seedlings benefit from apoplastic nutrition by inducing SWEET15-mediated unloading of sucrose from the host's...

Cuscuta species are holoparasitic plants that penetrate host stems with haustoria, connect to the vasculature and exhaust water, nutrients and carbohydrates. Parasite seedlings possess only limited maternal reserves and the development of a vascular connection takes several days. Until then, an alternative access to host assimilates is critical for the survival of the parasite. Here, we investigated the sucrose flux and nutrition mechanisms of dodder during early infection. Using phloem-mobile fluorescent tracers, we show that an apoplastic sucrose transfer occurs before symplastic connections between host and parasite are formed. We identified sucrose transporters of both dodder and host that are critical for assimilate transfers. CrSUT1, CrSUT3 and CrSWEET10 mediate sucrose transport during haustorium development. In the phloem of Arabidopsis, at the infection site, the sucrose-exporter AtSWEET15 is induced through basic leucine zipper transcription factors. CrSUT2 was identified as a transporter for sucrose uptake into the invading haustorium. The growth of dodder seedlings on atsweet15 hosts is reduced, demonstrating the importance of the sucrose export by AtSWEET15 and availability within the apoplast. Our data highlight the relevance of apoplastic nutrition for the survival of parasitic plants. Dodder manipulates the host, causing it to release carbohydrates from its phloem during the initial infection.