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Cuscuta australis (dodder) parasite eavesdrops on the host plants’ FT signals to flower

Guojing Shen,Nian Liu,Jingxiong Zhang,Yuxing Xu,I. Baldwin,Jianqiang Wu

Published 2020 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance In many plants, flowering is regulated by environmental cues, such as day length. Under flowering-inductive conditions, leaves synthesize and transmit FLOWERING LOCUS T (FT) protein to the shoot apex, where FT activates flowering. Dodder Cuscuta australis, which is a root- and leafless parasitic plant, however, very likely does not have fully functional FT genes, and it flowers only when the host plants flower. We show that host-synthesized FT protein is able to move into dodder stems, where FT physically interacts with dodder FD transcription factor, activating flowering of dodder. This specific manner of flowering allows dodder to synchronize its flowering time with that of the host plant, and this is likely a trait that is beneficial for dodder’s reproductive success. Many plants use environmental cues, including seasonal changes of day length (photoperiod), to control their flowering time. Under inductive conditions, FLOWERING LOCUS T (FT) protein is synthesized in leaves, and FT protein is a mobile signal, which is able to travel to the shoot apex to induce flowering. Dodders (Cuscuta, Convolvulaceae) are root- and leafless plants that parasitize a large number of autotrophic plant species with varying flowering time. Remarkably, some dodder species, e.g., Cuscuta australis, are able to synchronize their flowering with the flowering of their hosts. Detailed sequence inspection and expression analysis indicated that the FT gene in dodder C. australis very likely does not function in activating flowering. Using soybean host plants cultivated under inductive and noninductive photoperiod conditions and soybean and tobacco host plants, in which FT was overexpressed and knocked out, respectively, we show that FT-induced flowering of the host is likely required for both host and parasite flowering. Biochemical analysis revealed that host-synthesized FT signals are able to move into dodder stems, where they physically interact with a dodder FD transcription factor to activate dodder flowering. This study demonstrates that FTs can function as an important interplant flowering signal in host–dodder interactions. The unique means of flowering regulation of dodder illustrates how regressive evolution, commonly found in parasites, may facilitate the physiological synchronization of parasite and host, here allowing the C. australis parasite to time reproduction exactly with that of their hosts, likely optimizing parasite fitness.

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