Highlights d The Striga genome reflects a three-phase model of parasitic plant genome evolution d A family of strigolactone receptors has undergone a striking expansion in Striga d Genes in lateral root development are coordinately induced in a parasitic organ d Host genes and retrotransposons are horizontally transferred into Striga
Parasitic plants in the Orobanchaceae cause serious agricultural problems worldwide. Parasitic plants develop a multicellular infectious organ called a haustorium after recognition of host-released signals. To understand the molecular events associated with host signal perception and haustorium development, we identified differentially regulated genes expressed during early haustorium development in the facultative parasite Phtheirospermum japonicum using a de novo assembled transcriptome and a customized microarray. Among the genes that were upregulated during early haustorium development, we identified YUC3, which encodes a functional YUCCA (YUC) flavin monooxygenase involved in auxin biosynthesis. YUC3 was specifically expressed in the epidermal cells around the host contact site at an early time point in haustorium formation. The spatio-temporal expression patterns of YUC3 coincided with those of the auxin response marker DR5, suggesting generation of auxin response maxima at the haustorium apex. Roots transformed with YUC3 knockdown constructs formed haustoria less frequently than nontransgenic roots. Moreover, ectopic expression of YUC3 at the root epidermal cells induced the formation of haustorium-like structures in transgenic P. japonicum roots. Our results suggest that expression of the auxin biosynthesis gene YUC3 at the epidermal cells near the contact site plays a pivotal role in haustorium formation in the root parasitic plant P. japonicum.
Parasitic plants share a common anatomical feature, the haustorium. Haustoria enable both infection and nutrient transfer, which often leads to growth penalties for host plants and yield reduction in crop species. Haustoria also reciprocally transfer substances, such as RNA and proteins, from parasite to host, but the biological relevance for such movement remains unknown. Here, we studied such interspecies transport by using the hemiparasitic plant Phtheirospermum japonicum during infection of Arabidopsis thaliana. Tracer experiments revealed a rapid and efficient transfer of carboxyfluorescein diacetate (CFDA) from host to parasite upon formation of vascular connections. In addition, Phtheirospermum induced hypertrophy in host roots at the site of infection, a form of enhanced secondary growth that is commonly observed during various parasitic plant-host interactions. The plant hormone cytokinin is important for secondary growth, and we observed increases in cytokinin and its response during infection in both host and parasite. Phtheirospermum-induced host hypertrophy required cytokinin signaling genes (AHK3,4) but not cytokinin biosynthesis genes (IPT1,3,5,7) in the host. Furthermore, expression of a cytokinin-degrading enzyme in Phtheirospermum prevented host hypertrophy. Wild-type hosts with hypertrophy were smaller than ahk3,4 mutant hosts resistant to hypertrophy, suggesting hypertrophy improves the efficiency of parasitism. Taken together, these results demonstrate that the interspecies movement of a parasite-derived hormone modified both host root morphology and fitness. Several microbial and animal plant pathogens use cytokinins during infections, highlighting the central role of this growth hormone during the establishment of plant diseases and revealing a common strategy for parasite infections of plants.cytokinin | transport | hypertrophy | parasitism | Arabidopsis P arasitic plants are widespread agricultural pests and account for ∼1% of known flowering plants species (1). Parasitism ranges from holoparasites, which depend entirely on nutrient supply from host plants, to hemiparasites, which obtain nutrients via their own photosynthesis and from their hosts (1). Many hemiparasites do not depend on parasitism but often parasitize when conditions are suitable. These hemiparasitic plants include parasitic plants such as the commonly studied Orobanchaceae species Rhinanthus minor, Triphysaria versicolor, and Phtheirospermum japonicum. Both hemiparasites and holoparasites form specialized organs called haustoria that undergo a developmental transition from proto-haustoria to mature haustoria during the penetration and infection of host tissues to acquire nutrients and water (2). Some parasitic plants such as Striga or Rhinanthus form vascular connections exclusively to host xylem via xylem bridges (xylem-feeding), whereas haustoria of other plants such as Cuscuta or Orobanche also form symplastic phloem-to-phloem connections to host plants (phloem-feeding) (1). In addition to water and nutrients, other ...
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