Interspecies hormonal control of host root morphology by parasitic plants
Sunday, 2017/05/21 | 06:53:05
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Thomas Spallek, Charles W. Melnyk, Takanori Wakatake, Jing Zhang, Yuki Sakamoto, Takatoshi Kiba, Satoko Yoshida, Sachihiro Matsunaga, Hitoshi Sakakibara, and Ken Shirasu SignificanceParasitic plants are pests of many plants, including major crop species. An important step toward creating resistance to parasitic plants is gaining a better understanding of how these pathogens control the physiology and development of their hosts. We combined genetic, cell-biological, and biochemical methods to identify the plant hormone cytokinin as a mobile signal between the hemiparasitic plant Phtheirospermum japonicum and the host Arabidopsis thaliana. Transport of parasite-derived cytokinins induced morphological changes in host roots, revealing insights into how parasitic plants manipulate host development and laying the foundation for future explorations for bioactive molecule transfer from parasitic plants to hosts. AbstractParasitic 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.
See: http://www.pnas.org/content/114/20/5283.abstract.html?etoc PNAS May 16 2017; vol.114; no.20: 5283–5288
Fig. 1. Phtheirospermum parasitizes Arabidopsis. (A) Phtheirospermum growing alone (Pj-) or infecting (Pj+) Arabidopsis (At+) show increased Phtheirospermum size and decreased Arabidopsis size compared with uninfected controls (At-) at 30 dpi. (B) Detail image of Phtheirospermum-infecting Arabidopsis with Phtheirospermum haustorium (haust.) attachment site (HA). (C) Images of Safranin-O stained proto- and mature haustoria show differences in xylem bridge (XB) formation. (D) CFDA transport ability of 11 dpi haustoria were assayed 90 min after application of CFDA onto host leaves (asterisk). (E) Ratios of mature haustoria (brown bar) and haustoria with CFDA transport ability (green bar) (n = 35–86) were quantified for the indicated time points (Fisher Exact Test, P < 0.001). (F) A fluorescent image of a single optical plane of the haustorium 90 min after CFDA application onto a host leaf. CFDA fluorescence is green, and cell walls were stained with propidium iodide in magenta. (G) Schematic representation of F with indicated optical section of the haustorium (H), the host root above (I) or below (J) the HA. (Scale bars: A, B, and D, 1 mm; C, F, and G, 50 µm; H and I, 25 µm.) |
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