Haustorial Hairs Are Specialized Root Hairs That Support Parasitism in the Facultative Parasitic Plant Phtheirospermum japonicum

Abstract

A haustorium is the unique organ that invades host tissues and establishes vascular connections. Haustorium formation is a key event in parasitism, but its underlying molecular basis is largely unknown. Here, we use Phtheirospermum japonicum, a facultative root parasite in the Orobanchaceae, as a model parasitic plant. We performed a forward genetic screen to identify mutants with altered haustorial morphologies. The development of the haustorium in P. japonicum is induced by host-derived compounds such as 2,6-dimethoxy-p-benzoquinone. After receiving the signal, the parasite root starts to swell to develop a haustorium, and haustorial hairs proliferate to densely cover the haustorium surface. We isolated mutants that show defects in haustorial hair formation and named them haustorial hair defective (hhd) mutants. The hhd mutants are also defective in root hair formation, indicating that haustorial hair formation is controlled by the root hair development program. The internal structures of the haustoria in the hhd mutants are similar to those of the wild type, indicating that the haustorial hairs are not essential for host invasion. However, all the hhd mutants form fewer haustoria than the wild type upon infection of the host roots. The number of haustoria is restored when the host and parasite roots are forced to grow closely together, suggesting that the haustorial hairs play a role in stabilizing the host-parasite association. Thus, our study provides genetic evidence for the regulation and function of haustorial hairs in the parasitic plant.

Interspecies hormonal control of host root morphology by parasitic plants

“…Safranin-O staining of haustoria confirmed the formation of xylem bridges from Phtheirospermum to Arabidopsis during transition from protohaustoria to mature haustoria, typically 3-4 dpi, consistent with normal haustorial development ( Fig. 1 C and E) (18).…”

“…We sought to identify conditions that promote Arabidopsis infection because growth of Phtheirospermum does not absolutely depend on parasitism. As previously described, haustorium development occurs when Phtheirospermum comes in contact with its host on water-agar with no additional nutrients (18,19). We used a similar water-only setup, but substituted Whatman filter paper and nylon membrane for agar to anchor the plants, similar to an experimental setup used for Arabidopsis grafting (20).…”

“…Phtheirospermum infects a variety of plant species including rice, maize, and Arabidopsis (18,19). We sought to identify conditions that promote Arabidopsis infection because growth of Phtheirospermum does not absolutely depend on parasitism.…”

Local Auxin Biosynthesis Mediated by a YUCCA Flavin Monooxygenase Regulates Haustorium Development in the Parasitic Plant Phtheirospermum japonicum

“…Among these HIFs, 2,6-dimethoxy-p-benzoquinone (DMBQ) was originally identified from host root extracts and was shown to activate haustorium formation in parasite roots (Chang and Lynn, 1986;Smith et al, 1990). Although haustoria can be observed in different parts of the root, the area between the distal elongation zone and the meristematic root tip is the most sensitive to HIFs (Cui et al, 2016;Baird and Riopel, 1984). Typically, this area becomes swollen and forms a haustorium ;24 h after DMBQ treatment (Albrecht et al, 1999;Ishida et al, 2011).…”

“…The morphological changes that occur during haustorium development have been described histologically in several parasitic plant species (Baird and Riopel, 1984;Ishida et al, 2011;Riopel and Musselman, 1979;Jamison and Yoder, 2001;Cui et al, 2016). In the facultative parasite Agalinis purpurea, cortex cells slightly expand radially 6 h after exposure to HIF.…”