Host root exudates initiate a foraging preference by the root parasite Santalum album.

Abstract

Haustoria of root-parasitic plants draw nutrients from the roots of host species. While recent studies have assessed host preferences of parasitic plants, how root-exuded chemicals can mediate host tropism and selection by root-parasitic plants is poorly understood. Under greenhouse conditions, we performed two pot experiments to determine whether the root parasite Santalum album selectively forages for superior hosts (N2-fixing Acacia confusa Merr. or Dalbergia odorifera T. Chen) rather than for inferior hosts (non-N2-fixing Bischofia polycarpa (levl.) Airy Shaw or Dracontomelon duperreranum Pierre), and whether S. album uses host root exudates and/or specific chemicals in these root exudates to locate and trigger haustorium formation. Lateral roots and haustoria of S. album seedlings exhibited greater growth in the direction of D. odorifera roots than toward roots from the other three hosts. Comparative metabolic analysis revealed that D. odorifera root exudates were enriched in isoflavonoid, flavonoid and flavone/flavonol biosynthesis pathways, and that the relative contents of flavonoids were significantly greater in the root exudates of D. odorifera than in those of the other three hosts. Root exudates from D. odorifera significantly promoted S. album root growth, haustorium formation and reactive oxygen species accumulation in haustoria. Our results demonstrate that the key step in plant parasitism by S. album is based on root exudation by a host plant; the exudates function as a metabolite signal that activate lateral root growth and haustorium formation. Our results also indicate that flavonoids in the root exudates could play an important role in S. album foraging activity. Information on the responses of root parasites to host root exudates and/or haustorium-inducing chemicals may be useful for selecting superior host species to plant with valuable species of root parasites.