The medicinal plant Cistanche deserticola Ma (Orobanchaceae) is a holoparasitic angiosperm that takes life-essential materials from Haloxylon ammodendron (C. A. Mey.) Bunge (Amaranthaceae) roots. Although many experiments have been conducted to improve the quality of C. deserticola, little attention has been paid to the host’s influence on metabolite accumulation. In this study, transcriptomic and metabolomic analyses were performed to unveil the host’s role in C. deserticola’s metabolite accumulation, especially of phenylethanoid glycosides (PhGs). The results indicate that parasitism by C. deserticola causes significant changes in H. ammodendron roots in relation to metabolites and genes linked to phenylalanine metabolism, tryptophan metabolism and phenylpropanoid biosynthesis pathways, which provide precursors for PhGs. Correlation analysis of genes and metabolites further confirms that C. deserticola’s parasitism affects PhG biosynthesis in H. ammodendron roots. Then we found specific upregulation of glycosyltransferases in haustoria which connect the parasites and hosts. It was shown that C. deserticola absorbs PhG precursors from the host and that glycosylation takes place in the haustorium. We mainly discuss how the host resists C. deserticola parasitism and how this medicinal parasite exploits its unfavorable position and takes advantage of host-derived metabolites. Our study highlights that the status of the host plant affects not only the production but also the quality of Cistanches Herba, which provides a practical direction for medicinal plant cultivation.

Cistanche deserticola, a holoparasitic plant widely used in traditional Chinese medicine, relies on chemical signals from its host plant, Haloxylon ammodendron, to initiate seed germination and haustorium induction. This study employed UPLC-MS/MS to analyze the root metabolites of H. ammodendron. The results showed that 11 substances such as phenolic acids, flavonoids, and alkaloids were mainly contained in the roots of H. ammodendron, among which phenolic acids accounted for the largest proportion, accounting for 18.00% in winter samples and 16.11% in autumn samples. Based on the reported exogenous substances that promote haustorium induction in C. deserticola and the differential metabolites in H. ammodendron roots, we selected seven exogenous signaling substances: 2,6-dimethoxy-1,4-benzoquinone, resorcinol, ferulic acid, syringic acid, vanillic acid, vanillin, and pelargonidin. Through concentration-gradient experiments (0.1–100 μM), we assessed their effects on haustorium induction in C. deserticola seeds. The results showed that among the seven substances, syringic acid, vanillic acid, and vanillin had the best impact on promoting the haustorium induction of C. deserticola seeds. Vanillic acid had the best impact at the concentration of 10 μmol/L, and the highest haustorium induction rate was 50.2%. There was no significant difference in the concentrations of vanillin and syringic acid. The results showed that phenolic acids in the host root system stimulated haustoria induction in C. deserticola seeds, with different substances requiring different optimal concentrations. This study not only identifies specific phenolic acids that enhance C. deserticola productivity but also establishes a chemical ecology framework for investigating host–parasite interactions in other root parasitic species.