The effect of parasitic plants on host plant immunity against microbial pathogens

Plants in natural environments are frequently exposed to multiple biotic and abiotic stresses, and their combined effects often trigger complex and non-additive physiological and molecular responses (Suzuki et al., 2014). Among these, parasitic plants impose a major biotic stress, establishing haustoria connections with host roots to extract water, nutrients, and signalling molecules (Albert et al., 2021; Yoshida et al., 2016). Parasitism may profoundly influence the host’s immune competence and interactions with other microbial pathogens. However, the impact of parasitic plants on host immune regulation against microbial infections remains largely unexplored. This study examined the impact of parasitism by the facultative hemiparasite Phtheirospermum japonicum on the immune responses of Arabidopsis thaliana to microbial pathogens. Parasitization assays revealed that A. thaliana plants parasitized by P. japonicum exhibited a significant reduction in growth and biomass, suggesting a substantial physiological burden for the host. To examine whether this effect extends to immune regulation, early pattern-triggered immunity (PTI) responses were analyzed using flg22 and chitin treatments. Measurements of reactive oxygen species (ROS) production, Mitogen-Activated Protein Kinase (MAPK) phosphorylation, and defence gene expression revealed that parasitized plants exhibited significantly reduced PTI activation compared to unparasitized controls. To determine whether this compromised immunity translated into altered disease susceptibility, infection assays were conducted using the hemibiotrophic bacterium Pseudomonas syringae pv. tomato DC3000 and the necrotrophic fungus Botrytis cinerea strain B05.10. Parasitized A. thaliana plants exhibited hypersusceptibility to both pathogens, characterized by higher bacterial titers and larger necrotic lesions compared to unparasitized plants, confirming a broad suppression of immune competence. To elucidate the molecular mechanisms underlying this immune attenuation, transcriptomic profiling (RNA-seq) was performed on parasitized and unparasitized A. thaliana plants treated with flg22 or infected with Pst DC3000. The results revealed that P. japonicum parasitism markedly suppressed flg22- and Pst-triggered transcriptional responses. In parasitized plants, PTI-associated genes and growth-related pathways were downregulated, while nutrient starvation pathways were induced. Moreover, infection with Pst DC3000 triggered strong phosphate starvation responses and repressed key defence pathways involving salicylic acid (SA), jasmonic acid (JA), and glucosinolate biosynthesis. Phosphate starvation is well documented to suppress plant immunity, a phenomenon that appears to be evolutionarily conserved across multiple plant species, where nutrient deprivation often compromises defence signalling and increases susceptibility to pathogens. Finally, to identify which phytohormone signalling networks are altered during parasitism, phytohormone reporter lines of A. thaliana were used to monitor SA, JA, JA/ethylene (JA/ET), and abscisic acid (ABA) activity in roots. Parasitism induced strong ABA signalling, whereas SA and JA/ET pathways remained largely unresponsive. Interestingly, JA reporters revealed a complex pattern, with induction of VSP2 and JAZ9 but no activation of AOS in the host roots. As previous transcriptomic studies have shown AOS induction in P. japonicum haustoria during parasitism (Kokla et al., 2022), this suggests that the observed JA response may originate in the parasite rather than the host, although this remains to be confirmed. Collectively, this study provides novel insights into how P. japonicum modulates host immunity and nutrient signalling. The findings highlight that parasitism induces nutrient starvation responses, particularly phosphate limitation, which are closely linked to suppression of immune signalling. This work underscores the intricate trade-offs between growth, defence, and nutrient acquisition in plants subjected to combined stresses, including parasitism and pathogen attack.