A composite, host‐participatory haustorium links host compatibility to defence bifurcation in Alectra vogelii (Orobanchaceae)

Societal Impact Statement Parasitic weeds of the family Orobanchaceae are among the most damaging constraints on food production in the tropics, draining water and nutrients from their hosts and threatening the livelihoods of millions of smallholder farmers. Yellow witchweed ( Alectra vogelii ) can destroy entire legume harvests across sub‐Saharan Africa, where these crops are a primary source of dietary protein and household income. By revealing how a compatible host enables this parasite to develop, our work pinpoints the developmental and metabolic steps that turn an attachment into a damaging infection—knowledge that can guide the breeding of resistant crops and the design of more sustainable, targeted control of parasitic weeds. Summary Yellow witchweed ( Alectra vogelii Benth., Orobanchaceae) is an obligate hemiparasitic weed and a major pest of grain legumes across sub‐Saharan Africa, where it causes severe crop losses and threatens smallholder food security, yet its developmental biology and mechanisms of host compatibility remain poorly understood. By combining phenotypic, anatomical and transcriptomic analyses, we show that host compatibility in Alectra is expressed primarily through post‐attachment developmental progression rather than attachment success alone. Matched‐stage comparisons reveal accelerated development on compatible hosts and profound reorganisation in the host–parasite interface region, characterised by host tissue proliferation, vascular integration and coordinated transcriptional programmes spanning both host and parasite, whereas incompatible interactions are dominated by defence and reinforcement responses that constrain parasite growth. Notably, compatible interactions are associated with early activation of photosynthesis‐related programmes, indicating a transition towards metabolic autonomy that is supported by enhanced nutrient acquisition and internal recycling. Predictive modelling further identifies pathway‐level transcriptional states associated with successful development and reinforces the view that compatibility reflects systems‐level integration rather than parasite gene expression alone. These findings position the Alectra haustorium as a dynamic, host‐participatory composite organ central to host compatibility and highlight post‐attachment integration, metabolic reprogramming and autophagy‐related processes as key determinants of developmental success.