Sister species, shared and divergent responses: early transcriptomic profiling of Bursaphelenchus xylophilus exposed to Esteya spp.

Abstract

Bursaphelenchus xylophilus (pinewood nematode, PWN) responds transcriptionally to nematophagous fungi, but the earliest events preceding cuticle penetration are poorly characterized, and whether closely related fungal antagonists elicit comparable responses is unknown. Here, we compared PWN transcriptomic responses to Esteya floridanum V14639 (EF) and E. vermicola CCF3117 (EV) at 1 h post-inoculation (hpi), capturing the onset of host-fungus interaction. Despite their phylogenetic proximity, under our exposure conditions the two fungi elicited partly divergent host responses at 1 hpi. EF induced a broad transcriptional response enriched in peptidase activity and lysosomal pathways, accompanied by downregulation of cuticle structural components. In contrast, EV triggered a narrower response, without the proteolytic and lysosomal enrichment observed with EF. Direct comparison of the two treatments revealed no significantly enriched Gene Ontology categories, although pathway analysis identified DNA replication and repair pathways, comprising genes more highly expressed under EF. Enrichment analyses revealed a shared transcriptional signature in both interactions characterized by downregulation of xenobiotic- and central carbon-metabolism pathways, suggesting an early reduction in xenobiotic detoxification capacity rather than induction of detoxification programs. These findings suggest that phylogenetic proximity does not necessarily predict conserved early transcriptional responses, although comparisons of single isolates cannot separate species-level from isolate-level effects.