Koski, T.-M. | bioRxiv Science

bioRxiv2022

The entry of pinewood nematode is linked to programmed tracheal development of vector beetles

The transmission of some pathogens by insect vectors often requires fine-tuned biological synchronization and communication between the two parties. However, the role of tissue development in mediating this pathogen-vector coordination remains elusive. Here we investigated the association between tracheal development of Monochamus alternatus beetle and a notorious plant parasitic pine wood nematode Bursaphelenchus xylophilus, which enter and inhabit inside the tracheal system after adult beetle eclosion and then were transmitted to pine trees (Pinus spp.) by the beetle. We found that the tracheal systems of newly emerged adult beetles underwent morphological changes during the adult sclerotization, characterized by a remarkable increase of diameter of thoracic tracheal dorsal tubes. Consistently, comparative transcriptomics further revealed dramatic changes in gene expression occurring within five days after eclosion, demonstrating sequential regulation of tracheal genes. Genes controlling primary branching were up-regulated soon after eclosion, whereas those controlling terminal branching and branch fusion were up-regulaed at the later stage. Interestingly, during tracheal maturation, genes involved in biosynthesis of Juvenile Hormone (JH) and ecdysteroids were activated. Nematode loading assay further revealed that the entry of nematodes to beetle tracheae was initiated earliest after three days post eclosion, implying that nematode entry is reliant on the formation of the vectors primary tracheal branches and is perhaps stimulated by production of insect hormones or their precursors. In addition, specific regulation on secreted proteins, such as Defensin-1-like and membrane proteins, at later stages of tracheal maturation may further facilitate the entry of nematodes by improving their retention. Therefore, this study highlights vital role of programed tracheal development on nematode entry into its vector beetle, and suggests a potential roles of insect genes and metabolites in manipulation of interspecific biological developmental synchronization between parasites and their insect vectors.

ecology↗

bioRxiv2022

Hypoxia-induced tracheal elasticity in vector beetle facilitates the loading of pinewood nematode

Many pathogens rely on their insect vectors for transmission. Such pathogens are under selection to improve vector competence for their transmission by employing various tissue or cellular responses of vectors. However, whether pathogens can actively cause hypoxia in vectors and exploit hypoxia responses to promote their vector competence is still unknown. Fast dispersal of pinewood nematode (PWN), the causal agent for the destructive pine wilt disease and subsequent infection of pine trees is characterized by the high vector competence of pine sawyer beetles (Monochamus spp.), and a single beetle can harbor over 200,000 PWNs in its tracheal system. Here, we demonstrate that PWN loading activates hypoxia in tracheal system of the vector beetles. Both PWN loading and hypoxia enhanced tracheal elasticity and thickened the apical extracellular matrix (aECM) of the tracheal tubes while a notable upregulated expression of a resilin-like mucin protein Muc91C was observed at the aECM layer of PWN-loaded and hypoxic tracheal tubes. RNAi knockdown of Muc91C reduced tracheal elasticity and aECM thickness under hypoxia conditions and thus decreasing PWN loading. Our study suggests a crucial role of hypoxia-induced developmental responses in shaping vector tolerance to the pathogen and provides clues for potential molecular targets to control pathogen dissemination.

ecology↗