Coregulation of host-response genes in integument: switchover of gene expression correlation pattern and impaired immune responses induced by dipteran parasite infection in the silkworm, Bombyx mori.

The activation of host response proteins against parasitic infection is dependent on the coregulation of immune gene expression. The infection of commercially important silkworm Bombyx mori through endoparasite Exorista bombycis enhanced host-response gene expression in integument early in the infection and was lowered asymptotically. Principal component analysis (PCA) showed heterogeneity while explaining ∼80 % variance among expression timings. PCA showed positive and negative correlation with gene expression and differentiated transcriptional timings, and revealed cross talk within the immune system. Pearson correlation analysis showed significant linear correlation (mean R (2) = >0.7; P < 0.004) between the expression of 16 pairs of genes in control, while the relation switched over to curvilinear due to parasitism. The genes showed pleiotropic interaction among them, with four genes each for prophenoloxidase activating enzyme (PPAE) and caspase. Besides, after parasitism, exclusive correlation of five gene pairs including PPAE-Spatzle pair (R (2) = 0.9; P < 0.011) was observed in the integument. In integument, the phenol oxidase (PO) activity showed a positive correlation with the tyrosine level (R (2) = 0.410; P < 0.002) and a curvilinear relation (R (2) = 0.745; P < 0.0002) with the expanding lysis area. The PO activity was positively correlated with BmToll expression and negatively correlated with paralytical peptide expression, revealing polygenic influence. Caspase expression was tightly regulated by signal genes in control integument, whereas they were deregulated after infection. Switchover from linear to curvilinear correlation and the appearance of new gene correlations in parasitized integument revealed deviation from gene coregulation, leading to impaired immune responses, characterized by lowered gene expression and varied phenotypic consequences.