Peptidoglycan recognition proteins (PGRPs) play a critical role in insect innate immunity in defending against pathogen invasion and regulating the homeostasis of endosymbionts. Arsenophonus, an emerging clade of intracellular symbionts, has been extensively studied for its roles in host reproductive manipulation and environmental adaptation. However, the molecular mechanisms by which host insects maintain Arsenophonus homeostasis through PGRPs remain largely unexplored. Here, we investigated the functional roles of PGRPs in regulating Arsenophonus homeostasis in the brown planthopper, Nilaparvata lugens, a devastating pest of rice crops. While a previous study reported the existence of only two PGRPs (PGRP-LC and PGRP-LB) in N. lugens, we further determined that PGRP-LC produced two functional isoforms, PGRP-LCa and PGRP-LCb, respectively. PGRP-LCa and PGRP-LCb shared identical intracellular domains but possessed different extracellular domains. Simultaneously, Arsenophonus was observed to localize to the gut muscle layer, fat bodies and ovarian tissues by Transmission electron microscopy (TEM). Functional assays revealed that PGRP-LCa and PGRP-LCb bound not only peptidoglycan but also directly interacted with cultured Arsenophonus. Artificially transfected Arsenophonus upregulated the expression of PGRP-LCa, PGRP-LCb and Relish, while suppressing PGRP-LB. PGRP-LCa or Relish knockdown increased Arsenophonus density, whereas silencing PGRP-LCb reduced the symbiont load and female fecundity by the non-IMD pathway. Notably, inhibiting PGRP-LB not only elevated Arsenophonus density but also triggered symbiont dispersal from the gut muscle layer into epithelium. Our findings indicate that PGRPs cooperatively maintain Arsenophonus homeostasis to ensure the fecundity in N. lugens. These studies provide insight into the interaction of immunity between host and endosymbiont.
Qin et al. (Tue,) studied this question.