Host PGRP gene expression and bacterial release in endosymbiosis of the weevil Sitophilus zeamais.
Intracellular symbiosis (endosymbiosis) with gram-negative bacteria is common in insects, yet little is known about how the host immune system perceives the endosymbionts and controls their growth and invasion without complete bacterial clearance. In this study, we have explored the expression of a peptidoglycan recognition protein gene of the weevil Sitophilus zeamais (wPGRP); an ortholog in Drosophila (i.e., PGRP-LB) was recently shown to downregulate the Imd pathway (A. Zaidman-Remy, M. Herve, M. Poidevin, S. Pili-Floury, M. S. Kim, D. Blanot, B. H. Oh, R. Ueda, D. Mengin-Lecreulx, and B. Lemaitre, Immunity 24:463-473, 2006). Insect challenges with bacteria have demonstrated that wPGRP is induced by gram-negative bacteria and that the level of induction depends on bacterial growth. Real-time reverse transcription-PCR quantification of the wPGRP gene transcript performed at different points in insect development has shown a high steady-state level in the bacteria-bearing organ (the bacteriome) of larvae and a high level of wPGRP up-regulation in the symbiotic nymphal phase. Concomitantly, during this stage fluorescence in situ hybridization has revealed an endosymbiont release from the host bacteriocytes. Together with the previously described high induction level of endosymbiont virulence genes at the nymphal phase (C. Dale, G. R. Plague, B. Wang, H. Ochman, and N. A. Moran, Proc. Natl. Acad. Sci. USA 99:12397-12402, 2002), these findings indicate that insect mutualistic relationships evolve through an interplay between bacterial virulence and host immune defense and that the host immunity engages the PGRP gene family in that interplay.
Anselme
Caroline
C
Laboratoire de Biologie Fonctionnelle Insectes et Interactions (BF2I), UMR INRA/INSA de Lyon, Bât. Louis Pasteur, 20 Avenue Albert Einstein, 69621 Villeurbanne Cedex, France.
Vallier
Agnès
A
Balmand
Séverine
S
Fauvarque
Marie-Odile
MO
Heddi
Abdelaziz
A
D000818:Animals; D001419:Bacteria / Q000378:metabolism*; D018407:Bacterial Physiological Phenomena; D002352:Carrier Proteins / Q000235:genetics / Q000378:metabolism*; D015870:Gene Expression; D017404:In Situ Hybridization, Fluorescence; D020133:Reverse Transcriptase Polymerase Chain Reaction; D013559:Symbiosis; D048889:Weevils / Q000382:microbiology* / Q000502:physiology
D002352:Carrier Proteins; C118897:peptidoglycan recognition protein