Abstract
The bean bug Riptortus pedestris possesses a specialized symbiotic organ in a posterior region of the midgut, where numerous crypts harbor extracellular betaproteobacterial symbionts of the genus Burkholderia. Second instar nymphs orally acquire the symbiont from the environment, and the symbiont infection benefits the host by facilitating growth and by occasionally conferring insecticide resistance. Here we performed comparative transcriptomic analyses of insect genes expressed in symbiotic and non-symbiotic regions of the midgut dissected from Burkholderia-infected and uninfected R. pedestris. Expression sequence tag analysis of cDNA libraries and quantitative reverse transcription PCR identified a number of insect genes expressed in symbiosis- or aposymbiosis-associated patterns. For example, genes up-regulated in symbiotic relative to aposymbiotic individuals, including many cysteine-rich secreted protein genes and many cathepsin protease genes, are likely to play a role in regulating the symbiosis. Conversely, genes up-regulated in aposymbiotic relative to symbiotic individuals, including a chicken-type lysozyme gene and a defensin-like protein gene, are possibly involved in regulation of non-symbiotic bacterial infections. Our study presents the first transcriptomic data on gut symbiotic organ of a stinkbug, which provides initial clues to understanding of molecular mechanisms underlying the insect-bacterium gut symbiosis and sheds light on several intriguing commonalities between endocellular and extracellular symbiotic associations.
Highlights
The majority of insects are associated with microbial symbionts within their alimentary tract, body cavity and/or cells, and they are often benefited from the symbiosis for their growth, viability and fecundity
M4 and M4 bulb (M4B) were enlarged in symbiotic insects (Fig. 1A–C), whereas the midgut regions were atrophied in aposymbiotic insects (Fig. 1D–F)
In the cDNA libraries of R. pedestris, we identified several cysteine-rich secreted protein genes whose expression patterns were strongly associated with the midgut region M4 of symbiotic insects (Fig. 3; Table 2)
Summary
The majority of insects are associated with microbial symbionts within their alimentary tract, body cavity and/or cells, and they are often benefited from the symbiosis for their growth, viability and fecundity. Transcriptomic analyses of the bacteriomes, which are specialized insect organs consisting of bacteriocytes for harboring microbial symbionts, have been conducted for aphid-Buchnera, weevil-Sodalis and bedbug-Wolbachia endosymbiotic associations of obligate nature [7,8,9,10,11,12]. Comparative transcriptomics of symbiontinfected and uninfected individuals have been applied to diverse arthropods and their facultative endosymbionts like Wolbachia, Cardinium and Serratia [13,14,15,16,17,18] These studies show that the expression of immune-related genes such as lysozyme genes and antimicrobial peptide genes is often affected by endosymbiont infection in a tissue-specific manner. A number of cysteine-rich secreted proteins are highly expressed in the aphid bacteriocytes [7], which has been known in plant symbioses such as legume-Rhizobium associations [19]
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