An entomopathogenic bacterium Photorhabdus temperata subsp. temperata (Ptt) infects insect hemocoel by the vectoring activity of its symbiotic nematode, Heterorhabditis megidis. The bacterium induces host immunosuppression by inhibiting eicosanoid biosynthesis. This study investigated the role of eicosanoids in immune responses of the beet armyworm, Spodoptera exigua, in the early bacterial infection stage (first 3 hr postinfection [PI]). After infection with the nonpathogenic Escherichia coli (Ec), the bacterium maintained its population for the first 3 hr PI, then rapidly decreased in numbers. During the 3 hr PI of Ptt, this pathogenic bacterium also did not show any significant change in bacterial population. However, Ptt rapidly increased its population size after the initial lag phase, inducing fatal septicemia. This study further analyzed cellular and humoral immune responses of the beet armyworm during the initial 3 hr PI. During this early stage, challenge with Ec stimulated hemocyte-spreading behavior along with extensive F-actin growth. However, Ptt infection suppressed hemocyte spreading. Expression levels of three antimicrobial peptides (lysozyme, gloverin, and gallerimycin) were significantly inhibited during Ptt infection. Phospholipase A activity was significantly induced during the early infection stage of Ec, but not during Ptt infection. Addition of eicosanoid biosynthesis inhibitors significantly reversed the initial immunosuppression. These results suggest that, during the early infection stage, Ptt can shutdown eicosanoid biosynthesis which can prevent acute immune responses of host insects.
Eicosanoids mediate various insect physiological processes, including reproduction. Especially, the eicosanoid prostaglandin E 2 (PGE 2 ) is known to mediate oocyte development in some insects. The explosive reproductive potential of the Western flower thrips, Frankliniella occidentalis, damages various agricultural crops. However, little is known about the underlying physiological processes of egg development in this pest. This study found that treatment with aspirin (ASP) (a specific cyclooxygenase (COX) inhibitor) used to inhibit PGE 2 biosynthesis during ovarian development significantly suppressed the reproduction of female F. occidentalis. However, the addition of PGE 2 to ASPtreated females significantly rescued the suppressed reproduction. PGE 2 was detected in growing ovarian follicles in an immunofluorescence assay. The hypothetical biosynthetic machinery of PGE 2 was predicted from the F. occidentalis genome and included phospholipase A 2 (PLA 2 ), COX-like peroxidase (POX), and PGE 2 synthase (PGES). Three specific PLA 2 s were highly expressed in female adults during active oogenesis. Specific POX and PGES genes also showed high expression during active oogenesis. The adverse effect of ASP treatment on oogenesis was observed in follicle formation in the germarium where the follicle numbers in an ovariole were decreased, which resulted in hypotrophied ovaries. This impairment was rescued by the addition of PGE 2 . ASP treatment also significantly inhibited chorion formation and
Several endocrine signals mediate mosquito egg development, including 20-hydroxyecdysone (20E). This study reports on prostaglandin E2 (PGE2) as an additional, but core, mediator of oogenesis in a human disease-vectoring mosquito, Aedes albopictus. Injection of aspirin (an inhibitor of cyclooxygenase (COX)) after blood-feeding (BF) inhibited oogenesis by preventing nurse cell dumping into a growing oocyte. The inhibitory effect was rescued by PGE2 addition. PGE2 was found to be rich in nurse cells and follicular epithelium after BF. RNA interference (RNAi) treatments of PG biosynthetic genes, including PLA2 and two COX-like peroxidases, prevented egg development. Interestingly, 20E treatment significantly increased the expressions of PG biosynthetic genes, while the RNAi of Shade (which is a 20E biosynthetic gene) expression prevented inducible expressions after BF. Furthermore, RNAi treatments of PGE2 receptor genes suppressed egg production, even under PGE2. These results suggest that a signaling pathway of BF-20E-PGE2 is required for early vitellogenesis in the mosquito.
The western flower thrips, Frankliniella occidentalis, is one of the most devastating insect pests with explosive reproductive potential. However, its reproductive physiological processes are not well understood. This study reports the ovarian development and associated transcriptomes of F. occidentalis. Each ovary consisted of four ovarioles, each of which contained a maximum of nine follicles in the vitellarium. The germarium consisted of several dividing cells forming a germ cell cluster, presumably consisting of oocytes and nurse cells. The nurse cells were restricted to the germarium while the subsequent follicles did not possess nurse cells or a nutritive cord, supporting the neo-panoistic ovariole usually found in thysanopteran insects. Oocyte development was completed 72 h after adult emergence (AAE). Transcriptome analysis was performed at mid (36 h AAE) and late (60 h AAE) ovarian developmental stages using RNA sequencing (RNASeq) technology. More than 120 million reads per replication were matched to ≈ 15,000 F. occidentalis genes. Almost 500 genes were differentially expressed at each of the mid and late ovarian developmental stages. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed that these differentially expressed genes (DEGs) were associated with metabolic pathways along with protein and nucleic acid biosynthesis. In both ovarian developmental stages, vitellogenin, mucin, and chorion genes were highly (> 8-fold) expressed. Endocrine signals associated with ovarian development were further investigated from the DEGs. Insulin and juvenile hormone signals were upregulated only at 36 h AAE, whereas the ecdysteroid signal was highly maintained at 60 h AAE. This study reports the transcriptome associated with the ovarian development of F. occidentalis, which possesses a neo-panoistic ovariole.
Western flower thrips, Frankliella occidentalis, is a serious pest by directly infesting host crops. It can also give indirect damage to host crops by transmitting a plant virus called tomato spotted wilt virus. A fungal pathogen, Beauveria bassiana, can infect thrips. It has been used as a biopesticide. However, little is known on the defense of thrips against this fungal pathogen. This study assessed the defense of thrips against the fungal infection with respect to immunity by analyzing immune-associated genes of F. occidentalis in both larvae and adults. Immunity-associated genes of western flower thrips were selected from three immunity steps: nonself recognition, mediation, and immune responses. For the pathogen recognition step, dorsal switch protein 1 (DSP1) was chosen. For the immune mediation step, phospholipase A2 (PLA2) and prostaglandin E2 synthase were also selected. For the step of immune responses, two phenoloxidases (PO) genes and four proPO-activating peptidase genes involved in melanization against pathogens were chosen. Dual oxidase gene involved in the production of reactive oxygen species and four antimicrobial peptide genes for executing humoral immune responses were selected. All immunity-associated genes were inducible to the fungal infection. Their expression levels were induced higher in adults than in larvae by the fungal infections. However, inhibitor treatments specific to DSP1 or PLA2 significantly suppressed the inducible expression of these immune-associated genes, leading to significant enhancement of fungal pathogenicity. These results suggest that immunity is essential for thrips to defend against B. bassiana, in which DSP1 and eicosanoids play a crucial role in eliciting immune responses.
Chorion—i.e., the eggshell—is formed during the late stage of oogenesis by follicular epithelium in the ovary. Although the endocrine signal(s) driving choriogenesis remain unclear in mosquitoes, this process in other insects has been suspected to involve the mediation of prostaglandins (PGs). This study tested the role of PG in the choriogenesis of the Asian tiger mosquito, Aedes albopictus, and its influence on controlling the expressions of genes associated with chorion formation by a transcriptome analysis. An immunofluorescence assay showed that PGE2 is localised in follicular epithelium. With the treatment of aspirin, an inhibitor of PG biosynthesis, at mid oogenesis, the PGE2 signal disappeared in the follicular epithelium led to significantly inhibited chorion formation along with a malformed eggshell. Ovary transcriptomes were assessed by RNASeq at the mid and late ovarian developmental stages. Differentially expressed genes (DEGs) exhibiting more than twofold changes in expression levels included 297 genes at mid stage and 500 genes at late stage. These DEGs at these two developmental stages commonly included genes associated with egg and chorion proteins of Ae. albopictus. Most chorion‐associated genes were clustered in the 168 Mb region on a chromosome and exhibited significantly induced expressions at both ovarian developmental stages. The inhibition of PG biosynthesis significantly suppressed the expression of the chorion‐associated genes while the addition of PGE2 rescued the gene expressions and led to recovery of choriogenesis. These results suggest that PGE2 mediates the choriogenesis of Ae. albopictus.
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