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The molecular biology of the olive fly comes of age.

Sagri E, Reczko M, Tsoumani KT, Gregoriou ME, Harokopos V, Mavridou AM, Tastsoglou S, Athanasiadis K, Ragoussis J, Mathiopoulos KD - BMC Genet. (2014)

Bottom Line: Many years of experience from successful SIT applications in related species, primarily the Mediterranean fruit fly, Ceratitis capitata, demonstrated that efficient SIT protocols require the availability of fundamental genetic and molecular information.Furthermore, at least five olfactory-related genes were shown to be differentially expressed in the female and male reproductive systems analyzed.Finally, the expression profile of the embryonic serendipity-α locus and the pre-apoptotic head involution defective gene were analyzed during embryonic developmental stages.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: Olive cultivation blends with the history of the Mediterranean countries since ancient times. Even today, activities around the olive tree constitute major engagements of several people in the countryside of both sides of the Mediterranean basin. The olive fly is, beyond doubt, the most destructive pest of cultivated olives. The female fly leaves its eggs in the olive fruit. Upon emergence, the larvae feed on the olive sap, thus destroying the fruit. If untreated, practically all olives get infected. The use of chemical insecticides constitutes the principal olive fly control approach. The Sterile Insect Technique (SIT), an environmentally friendly alternative control method, had been tried in pilot field applications in the 1970's, albeit with no practical success. This was mainly attributed to the low, non-antagonistic quality of the mixed-sex released insects. Many years of experience from successful SIT applications in related species, primarily the Mediterranean fruit fly, Ceratitis capitata, demonstrated that efficient SIT protocols require the availability of fundamental genetic and molecular information.

Results: Among the primary systems whose understanding can contribute towards novel SIT approaches (or its recently developed alternative RIDL: Release of Insects carrying a Dominant Lethal) is the reproductive, since the ability to manipulate the reproductive system would directly affect the insect's fertility. In addition, the analysis of early embryonic promoters and apoptotic genes would provide tools that confer dominant early-embryonic lethality during mass-rearing. Here we report the identification of several genes involved in these systems through whole transcriptome analysis of female accessory glands (FAGs) and spermathecae, as well as male testes. Indeed, analysis of differentially expressed genes in these tissues revealed higher metabolic activity in testes than in FAGs/spermathecae. Furthermore, at least five olfactory-related genes were shown to be differentially expressed in the female and male reproductive systems analyzed. Finally, the expression profile of the embryonic serendipity-α locus and the pre-apoptotic head involution defective gene were analyzed during embryonic developmental stages.

Conclusions: Several years of molecular studies on the olive fly can now be combined with new information from whole transcriptome analyses and lead to a deep understanding of the biology of this notorious insect pest. This is a prerequisite for the development of novel embryonic lethality female sexing strains for successful SIT efforts which, combined with improved mass-reared conditions, give new hope for efficient SIT applications for the olive fly.

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Functional annotation of differentially expressed sex-differentiation genes. In the left part of the figure, the gene expression levels of the differentially expressed sex-differentiation genes (Log2, fold change) are shown, as resulted from the RNA-seq analysis. The up-regulated genes in males are depicted in blue bars and the up-regulated genes in females in red bars. At the right part of the figure, the Gene Ontology (GO) classification of the same genes for the ontologies: Biological Process (BP), Molecular Function (MF), and Interpro (IP) protein domains is listed.
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Figure 4: Functional annotation of differentially expressed sex-differentiation genes. In the left part of the figure, the gene expression levels of the differentially expressed sex-differentiation genes (Log2, fold change) are shown, as resulted from the RNA-seq analysis. The up-regulated genes in males are depicted in blue bars and the up-regulated genes in females in red bars. At the right part of the figure, the Gene Ontology (GO) classification of the same genes for the ontologies: Biological Process (BP), Molecular Function (MF), and Interpro (IP) protein domains is listed.

Mentions: In order to validate the differential expression of various genes observed after the RNAseq analysis of reproductive tissues of female and male olive flies, further functional analysis was performed for twelve genes that were differentially expressed in female accessory glands and spermathecae, on one hand, and male testes, on the other (Figure 4). These genes were selected on the basis of known involvement in sexual differentiation in other insects. Seven of them were selected from the 1238 significantly up-regulated in MALE (Table S4): kl2 (male fertility factor kl2), kl3 (male fertility factor kl3), kl5 (male fertility factor kl5), ory (occludin-related Y protein), fem-1 (sex-determining protein fem-1), gas8 (growth arrest specific protein 8) and lobo (lost boys). Three more genes that were up-regulated in MALE [ix (intersex), pbl (pebble) and hcf (host cell factor C1)] and two that were up-regulated in FEMALE [sox and pcp (pupal cuticle protein 78E)], albeit with lower statistical power (i.e., q>0.05) were also selected for further validation.


The molecular biology of the olive fly comes of age.

Sagri E, Reczko M, Tsoumani KT, Gregoriou ME, Harokopos V, Mavridou AM, Tastsoglou S, Athanasiadis K, Ragoussis J, Mathiopoulos KD - BMC Genet. (2014)

Functional annotation of differentially expressed sex-differentiation genes. In the left part of the figure, the gene expression levels of the differentially expressed sex-differentiation genes (Log2, fold change) are shown, as resulted from the RNA-seq analysis. The up-regulated genes in males are depicted in blue bars and the up-regulated genes in females in red bars. At the right part of the figure, the Gene Ontology (GO) classification of the same genes for the ontologies: Biological Process (BP), Molecular Function (MF), and Interpro (IP) protein domains is listed.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4255830&req=5

Figure 4: Functional annotation of differentially expressed sex-differentiation genes. In the left part of the figure, the gene expression levels of the differentially expressed sex-differentiation genes (Log2, fold change) are shown, as resulted from the RNA-seq analysis. The up-regulated genes in males are depicted in blue bars and the up-regulated genes in females in red bars. At the right part of the figure, the Gene Ontology (GO) classification of the same genes for the ontologies: Biological Process (BP), Molecular Function (MF), and Interpro (IP) protein domains is listed.
Mentions: In order to validate the differential expression of various genes observed after the RNAseq analysis of reproductive tissues of female and male olive flies, further functional analysis was performed for twelve genes that were differentially expressed in female accessory glands and spermathecae, on one hand, and male testes, on the other (Figure 4). These genes were selected on the basis of known involvement in sexual differentiation in other insects. Seven of them were selected from the 1238 significantly up-regulated in MALE (Table S4): kl2 (male fertility factor kl2), kl3 (male fertility factor kl3), kl5 (male fertility factor kl5), ory (occludin-related Y protein), fem-1 (sex-determining protein fem-1), gas8 (growth arrest specific protein 8) and lobo (lost boys). Three more genes that were up-regulated in MALE [ix (intersex), pbl (pebble) and hcf (host cell factor C1)] and two that were up-regulated in FEMALE [sox and pcp (pupal cuticle protein 78E)], albeit with lower statistical power (i.e., q>0.05) were also selected for further validation.

Bottom Line: Many years of experience from successful SIT applications in related species, primarily the Mediterranean fruit fly, Ceratitis capitata, demonstrated that efficient SIT protocols require the availability of fundamental genetic and molecular information.Furthermore, at least five olfactory-related genes were shown to be differentially expressed in the female and male reproductive systems analyzed.Finally, the expression profile of the embryonic serendipity-α locus and the pre-apoptotic head involution defective gene were analyzed during embryonic developmental stages.

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Background: Olive cultivation blends with the history of the Mediterranean countries since ancient times. Even today, activities around the olive tree constitute major engagements of several people in the countryside of both sides of the Mediterranean basin. The olive fly is, beyond doubt, the most destructive pest of cultivated olives. The female fly leaves its eggs in the olive fruit. Upon emergence, the larvae feed on the olive sap, thus destroying the fruit. If untreated, practically all olives get infected. The use of chemical insecticides constitutes the principal olive fly control approach. The Sterile Insect Technique (SIT), an environmentally friendly alternative control method, had been tried in pilot field applications in the 1970's, albeit with no practical success. This was mainly attributed to the low, non-antagonistic quality of the mixed-sex released insects. Many years of experience from successful SIT applications in related species, primarily the Mediterranean fruit fly, Ceratitis capitata, demonstrated that efficient SIT protocols require the availability of fundamental genetic and molecular information.

Results: Among the primary systems whose understanding can contribute towards novel SIT approaches (or its recently developed alternative RIDL: Release of Insects carrying a Dominant Lethal) is the reproductive, since the ability to manipulate the reproductive system would directly affect the insect's fertility. In addition, the analysis of early embryonic promoters and apoptotic genes would provide tools that confer dominant early-embryonic lethality during mass-rearing. Here we report the identification of several genes involved in these systems through whole transcriptome analysis of female accessory glands (FAGs) and spermathecae, as well as male testes. Indeed, analysis of differentially expressed genes in these tissues revealed higher metabolic activity in testes than in FAGs/spermathecae. Furthermore, at least five olfactory-related genes were shown to be differentially expressed in the female and male reproductive systems analyzed. Finally, the expression profile of the embryonic serendipity-α locus and the pre-apoptotic head involution defective gene were analyzed during embryonic developmental stages.

Conclusions: Several years of molecular studies on the olive fly can now be combined with new information from whole transcriptome analyses and lead to a deep understanding of the biology of this notorious insect pest. This is a prerequisite for the development of novel embryonic lethality female sexing strains for successful SIT efforts which, combined with improved mass-reared conditions, give new hope for efficient SIT applications for the olive fly.

Show MeSH
Related in: MedlinePlus