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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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Expression profile analysis during the early stages of embryogenesis. Expression levels of Α) Bosry-α and B) Bohid in individual eggs collected at different time points during embryonic development, as determined by qRT-PCR. Standard error of the mean of two biological replicates per time point is depicted in bars.
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Figure 8: Expression profile analysis during the early stages of embryogenesis. Expression levels of Α) Bosry-α and B) Bohid in individual eggs collected at different time points during embryonic development, as determined by qRT-PCR. Standard error of the mean of two biological replicates per time point is depicted in bars.

Mentions: Based on this sequence, B. oleae-specific primers were designed and the expression profiles of sry-α mRNA were studied by qRT-PCR analysis at different stages of B. oleae embryonic development. Eggs were collected throughout embryogenesis from the time of egg laying to larval hatching. The selected time points represented embryos at 0h, 4h, 8h, 9h, 10h, 11h, 12h, 15h and 18h after oviposition (Figure 8, panel A). This analysis revealed that sry-α mRNA is developmentally regulated during the second major event in the first stage of embryogenesis. It is initially present in large amounts just after oviposition (0h embryos), following a reduction in 4h embryos. The larger amounts of the transcripts among all time points examined were detected in 8h embryos. This suggests the presence of maternal mature transcripts which in turn are eliminated probably in the first event of maternal-to-zygotic transition (MZT). The subsequent wave of 'zygotic' activity requires zygotically synthesized transcripts [116]. In D. melanogaster as well as in C. capitata, sry-α is expressed only in the zygote [117]. However the retrieved B. oleae transcript shared greater amino acid similarity to the D. melanogaster CG8247 gene than to sry-α, as was also reported for the Ccsry-α like gene [118]. The orthologous CG8247 in D. melanogaster is characterized as a sry-α-like gene being also involved in cellular blastoderm formation. However, it is maternally inherited in contrast to sry-α, demonstrating a different mechanism of molecular control of transcription. In our case Bosry-α like gene seems to be maternally supplied in the embryos as mature transcripts. Previous studies have designated that the cellular blastoderm formation in C. capitata occurs within 9 h and 11 h after oviposition [115]. In accordance with C. capitata, a relative Tephritid species, we suggest that the cellurarization process in B. oleae during embryogenesis also occurs at 8h, since the sry-α transcripts were detected at higher levels during this time.


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)

Expression profile analysis during the early stages of embryogenesis. Expression levels of Α) Bosry-α and B) Bohid in individual eggs collected at different time points during embryonic development, as determined by qRT-PCR. Standard error of the mean of two biological replicates per time point is depicted in bars.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Expression profile analysis during the early stages of embryogenesis. Expression levels of Α) Bosry-α and B) Bohid in individual eggs collected at different time points during embryonic development, as determined by qRT-PCR. Standard error of the mean of two biological replicates per time point is depicted in bars.
Mentions: Based on this sequence, B. oleae-specific primers were designed and the expression profiles of sry-α mRNA were studied by qRT-PCR analysis at different stages of B. oleae embryonic development. Eggs were collected throughout embryogenesis from the time of egg laying to larval hatching. The selected time points represented embryos at 0h, 4h, 8h, 9h, 10h, 11h, 12h, 15h and 18h after oviposition (Figure 8, panel A). This analysis revealed that sry-α mRNA is developmentally regulated during the second major event in the first stage of embryogenesis. It is initially present in large amounts just after oviposition (0h embryos), following a reduction in 4h embryos. The larger amounts of the transcripts among all time points examined were detected in 8h embryos. This suggests the presence of maternal mature transcripts which in turn are eliminated probably in the first event of maternal-to-zygotic transition (MZT). The subsequent wave of 'zygotic' activity requires zygotically synthesized transcripts [116]. In D. melanogaster as well as in C. capitata, sry-α is expressed only in the zygote [117]. However the retrieved B. oleae transcript shared greater amino acid similarity to the D. melanogaster CG8247 gene than to sry-α, as was also reported for the Ccsry-α like gene [118]. The orthologous CG8247 in D. melanogaster is characterized as a sry-α-like gene being also involved in cellular blastoderm formation. However, it is maternally inherited in contrast to sry-α, demonstrating a different mechanism of molecular control of transcription. In our case Bosry-α like gene seems to be maternally supplied in the embryos as mature transcripts. Previous studies have designated that the cellular blastoderm formation in C. capitata occurs within 9 h and 11 h after oviposition [115]. In accordance with C. capitata, a relative Tephritid species, we suggest that the cellurarization process in B. oleae during embryogenesis also occurs at 8h, since the sry-α transcripts were detected at higher levels during this time.

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