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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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Validation profiles of differentially expressed sex-differentiation genes. Differentially expressed sex-differentiation genes of Figure 4 were further validated by qRT-PCR. Expression in male testes is depicted in blue color columns and expression in female accessory glands and spermathecae in red. Standard error of the mean of the two biological replicates is shown in bars. In all genes, except sox and pcp, expression in FEMALE and MALE was significantly different, as determined by t-test (p < 0.05).
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Figure 5: Validation profiles of differentially expressed sex-differentiation genes. Differentially expressed sex-differentiation genes of Figure 4 were further validated by qRT-PCR. Expression in male testes is depicted in blue color columns and expression in female accessory glands and spermathecae in red. Standard error of the mean of the two biological replicates is shown in bars. In all genes, except sox and pcp, expression in FEMALE and MALE was significantly different, as determined by t-test (p < 0.05).

Mentions: Quantitative RT-PCR confirmed the elevated expression of kl2, kl3, kl5 and ory in male testes of the olive fly (Figure 5). In Drosophila melanogaster, kl3 and kl5 (along with kl2) are known Y-linked fertility factors. The lack of kl3 or kl5 causes the loss of the outer arm of the sperm tail axoneme [59], a structure known to contain the molecular motor protein dynein in other organisms [60]. Indeed, Goldstein et al. showed in 1982 that sperm from mutant kl3- and kl5- males lack three discrete high molecular weight proteins with mobility similar to dynein heavy chains of Chlamydomonas reinhardtii and proposed that these fertility factors are the structural genes of three different dynein heavy chain proteins [61]. In 1993, Gepner and Hays sequenced part of kl5 and showed that it encodes an axonemal β-dynein heavy chain that is expressed in the testes [62].


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)

Validation profiles of differentially expressed sex-differentiation genes. Differentially expressed sex-differentiation genes of Figure 4 were further validated by qRT-PCR. Expression in male testes is depicted in blue color columns and expression in female accessory glands and spermathecae in red. Standard error of the mean of the two biological replicates is shown in bars. In all genes, except sox and pcp, expression in FEMALE and MALE was significantly different, as determined by t-test (p < 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Validation profiles of differentially expressed sex-differentiation genes. Differentially expressed sex-differentiation genes of Figure 4 were further validated by qRT-PCR. Expression in male testes is depicted in blue color columns and expression in female accessory glands and spermathecae in red. Standard error of the mean of the two biological replicates is shown in bars. In all genes, except sox and pcp, expression in FEMALE and MALE was significantly different, as determined by t-test (p < 0.05).
Mentions: Quantitative RT-PCR confirmed the elevated expression of kl2, kl3, kl5 and ory in male testes of the olive fly (Figure 5). In Drosophila melanogaster, kl3 and kl5 (along with kl2) are known Y-linked fertility factors. The lack of kl3 or kl5 causes the loss of the outer arm of the sperm tail axoneme [59], a structure known to contain the molecular motor protein dynein in other organisms [60]. Indeed, Goldstein et al. showed in 1982 that sperm from mutant kl3- and kl5- males lack three discrete high molecular weight proteins with mobility similar to dynein heavy chains of Chlamydomonas reinhardtii and proposed that these fertility factors are the structural genes of three different dynein heavy chain proteins [61]. In 1993, Gepner and Hays sequenced part of kl5 and showed that it encodes an axonemal β-dynein heavy chain that is expressed in the testes [62].

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